Unfolding molecular switches in plant heat stress resistance: A comprehensive review.

Vol.:(0123456789) 1 3 Plant Cell Reports https://doi.org/10.1007/s00299-021-02754-w

REVIEW Unfolding molecular switches in plant heat stress resistance:

A comprehensive review Saqlain Haider1 · Javed Iqbal1,2   · Sana Naseer1 · Muzzafar Shaukat1 · Banzeer Ahsan Abbasi1 · Tabassum Yaseen2 ·

Syeda Anber Zahra1 · Tariq Mahmood1,3 Received: 10 April 2021 / Accepted: 7 July 2021

© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021

Abstract Key message  Plant heat stress response is a multi-factorial trait that is precisely regulated by the complex web of transcription factors from various families that modulate heat stress responsive gene expression.

Abstract  Global warming due to climate change affects plant growth and development throughout its life cycle. Adds to this, the frequent occurrence of heat waves is drastically reducing the global crop yield. Molecular plant scientists can help crop breeders by providing genetic markers associated with stress resistance. Plant heat stress response (HSR), however, is a multi-factorial trait and using a single stress resistance trait might not be ideal to develop thermotolerant crops. Transcrip- tion factors participate in regulation of plant biological processes and environmental stress responses. Recent studies have revealed that plant HSR is precisely regulated by the complex web of transcription factors from various families. These transcription factors enhance plant heat stress tolerance by regulating the expression level of several stress-responsive genes independently or in cross talk with different other transcription factors. This review explores how signaling pathways trig- gered by heat stress are regulated by multiple transcription factor families. To our knowledge, we for the first time analyze the role of major transcription factor families in plant HSR along with their regulatory mechanisms. In the end, we will also discuss the potential of emerging technologies to improve thermotolerance in plants.

Keywords  Climate change · Cellular signaling · Epigenetics · Gene regulation · High temperature · Heat stress tolerance ·

Transcription factors Abbreviations DREB Dehydration responsive element binding transcriptional activator bHLH

Basic helix–loop–helix HSE Heat shock element OD

Oligomerization domain AHA Activator motif JA Jasmonic acid

AT Acquired thermotolerance HSF Heat shock factor

ET Ethylene ABA Abscisic acid MBF1c Multi protein bridging factor 1c

HSP Heat shock protein DBD DNA-binding domain UPR

Unfolded protein response DEG Differentially expressed genes

DPB3-1 DNA polymerase II subunit B3-1 ANN Annexin

IAA Indole acetic acid TSS Total soluble sugar SA

Salicylic acid MDA Melanodialdehyde JUB1 JUNGBRUNNEN 1

PCD Program cell death H3K4me2 Histone 3 lysine 4 di-methylation

Communicated by Manzer H. Siddiqui.

* Javed Iqbal

javed89qau@gmail.com * Tariq Mahmood

tmahmood@qau.edu.pk 1 Plant Biochemistry and Molecular Biology Laboratory,

Department of Plant Sciences, Quaid-I-Azam University,

Islamabad 45320, Pakistan 2 Department of Botany, Bacha Khan University,  Charsadda,

Khyber Pakhtunkhwa, Pakistan 3 Pakistan Academy of Sciences, Islamabad, Pakistan

Plant Cell Reports 1 3 AP2/ERF APETALA2/Ethylene Responsive Element

Factor LEA Late embryogenesis abundant proteins PIF4

Phytochrome interacting factor 4 phyB Phytochrome B

H3K4me Histone 3 lysine 4 methylation GRF7 Growth regulating factor 7

EIN2 Ethylene insensitive factor 2 ASF1 Anti silencing function 1

H3K56ac Histone 3 lysine 56 acetylation SPL Squamosa promoter-binding protein-like

H3K4me3 Histone 3 lysine 4 tri-methylation Introduction

Being sessile organisms, plants rely on various environmen- tal cues for growth and development. The ambient tempera- ture fluctuates considerably during different seasons and dur- ing the day and night cycle (Bratzel and Turck 2015). All the biological processes in plants are dependent on optimum temperature (Lippmann et al. 2019). The temperatures above this range is considered heat stress (HS) (Hatfield and Prue- ger 2015; Sarwar et al. 2019). Wahid et al. (2007) described

HS as rise in temperature above threshold value for a consid- erable period of time causing irreversible damage to plants.

Generally temperature 10–15 °C above optimum range is considered as HS. HS is responsible for damages to agri- cultural production estimated at billions of dollars (Zhang et al. 2019a). The global mean temperature will increase

2–4 °C by the end of twenty-first century (Stocker 2014).

The world’s food demand in 2050 would be 70% more than it is today, and this increase will be particularly greater in many low-income countries where food security is already a challenging issue (UNDESA 2015). The anticipated rise in global temperature together with the other abiotic and biotic stresses will potentiate the challenges for plant species (Lippmann et al. 2019). Under these conditions, a major goal of modern plant research is to expand germplasm resource and develop strategies that would ensure adequate food pro- duction to satisfy the need of ever growing human popula- tion (Fragkostefanakis et al. 2015).

HS affects a variety of physiological and biochemical processes in plants (Zhao et al. 2021). These include cell growth, division and differentiation, photosynthesis, res- piration, water potential, transpiration, nutrient uptake and transport (Wahid et al. 2007; Hasanuzzaman et al. 2013;

Giri et al. 2017; Lippmann et al. 2019). At cellular level, HS results in excessive production of reactive oxygen species (ROS) creating metabolic imbalance, triggers protein dena- turation and deformation which creates proteotoxic stress, disrupts membrane stability, and cytoskeleton integrity leading to collapse of cellular structure (Mittler et al. 2012;

Hasanuzzaman et al. 2013; Hayes et al. 2021; Haider et al.

2021a). To counter the negative effects associated with high temperatures, plants evolved sophisticated signaling net- works which allow them to perceive rise in ambient tempera- ture and then activate a defense response through changes in their transcriptome, proteome and metabolome (Zhu 2016;

Raza 2020; Haider et al. 2021a; Sarwar et al. 2018; Kaur et al. 2018). In the past two decades, considerable progress has been made in unraveling the role of HS-responsive tran- scription factors (TFs), HS-inducible genes, small RNAs, and chromatinmodifications in plant HS tolerance. (reviewed by Lämke and Bäurle 2017; Zhao et al. 2021; Haider et al.

2021a, b). However, an extensive literature review indicated that when studying plant tolerance to high temperature, only the function of heat shock transcription factors (HSFs) has been reviewed. So, to our knowledge, we, for the first time comprehensively analyze the role of major TF families in addition to HSFs in plant HSR.

The transcriptional regulation of genes is a key step whereby the TFs bind to cis-acting elements in the promoter sequence of target genes and may activate or repress their expression (Meshi and Iwabuchi 1995; Scharf et al. 2012).

Higher plant genomes devote ~ 7% of their coding capacity to TFs (Rushton et al. 2008). The expression pattern of a specific gene can be regulated by a single TF or by multiple

TFs. From the context of protein structure, TFs consists of four important domains. The DNA-binding domain (DBD) is usually located at the N-terminal of proteins. The DBD makes contacts with the DNA in a sequence-dependent man- ner. At the C-terminal, a transcriptional regulatory domain is located which enables the interaction of TFs with other proteins/factors. The nuclear localization signal (NLS) and nuclear export signal (NES) are responsible for intracellu- lar distribution of TFs (Meshi and Iwabuchi 1995; Scharf et al. 2012; Li et al. 2019 b). TFs are classified into differ- ent families based on specificity of DNA binding region (Li et al. 2019 b). TFs are core component of stress-induced signaling pathway, and play key role in the conversion of stress signal perception to stress-responsive gene expres- sion (Dubos et al. 2010; Rushton et al. 2010; Mizoi et al.

2012; Puranik et al. 2012; Andrási et al. 2021). The ability of plants to acclimate to adverse stress events is insepara- ble from the expression of TF-regulated stress-responsive functional genes (Li et al. 2019 b). HSFs are considered as central regulators of plant HSR (Yoshida et al. 2011).

However, extensive research in the past decade suggests that apart from HSFs, several members of other TF fami- lies such as WRKY (named due to conserved WRKYGQK motif), MYB (v-myb avian myeloblastosis viral oncogene homolog), NAC (Petunia NAM, Arabidopsis ATAF1/2 and

CUC2), DREB (dehydration responsive binding transcrip- tional activator) and bHLH (basic helix–loop–helix) play key role in plant acclimation to high temperature by regulating

Plant Cell Reports 1 3 the expression of suite of HS-inducible genes (Koini et al.

2009; El-Kereamy et al. 2012; Fang et al. 2015; Guo et al.

2015; Zhao et al. 2017; Wang et al. 2018 b). These TFs col- lectively function to enhance plant HS tolerance by forming a complex regulatory network, the outcome of which is plant survival under adverse environmental conditions (Ohama et al. 2017; Haider et al. 2021a). The current article will discuss in detail about major TF families and reports on their role in regulation of resistance to HS. We will comprehen- sively analyze and review prospects of developing thermo- tolerant crop plants through modulation of TF networks. In the scenario where human population is expected to reach almost 10 billion by mid-2050, coupled with the continuous rise of global temperature, breeding for thermotolerant crops is necessary to meet increasing demand of world nutrition (UNDESA 2015).

Major TF families in plants and their role in regulation of plant HSR

When plants are stressed by high temperatures, they effec- tively regulate the expression of functional genes through multiple signaling networks and initiate a series of biochem- ical and physiological changes inside the cells. The outcome of these alterations is plant survival under HS conditions (Mittler et al. 2012; Ohama et al. 2017; Haider et al. 2021a).

The plant HSR is a highly sophisticated and complex process that involves various cellular compartments, multiple sign- aling networks, and multiple gene products (Ohama et al.

2017; Haider et al. 2021a).

Heat stress‑induced transcriptional cascade and signaling mechanisms in plants

When plants are exposed to HS, a suite of molecular altera- tions are initiated (for comprehensive see Ohama et al. 2017;

Hayes et al. 2021; Haider et al. 2021a; Siddiqui et al. 2018).

This is characterized by the rapid induction of HSFs and heat shock proteins’ (HSPs) expression. Both the HSFs and HSPs play major role in HSR and induce the thermotolerance (Ohama et al. 2017). However, the induction of HSFs/HSPs depends on some upstream factors (Mittler et al. 2012). It is proposed that the plant HSR is initiated by events that take place inside the plasma membrane (PM) following HS (Saidi et al. 2009). Even though the identity of primary HS sen- sors is unknown in plants, the cyclic nucleotide gated chan- nels (CNGCs) have been proposed as primary HS sensor in land plants. This is supported by fact that CNGC mutants failed to activate the expression of several HSFs/HSPs and showed reduced survival and fitness under HS conditions (Finka et al. 2012; Tunc-Ozdemir et al. 2013; Finka and

Goloubinoff 2014; Cui et al. 2020). HS changes the fluidity of plasma membrane which opens specific calcium channels (Saidi et al. 2009). The opening of CNGCs facilitates the inward flow of calcium ­(Ca2+) ions inside the cell (Saidi et al. 2009). The ­Ca2+ influx inside the cell can activate multiple signaling pathways (reviewed by Reddy et al. 2011;

Mittler et al. 2012; Li et al. 2018; Haider et al. 2021a).

The HS-induced transcriptional cascade is strictly regu- lated at the level of transcription factor expression in Arabi- dopsis thaliana (Ohama et al. 2016). Under non-stress conditions, HSFA1s activities are repressed through its inhibitory association with HSP70/HSP90 (Andrási et al.

2021). Exposure to HS triggers protein deformation/dena- turation inside the cells (Fig. 1). Both HSP70/HSP90 act as molecular chaperons and bind to denatured proteins to restore protein homeostasis inside the cell (Scharf et al.

2012; Jacob et al. 2017; Andrási et al. 2021). The HSFA1s are then activated through a series of sequential events and initiate a transcriptional cascade (Ohama et al. 2017; Haider et al. 2021a). The HSFA1s are master regulators of plant HS response and activate the expression of several TFs under

HS. HSFA1s rapidly induce the expression of HSFA2,

HSFA3, HSFA7s, HSFBs, dehydration-responsive binding transcriptional activator 2A (DREB2A) and multi protein bridging factor 1c (MBF1c) (Fig. 1) (Ohama et al. 2017).

Both HSFA1a and HSFA1b are essential for HS-responsive gene expression during the initial phase (Li et al. 2010a).

HSFA1d and HSFA1e regulate expression of HSFA2 and are considered as a key regulators of HSF signaling network in response to environmental stresses (Nishizawa-Yokoi et al.

2011). Under normal conditions, the expression of HSFA2 is undetectable. However, after HS, HSFA2 becomes the most strongly induced HSF and prolongs the acquired ther- motolerance (AT) in Arabidopsis through sustained expres- sion of HSPs (Nishizawa et al. 2006; Schramm et al. 2006).

HSFA2 and/or HSFA1s activate HSFA3, HSFA7a and HSFA7b (Fig. 1) (Liu and Charng 2013). Under normal con- ditions, growth-regulating factor 7 (GRF7) directly binds to

GRF7-targeting cis-element ‘5TGT​CAG​G3’ at the promoter of DREB2A genes and represses it expression (Kim et al.

2012). DREB2A trans-activates the expression of HSFA3 through a co-activator complex consisting of DNA polymer- ase II subunit B3-1 (DPB3-1), nuclear factor subunit YA2 (NF-YA2) and nuclear factor subunit YB3 (NF-YB3) by binding to two dehydration-responsive element (DRE) bind- ing sites present in the promoter of HSFA3 gene (Yoshida et al. 2008; Sato et al. 2014). DREB2C has also been shown to activate HSFA3 expression under HS (Chen et al. 2010).

HSFA3 over-expression induces the activation of HSFA1e,

HSFA7b and HSFB2b (Fig. 1) (Yoshida et al. 2008). HS results in overproduction of ROS (Kohli et al. 2019) and it has been proposed that certain HSFs might act as a ROS sen- sors (Miller and Mittler 2006). For example, both HSFA4a and HSFA8 act as ROS sensors under HS conditions (Qu et al. 2013). Class B HSFs are transcriptional repressor and

Plant Cell Reports 1 3 negatively regulate the activities of HSFs (HSFA2, HSFA7) and HSPs (HSP101, HSP70). Interestingly, HSFBs func- tion downstream in transcriptional cascade of HSFA1s, thus forming a regulatory loop which fine tunes the expression of HS inducible TFs in Arabidopsis and Solanum lycoper- sicum (Fig. 1) (Hahn et al. 2011; Ding et al. 2020). HSFA4 is induced by multiple stress conditions, including HS, and regulate the level of ROS through APX1. HSFA5 interacts with HSFA4 and inactivates it by inhibiting its DNA bind- ing activity (Baniwal et al. 2007). Therefore, it has been suggested that HSFA4 could be anti-apoptotic factor and

HSFA5 could be pro-apoptotic factor (Fragkostefanakis et al.

2015). Some HSFs participate in plant HSR independent of

HSFA1 signaling pathway (Ohama et al. 2017). For exam- ple, HSFA9 is expressed specifically in seeds independent of HSFA1-signaling pathway (Fig. 1) (von Koskull-Döring et al. 2007).

Apart from HSFs and DREBs, a number of other factors from MBF1c, WRKY, MYB, NAC and bZIP TF fami- lies have been reported to be essential for expression of

Fig. 1    Signaling cascade activated in response to heat stress and its regulation by transcription factors in plants. Under non-stress con- ditions, HSFA1 activity is repressed by HSP70, HSP90 complex.

However, after heat shock, HSP70/90 are detached and bind to mis- folded proteins, allowing HSFA1s to become transcriptionally active.

The activated HSFA1s then induce the expression of HSFs, DREBs and MBF1c TFs. The NAC019 directly binds to the promoter of

HSFA1b and drives its expression. Similarly, the overexpression of RCF2 increases the expression level of DREBS and HSFs. How- ever, whether RCF2 directly binds to the promoter elements of these genes is unclear yet. HsfA2 and/or HsfA1s induce the expression of

HsfA3, HsfA7a and HsfA7b. The HSFBs are transcriptional repres- sors and repress the activities of HSFA1s and HSFA2 under HS.

HSFA3 over-expression induces HSFA1e, HSFA7b and HSFB2b.

Some HSFs like HSFA9, HSFA4 and HSFA5 function independently of HSFA1 signaling pathway. Certain HSFs such as HSFA4a and

HSFA8a can directly sense increasing ROS levels inside the cells.

DREB2A is negatively regulated by GRF7, but under HS, GRF7 is dissociated from regulatory region of DREB2A. HSFA1, MBF1c and

JUB1 activate DREB2A. Overexpression of NAC2L and MYB80 elevates the expression of DREB2A under HS. MYB80 also elevates the expression of HSFA6b under HS. A trimer of DPB3-1, NF-YA2 and NF-YB3 confers target-specific selectivity to DREB2A. Both

DREB2A and DREB2C trans-activate the expression of HSFA3 and other HS-responsive genes. NTL4, a membrane-bound NAC TF, trig- gers ­H2O2 accumulation which then promotes its proteolytic release from membrane. Heat stress results in overproduction of ROS which in turn could activate MBF1c or different HSFs. MBF1c functions up-stream of several TFs and hormones and its activation initiates the expression of WRKYs through salicylic acid or ethylene-dependent pathways. Annexin genes encode ­Ca2+ regulated membrane-binding proteins and play role in ­Ca2+ influx. Annexin activity is regulated at transcriptional level by MYB30. The ER-UPR involves bZIP28, bZIP60, IREI and BiP. Under HS, IRE1 activates the alternative splicing of bZIP60 which activates UPR genes. Similarly, bZIP28 is detached from BiP under HS. bZIP28 is then processed in Golgi apparatus by S1P and S2P. Solid arrows represent factors for which there is direct experimental evidence while dashed arrows represent factors which need further confirmation

Plant Cell Reports 1 3 HS responsive genes. NAC TFs are plant-specific regu- latory proteins and participate in regulation of various stress responses (Puranik et al. 2012). Guan et al. (2014) reported that protein phosphatase RCF2, dephosphoryl- ates NAC TF, NAC09, and is required for HS-responsive gene regulation and thermotolerance. Under HS, reduced

DREB2A, DREB2C and HSFA3 expression was observed in rcf2 mutants during the reproductive stage. The NAC09 was shown to directly bind to CATGT sequence present in promoters of HSFA1b, HSFA6b, HSFA7a, and HSFC1 under HS and positively regulate their expression (Fig. 1) (Guan et al. 2014). Furthermore, reduced induction and accumulation of HSFs and HSPs was observed in nac019 mutants. JUNGBRUNNEN1 (JUB1) directly binds to the promoter sequence of DREB2A gene under HS condi- tions (Shahnejat-Bushehri et al. 2012; Wu et al. 2012).

Guo et al. (2015) reported that the overexpression of

TaNAC2L elevates the expression of HS marker genes such as AtHSFA1, RD29A, RD17, LEA and DREB2A and improves HS tolerance of wheat. Lee et al. (2014) reported that HS induces Arabidopsis NTL4; a membrane bound NAC TF, via ABA pathway. The heat-induced expression of NTL4 requires ABA and SA. NTL4 triggers

­H2O2 accumulation under HS, but interestingly, ­H2O2 pro- duced due to NTL4 signaling, also promotes its proteolytic release from membrane, constituting a positive feedback loop in inducing PCD. WRKYs constitute a diverse group of regulatory proteins with essential role for plant biotic and abiotic stress responses (Rushton et al. 2010). Li et al. (2010 b) reported that wrky39 mutants showed reduced expression of HSFA2, HSFB1, HSP70, HSP101, APX1, and Zat10 (well known HS marker genes). In addition,

Arabidopsis WRKY25, 26, 33 were shown to be essential for HS tolerance (Li et al. 2011). He et al. (2016) reported

TaWRKY33 overexpression increases Arabidopsis HS tolerance by activating the expression of several genes including DREB2B. MYB TFs play a major role in regu- lation of plant HSR. TaMYB80 overexpression increase the expression of DREB2A and HSFA6b through absci- sic acid (ABA) pathway (Fig. 1) (Zhao et al. 2017). In response to oxidative stress, the ANNEXIN (ANN) genes encode ­Ca2+ controlled membrane-binding proteins that modulate cytosolic calcium signatures (Laohavisit et al.

2010). MYB30 regulates cytosolic ­Ca2+ concentration under oxidative stress and HS conditions by repressing the expression of ANN1 and ANN4 genes, while mutants exhibit up-regulation of number of ANN genes (Fig. 1) (Liao et al. 2017). MBF1c is an evolutionary conserved protein and is essential for thermotolerance (Suzuki et al.

2011). MBF1c functions upstream of DREBs, some HSFs,

WRKYs, salicylic acid (SA) and ethylene (ET) insensi- tive factor (EIN2) (Zanetti et al. 2003; Suzuki et al. 2008,

2011; Li et al. 2010 b). In mbf1c mutants, the expression of DREB2A and HSFBs was reduced under HS (Suzuki et al. 2011). Yoshida et al. (2011) reported that HSFA1 regulate HS-induced MBF1c expression. WRKY39 overex- pression increased the HS-induced expression of MBF1c (Li et al. 2010 b).

Similarly, the induction of unfolded protein response (UPR) in endoplasmic reticulum (ER) is essential step in plant HSR (Zhu 2016; Zhao et al.2021). ER plays a key role in protein synthesis, folding and secretion (Anelli and

Sitia 2008). All the proteins are first transported to ER for biological activation where they go through a series of post- translational modifications (Howell 2013). As mentioned above, HS results in protein misfolding. The presence of unfolded proteins inside the ER is perceived as “ER stress” (Zhu 2016). Two UPR pathways are functional inside plant cells which are responsible for ER stress perception and signal transduction (Malini et al. 2020). Inositol-requiring enzyme 1 (IRE1) is an evolutionary conserved ER sensor among eukaryotes. Its activities are repressed by an ER localized molecular chaperone, BiP. However, IRE1 is dis- sociated from BiP under ER stress allowing IRE1 to dimer- ize and execute the stress-induced alternative splicing of bZIP60 mRNA (Schwarz and Blower 2016). bZIP60 is an membrane-bound TF. However, the bZIP60 that arises due to alternative splicing, lack transmembrane domain and gain entry inside the nucleus to translate UPR genes (Nagashima et al. 2011). Interestingly in maize, bZIP60 links UPR with

HSR (Li et al. 2020). The bZIP60 is essential for expres- sion of HSFs and its knockout compromised the plant HSR.

Another major player in ER-UPR is a membrane bound

TF, bZIP28. The N-terminal of bZIP28 is oriented towards cytosol while C-terminal towards ER lumen (Srivastava et al. 2014). Bip also repress the activities of bZIP28 under normal conditions through interaction with the C-terminal region of protein. However, under stress, BiP is dissociated from bZIP28. The release bZIP28 is then activated and gain access to Golgi apparatus. Here, it is cleaved by site-1 pro- tease (S1P) and site-2 protease (S2P) (Iwata et al. 2017).

The resulting protein enters nucleus and activates the UPR genes. The ER-UPR functions to limit proteins misfolding, reduce the protein translocation to ER and upregulate genes whose products participate in protein renaturation/refolding (Zhu 2016).

TFs for crop thermotolerance In recent years, significant progress has been made towards functional characterization of HS-inducible TFs in model plants and crops. Furthermore, advances in genomics has allowed the identification of novel TFs. This in turn, pro- vides an opportunity to harness the potential of these molec- ular regulators to develop thermotolerance in crop plants.

Plant Cell Reports 1 3 HSFs Plant HSFs are major components of signal-transduction pathways which play essential role in proper functioning of the cell (Jacob et al. 2017). Different environmental stresses may alter protein configuration and impede protein func- tioning (Scharf et al. 2012). In this regard, HSFs play an essential role by acting as a buffer to limit protein misfolding and resolve aggregates (Jacob et al. 2017). Under HS, due to accumulation of misfolded proteins, HSPs are detached from their inhibitory association with HSFs and bind to unfolded/ misfolded proteins (Voellmy and Boellmann 2007). The resulting HSFs then gain entry inside the nucleus to initiate

HSR (von Koskull-Döring et al. 2007).

Based on phylogenetic analysis, plant HSFs are divided into three classes: A, B and C. HSFs have a conserved struc- ture. Close to N-terminal, the DNA-binding domain (DBD) is responsible for binding with the so-called ‘‘heat shock elements’’ (HSE) present in the promoters of HS-induci- ble genes (Scharf et al. 2012). The HSEs have a consensus sequence (5′-AGAAnnTTCT-3′), which is highly conserved among eukaryotes (Scharf et al. 2012). The OD (HR-A/B) consists of hydrophobic heptad repeats and is separated from

DBD by a flexible linker. Both class B and C HSFs have no activator activity of their own (Baniwal et al. 2004). Here, we will briefly discuss recent advances in deciphering the role of HSFs in plant HS tolerance (Table 1). For detailed review on function of HSFs, reader is referred to published reviews by Fragkostefanakis et al. (2015), Guo et al. (2016),

Jacob et al. (2017) and Andrási et al. (2021).

Role in heat stress tolerance Among HSFs, class A HSFs are the key regulators of plant

HSR, class B HSFs as transcriptional repressors while class C HSFs are transcriptional activator like class A.

However, class C HSFs cannot activate transcription on their own (Jacob et al. 2017). HSFA1s are necessary for basal thermotolerance and acquired thermotolerance (AT) (Jacob et al. 2017). HSFBs are essential for proper recovery from HS (Jacob et al. 2017). Yoshida et al. (2011) reported that Arabidopsis HSFA1a, b, d and e trigger plant HSR.

Expression of chaperons and TFs was globally and drasti- cally impaired in knockout mutants and hence resistance to HS. HSFA1 is master regulators of HSR in tomato, and

HSFA1 co-suppression lines showed impair thermotolerance (Mishra et al. 2002). Overexpression of HSFA1 leads to two- to threefold increase in HS-induced synthesis of HSFs and

HSPs in the leaves and the HS-independent expression of

HSFs and HSPs in the pericarp. A defect in seed develop- ment was observed in hsfa1abde quadruple mutants. These seeds exhibit > 20% abortion and were unable to adapt to mild HS (Liu and Charng 2013). HSFA1b enables plants to adjust their growth and develop biologically under various stress conditions including HS to complete their life cycle (Albihlal et al. 2018). Albihlal et al. (2018) identified 952

HSFA1b target genes of which at least 85 were associated with development. Authors propose that HSFA1b deter- mines reproductive fitness by influencing seed yield.

HSFs and hormones play regulatory role in plant HSR (Baniwal et al. 2004). Recently, it is reported that HSFA1b regulates thermotolerance through TaOPR3 and jasmonic acid (JA) singling pathway in wheat and Arabidopsis.

Reduction in JA level was detected in opr3 mutants. Further analysis indicated that JA confers tolerance to HS by regu- lating DREB2A expression (Tian et al. 2020). Arabidopsis

HSFA1d improves thermotolerance in Solanum tuberosum possibly by elevating expression of HSP70 gene (Shah et al.

2020). HSFA2 is most highly induced HSF and is critical for AT (Jacob et al. 2017). Disruption of HSFA2 reduces expression of HSP genes and ultimately AT (Charng et al.

2007). During long-term HS events, HSFA2, HSFA3 and

HSFA7a, together with HSFA1 or separately, are required to prolong/extend HSR (Jacob et al. 2017). Recently, HSFA2 has been associated with epigenetic modification under HS (Lämke et al. 2016). Xin et al. (2017) reported that overex- pression of LlHSFA2b enhances HS and oxidative stress tolerance in Arabidopsis seedlings. Expression of AtHSFA2,

AtHSFA7a and AtHSP70-5, AtHSP25.3-P and AtApx2 (puta- tive downstream target genes of LlHSFA2b) was increased under non-stress conditions in LlHSFA2b overexpression lines. TaHSFA2–10 improves basal and AT in advanced developmental stages of wheat (Guo et al. 2020). OsHSF7 is involved in basal thermotolerance in rice (Liu et al. 2009).

The transcription of several HSPs increased many fold in

OsHSF7 overexpression lines. ZmHSF04 increases plant resistance to HS and salt stress by up-regulating the expres- sion level of specific HSPs and stress-related genes and is critical for short-term AT (Jiang et al. 2018).

TaHSFA6e modulates tolerance of wheat to HS and drought during pollination and grain filling stages (Kumar et al. 2018). Duan et al. (2019) performed genome-wide identification, phylogenetic analysis and expression profiling of wheat HSFs under abiotic stress events. TaHSFs showed class-specific, tissue-specific and organ-specific expression.

ZmHSF12 overexpression improves both basal and AT in

Arabidopsis by elevating the expression of HSPs (Li et al.

2019a). Several studies have shown that HSFs participate in multiple stress responses and hence are excellent candidate genes for development of stress resilient crops (Jacob et al.

2017; Andrási et al. 2021).

WRKY TFs WRKY TFs are present exclusively in plants and are regula- tors of many biological processes. WRKYs are involved in

Plant Cell Reports 1 3 Table 1   A brief overview on the role of transcription factors is plant heat stress tolerance

Transcription factor Source species Transgenic plant

Comments References HSFs SlHSFA1 Tomato Tomato Overexpression lines showed enhanced thermotolerance and elevated expression levels of HSFs, HSPs.

Contrastingly, HS-induced synthesis of chaperons and HSFs was strikingly reduced in co-suppression mutants.

Moreover, co-suppression plants and their fruits were extremely sensitive to high temperatures

Mishra et al. (2002) AtHSFA1a,b,d,e Arabidopsis Arabidopsis

HSFA1-type proteins are positive regu- lators of plant responses to HS and are critical for normal plant growth.

These proteins regulate the expres- sion of DREB2A and the expression of DREB2A completely disappeared in quadruple knockout mutants

Yoshida et al. (2011) AtHSFA2 Arabidopsis Arabidopsis

HSFA2 extends AT by sustaining the expression of HSP genes. The

HSFA2 is responsible for extension, but not induction of AT. HSFA2

KO mutants were more sensitive to severe HS than WT plants, following pre-treatment at 37 °C

Charng et al. (2007) Arabidopsis Arabidopsis HSFA2 is responsible for chromatin modification and sustained activation of HS-related genes by methylation (H3K4me2 and H3K4me3) of target genomic loci

Lämke et al. (2016) AtHSFA1d Arabidopsis Tomato Transgenic lines exhibited sixfold higher expression of HSP70 gene under HS. Both chlorophyll a and b were decreased in WT plants. WT plants turned yellow after HS expo- sure. No such effects were observed in overexpression lines. Overexpres- sion lines accumulated higher proline content and were more adaptive to

HS conditions compared to WT plants Shah et al. (2020)

LlHSFA2b Lily Arabidopsis LlHSFA2b is induced by HS and ­H2O2, but not by drought, ABA or salt treatment. Yeast one-hybrid system showed that LlHSFA2b lacks trans- activational activity and LlHSFA2b interacts with either AtHSFA1d or

AtHSFA2. Overexpression lines showed enhance tolerance to HS and oxidative stress

Xin et al. (2017) TaHSFA2–10 Wheat Arabidopsis Transgenic plants overexpressing

TaHSFA2–10 showed higher survival rate, growth vigor and had higher chlorophyll content. Reduced thermo- tolerance was observed in mutants

Guo et al. (2020) OsHSF7 Rice Rice The expression of OsHSF7 is rapidly induced by HS. Transgenic lines showed higher basal thermotolerance but not AT

Liu et al. (2009)

Plant Cell Reports 1 3 Table 1   (continued) Transcription factor

Source species Transgenic plant Comments References

TaHSFA6e Wheat Wheat In thermotolerant cultivars, there was an increase in catalase, guaiacol peroxidase, total antioxidant capacity and a decrease in lipid peroxidation

Kumar et al. (2018) ZmHSF04 Maize Arabidopsis ZmHSF04 is strongly induced by HS/ salt treatment. Transgenic lines showed significantly higher germina- tion rate, better leaf opening and higher cotyledon greening rates than

WT plants. In addition, overexpres- sion of ZmHSF04 increased sensitiv- ity to exogenous ABA

Jiang et al. (2018) ZmHSF12 Maize Arabidopsis ZmHSF12 expression is induced after heat shock and ZmHSF12 is expressed in many maize organs.

Arabidopsis seedlings showed improved basal thermotolerance and AT. The expression of HSPs, chlorophyll content and survival rate was significantly higher in transgenic lines

Li et al. (2019a) WRKY OsWRKY11 Rice Rice After prolonged heat and drought stress treatment, all WT plants died while transgenic lines survived and showed resistance to both HS and drought

Wu et al. (2009) AtWRKY25,26,33 Arabidopsis Arabidopsis

After 1 h of HS treatment, the transcripts of WRKY25 WRKY26 increased many fold. Contrarily,

WRKY33 transcripts were down- regulated. Results indicate functional redundancy between these three pro- teins and their simultaneous involve- ment in regulation of resistance to

HS. Expression of HS-marker genes HSFA2, HSFB1, HSP70, HSP101,

APX1 and Zat10 was reduced in mutant lines Li et al. (2011)

AtWRKY39 Arabidopsis Arabidopsis Transgenic lines showed higher ger- mination and survival rate. Expres- sion of two SA-related genes, e.g.

MBF1c and PR1 was increased in overexpression lines. Treatment with

MeJA induced WRKY39 expression and WRKY39 expression was lower in JA and SA mutants, indicating both these hormones are required for WRKY39 expression. The results showed that WRKY39 positively regulates SA-related HS defense genes and confer thermotolerance independently of HSPs and heat- induced oxidative stressed pathways

Li et al. (2010 b) TaWRKY1 and TaWRKY33 Wheat Arabidopsis

Transgenic lines showed faster germi- nation rate and promoted root growth under multiple stress conditions.

Results suggest that TaWRKY33 might have roles in interaction of the

ABA and MeJA signaling pathways He et al. (2016) Plant Cell Reports

1 3 Table 1   (continued) Transcription factor Source species

Transgenic plant Comments References ZmWRKY106 Maize

Arabidopsis Expression of several HS-responsive genes, for example HSP90, NCED3,

CuZnSOD, NCED6, RD29A and DREB2A was considerably high in transgenic lines. Transgenic lines showed high expression of key ROS scavenging genes SOD, POD, CAT​ and improved thermotolerance

Wang et al. (2018a) AtBAG7/At WRKY29 Arabidopsis Arabidopsis

AtBAG7 is SUMOylated upon HS which is essential for interaction with

WRKY29 and HS tolerance Li et al. (2017) CaWRKY40 Pepper

Tobacco CaWRKY40 expression can be induced by hormones such as SA, JA, ET and overexpression leads to modified expression of heat response associ- ated and PR-genes

Dang et al. (2013) AtWRKY30 Arabidopsis Wheat Overexpression lines exhibit higher plant growth, biomass, gas-exchange attributes, chlorophyll content, rela- tive water content, proline content and antioxidant enzymes' activity

El-Esawi et al. (2019) MYB AtMYB68 Arabidopsis Arabidopsis

AtMYB68 is associated with increased lignin content and greater root biomass production. myb68 mutants show reduction in growth as com- pared to WT plants. However, there was no significant difference in phenotype between knockout mutants and WT plants

Feng et al. (2004) OsMYB55 Rice Rice Transgenic lines showed higher coleoptile length, higher plant height, greater plant and root biomass, leaf sheath length and yield quantity than

WT under HS. Moreover, transgenic lines showed higher glutamic acid,

GABA, arginine and proline content under HS and thus increased resist- ance to HS

El-Kereamy et al. (2012) OsMYB55 Rice Maize Transgenic lines showed better germination rate, higher chlorophyll content, plant height, higher water potential, lower leaf temperature and higher photosynthetic activity under

HS and drought conditions. This study provides an insight into func- tions of MYB TFs under combination of heat and drought stress

Casaretto et al. (2016) LeAN2 Tomato Tomato After HS treatment, difference in germination rate were obvious in

35S:LeAN2 lines and WT plants. The decrease of maximal photochemical efficiency of photosystem II (Fv/Fm) and net photosynthetic rate in trans- genic plants were considerably high than WT plants. Transgenic lines had increased membrane stability and less ROS content

Meng et al. (2015)

Plant Cell Reports 1 3 Table 1   (continued) Transcription factor

Source species Transgenic plant Comments References

TaMYB80 Wheat Arabidopsis Transgenic lines showed decreased water loss, slower wilting, higher germination and survival rate than

WT plants Zhao et al. (2017) AtMYB30 Arabidopsis Arabidopsis

MYB30 is a regulator of cytosolic ­Ca2+ in response to oxidative stress and

HS. MYB30 repress the expression of ANN1 and ANN4 genes

Liao et al. (2017) AtMYB59 Arabidopsis Arabidopsis

AtMYB59 is a negative regulator of ­Ca2+ signaling and homeostasis.

Higher levels of cytosolic ­[Ca2+]cyt were detected in roots cells

Fasani et al. (2019) NAC AtNTL4 Arabidopsis Arabidopsis

The heat-induced expression of NTL4 requires ABA and SA. The NTL4 together with ­H2O2 form a regulatory loop which induce PCD

Lee et al. (2014) OsSNAC3 Rice Rice The overexpression of SNAC3 stabi- lizes plasma membrane, reduced membrane lipid peroxidation, decreased ­H2O2 content, enhanced water retention capacity and improved spikelet fertility and shoot length. On the other hand, suppres- sion of SNAC3 by RNAi leads to weaker tolerance to heat, drought and oxidative stress

Fang et al. (2015) JUB1 Arabidopsis Arabidopsis Transgenic lines showed decrease water loss, slower wilting, higher germination and survival rate than

WT plants. Overexpression of JUB1 induces expression of several ROS- responsive genes, including HSPs and glutathione S-transferase genes and elevates trehalose content

Wu et al. (2012) Overexpression of JUB1 upregulates the expression of many HSFs, HSPs and ROS scavenging genes in both primed and unprimed plants sub- jected to HS. A lesser survival rate was observed in jub1 mutants. The expression of JUB1 closely resembles expression pattern of HSFA2, HSA32, well-known thermomemory genes

Shahnejat-Bushehri et al. (2012) OsNTL3 Rice Rice ntl3 mutants were more sensitive to

HS, showed increase ROS content and higher electrolyte leakage than

WT plants Liu et al. (2020) Plant Cell Reports 1 3

Table 1   (continued) Transcription factor Source species

Transgenic plant Comments References AtNAC019 Arabidopsis

Arabidopsis NAC019 directly binds to CATGT sequence in promoters of HSFA1b,

HSFA6b, HSFA7a and HSFC1.

Under HS, reduced induction of HSFs and DREBs was observed in rcf2 mutants and at reproduc- tive stage, reduced induction and accumulation of HSFs and HSPs was observed in nac019 mutants. In short, RCF2 overexpression increases the expression level of stress-related genes and thus improves thermotoler- ance

Guan et al. (2014) TaNAC2L Arabidopsis Arabidopsis

TaNAC2L is induced by HS and regulates stress-responsive gene expression. Expression of marker genes such as AtHSFA1, RD29A,

RD17, LEA and DREB2A was considerably high in 35S:TaNAC2L lines. TaNAC2L protein is expressed at low level in transgenic lines; how- ever, after HS, a clear transcription pattern was detected in these lines.

TaNAC2L protein is degraded via ubiquitin proteasome 26S pathway independent of DRIP1

Guo et al. (2015) AtNAC78 and AtNAC53 Arabidopsis Arabidopsis

NAC78 and NAC53 homo- and heter- odimerize to regulate PSR and over- expression of NAC78 up-regulates other genes encoding proteasome accessory factor PA200, the NAS6 assembly chaperons, the UPS compo- nent of UFD1 and the HSP transcrip- tional regulator, HSF8A. Seedlings lacking both NAC78 and NAC53 failed to properly activate PSR and their growth was strongly hypersensi- tive to proteasome inhibitors

Gladman et al. (2016) ONAC127 and ONAC129 Rice Rice

ONAC127 and ONAC129 primarily regulate response to environmental stimuli, cell wall biosynthesis and nutrient transport. ONAC127 binds to promoters of calmodulin-like protein (OsMSR2) and monosac- charide transporter (OsMST6). Both

ONAC127 and ONAC129 repress the promoters of Ethylene-Response

AP2/ERF Factor (OsEATB) and sugar transporter (OsSWEET4) strongly in vivo

Ren et al. (2021) DREB TaDREB3 Wheat Arabidopsis Enhanced resistance to abiotic stresses in TaDREB3 overexpression lines was observed. Transgenic lines exhibited higher germination rate, survival rate, enhanced water reten- tion capacity, better stay green trait and stabilized membranes

Niu et al. (2020)

Plant Cell Reports 1 3 Table 1   (continued) Transcription factor

Source species Transgenic plant Comments References

ZmDREB2A Maize Arabidopsis The transcript of ZmDREB2A accumulates after HS, cold stress, salinity stress and dehydration stress treatments in maize seedlings.

ZmDREB2A produces two tran- scripts; however, only the functional transcription form of ZmDREB2A accumulates after stress treatments.

Overexpression enhances both heat- and drought-stress tolerance

Qin et al. (2007a) AtDREB1A Chrysanthemum Chrysanthemum

Transgenic lines showed higher sur- vival rate, photosynthetic capacity, and higher Rubisco and sucrose- phosphate synthase activity under

HS than WT plants. Leaf electrolyte leakage was significantly lower in

35:AtDREB1A lines Hong et al. (2009) OsDREB1B Rice

Rice OsDREB1B expression is induced by cold/HS treatments but not by other abiotic stresses or hormones such as ABA, MeJA or GA. OsDREB1B expression was detected in roots but not significantly in other organs. The survival rate of transgenic lines was significantly higher that WT plants

Qin et al. (2007 b) AmDREB3 Ammopiptanthus Ammopiptanthus AmDREB3 expression induced by a range of abiotic stresses and ABA- treatment. Transgenic lines showed higher survival rate, better growth after recovery and higher fresh weight after HS treatment. After HS treatment, the expression of stress- responsive genes (RDD29A, RD29B,

RAB18, COR47 and P5CS1) was higher in transgenic lines. In short,

AmDREB3 overexpression improves plant HS/drought and salinity stress tolerance

Ren et al. (2019) CmDREB6 Chrysanthemum Chrysanthemum

After HS treatment, the leaves of WT plants wilted severely, showed burning spots and dropped. No such effects were observed in overexpres- sion lines. Similarly, WT plants showed less survival rate than trans- genic lines

Du et al. (2018) LlDREB1G Llily Arabidopsis LlDREB1G expression is induced by multiple abiotic stresses and ABA.

Transgenic lines showed enhance tolerance to HS, cold stress and salin- ity stress

Liu et al. (2019) HS heat stress, HSPs heat shock proteins, DREB2A dehydration-responsive element binding transcriptional activator 2A, HSFs heat shock fac- tors, KO knockout mutants, TF transcription factors, WT wild type, AT acquired thermotolerance, H2O2 hydrogen peroxide, ABA abscisic acid,

MBF1c multi protein bridging factor 1C, PR1 pathogenesis related protein 1, SA salicylic acid, ET ethylene, JA jasmonic acid, GABA gamma- aminobutyric acid, Fv/Fm variable fluorescence by maximum fluorescence, ROS reactive oxygen species, ANN annxin, RNAi RNA interfer- ence, JUB1 JUNGBRUNNEN 1, DRIP1 DREB2A interacting protein, PSR proteasome stress regulon, MeJA methyl jasmonate, UFD1 ubiquitin fusion degradation 1, GA gibberellic acid, NAS 6 Probable nicotianamine synthase 6, PCD programmed cell death

Plant Cell Reports 1 3 regulation of diverse range of plant development and stress responses (Rushton et al. 2010). WRKYs contain a highly conserved WRKY (WRKYGQK) motif at the N-terminus, while a zinc-binding motif, C2H2 or C2HC is present at

C-terminus. WRKYs regulate transcription by binding spe- cifically to W-box (TTG​ACT​/C) sequence, present in the promoters of target genes (Rushton et al. 2010). On the basis of number of highly conserved WRKY domains and arrangement of zinc finger motifs, Eulgem et al. (2000) clas- sified Arabidopsis WRKY TFs into three groups. A single

WRKY TF might be involved in regulation of two seemingly contrasting phenomenon implying their role in modulating diversified plant processes (Rushton et al. 2010). A number of recent reports suggest that WRKYs are core component of cellular signaling network and their expression is asso- ciated with enhanced resistance to HS (Table 1). Various reports have revealed interaction between phytohormones and WRKYs in modulating plant HSR. For example, the exogenous application of hormones such as salicylic acid (SA), JA, ET and ABA has been shown to induce the expres- sion of HS-responsive WRKY genes (Li et al. 2011; Dang et al. 2013; He et al. 2016).

Role in heat stress tolerance WRKY TFs are associated with molecular reprogram- ming and stress-responsive gene expression that ensure plant survival under HS (Siddiqui et al. 2015). Constitu- tive expression of MBF1c up-regulates the expression lev- els of WRKY18, 33, 40 and 46 after HS treatment in trans- genic plants (Suzuki et al. 2005). The presence of W-box sequences in the promoters of HSFs and HSPs suggests the involvement of WRKY TFs in HS tolerance (Li et al. 2009).

Overexpression of OsWRKY11 enhances plant tolerance to heat and drought stress (Wu et al. 2009). AtWRKY39 confers thermotolerance in Arabidopsis thaliana by regulating the cooperation between SA and JA pathways (Li et al. 2010a, b). The wrky39 mutants exhibited reduced germination rate, decrease survival rate, increase susceptibility to HS, higher electrolyte leakage and reduced expression of HS marker genes. Li et al. (2011) reported the overexpression of

AtWRKY25, 26 and 33 increased the expression level of sev- eral HS-related genes and improved plant thermotolerance.

The overexpression of TaWRKY1 and TaWRKY33 improves heat/drought tolerance in transgenic Arabidopsis (He et al. 2016). TaWRKY33 overexpression lines showed higher expression level of genes including ABA1, ABA2,

ABI1, ABI5, DREB2B and RD29A, particularly ABA2 and

ABI5. Expression of RD29A suggests TaWRKY33 posi- tively regulates hyperosmotic stress response in Arabi- dopsis thaliana. Similarly, TaWRKY1 overexpression increases the transcripts of ABA1, ABA2, ABI1, ABI5 and

RD29A. AtBAG7 is an ER-localized co-chaperone and is an important player to regulate UPR during ER stress (Li et al. 2017). Under ER stress, AtBAG7 is cleaved at ­Ile378, translocated to the nucleus and interacts with AtWRKY29, which positively regulates AtBAG7 expression during HS.

AtBAG7 is SUMOylated upon HS which is essential for interaction with WRKY29 and HS tolerance (Li et al. 2017).

Dang et al. (2013) reported that overexpression of CaW- RKY40, a WRKY protein from pepper, enhances pepper HS tolerance and resistance to Ralstonia solanacearum. The silencing of CaWRKY40 leads to susceptibility to Ralsto- nia solanacearum and impair thermotolerance. Wang et al. (2018a) reported that ZmWRKY106 confers drought and HS tolerance in transgenic plant by regulating the expression of genes through ABA-signaling pathways. ZmWRKY106 regu- lates plant responses to range of abiotic stresses. Recently, it has been reported that AtWRKY30 enhances drought and

HS tolerance in bread wheat by activating the anti-oxidant machinery, osmolyte biosynthesis and stress-related gene expression (El-Esawi et al. 2019). Reports on the role of

WRKYs in regulation of resistance to HS are somewhat scarce, given the large size of this TF family. Additional studies are recommended to comprehensively characterize function of these regulatory proteins in HS adaptation, spe- cifically in crop plants.

MYB TFs MYB TFs are present in all eukaryotes and are associated with signaling networks which regulate plant development, primary and secondary metabolism, biotic and abiotic stress responses (Dubos et al. 2010). The N-terminal of MYB TFs is highly conserved and contains a DNA-binding domain, the MYB domain and a diverse C-terminal modulator region responsible for interaction with other TFs. MYB proteins are divided into four major classes: 1R-MYB (sin- gle repeat), R2R3-MYB (two repeats), 34-MYB (three repeats) and 4R-MYB (four repeats) based on the number of MYB domains (Dubos et al. 2010). Among these classes,

R2R3-MYB is most abundant in plants (Dubos et al. 2010).

MYB TFs are involved in regulation of HSR, from ­Ca2+ signaling to HS-responsive gene expression and hold great potential for crop trait improvement due to their inherent capability to enhance tolerance to multiple stress conditions (Table 1). Recent studies have revealed that MYB TFs are integral component of HS-induced signaling pathway; thus this group of regulatory proteins holds great potential for developing thermotolerant crop cultivars.

Role in heat stress tolerance The AtMYB68 confers thermotolerance during vegetative stage by increasing root lignin content (Feng et al. 2004).

OsMYB55 confers thermotolerance to transgenic rice

Plant Cell Reports 1 3 specifically during vegetative stage by increasing plant amino acid content (El-Kereamy et al. 2012).OsMYB55 binds to a CAG​TTA​ cis-acting motif, present in the promot- ers of GAT1, GAD3 and OsGS1;2 genes, 1079 bp, 460 bp and 554 bp upstream from the first ATG codon, and 10.1007/ s00299-021-02754-w enhance their expression. In tomato, a R2R3-MYB transcription factor LeAN2, confers thermo- tolerance by up-regulating genes involved in anthocyanin biosynthesis pathway, e.g. LeCHS1, LeCHS2, LeF3H and

LeDFR (Meng et al. 2015). Transgenic plants showed less accumulation of ROS content, increase membrane stabil- ity, higher D1 protein content (which constitutes the central core of PSII) and phenotype which is more adaptive to HS conditions. Liu et al. (2015) identified several MYB genes responsive to HS, drought stress and combination of both stresses. Constitutive expression of OsMYB55 confers ther- motolerance and enhance drought resistance in transgenic maize through activation of several stress-responsive genes (Casaretto et al. 2016). Transgenic lines showed better ger- mination rate, higher chlorophyll content, plant height, water potential, lower leaf temperature and higher photosynthetic activity under HS and drought conditions.

Zhao et al. (2017) reported that TaMYB80 enhances Arabidopsis tolerance to HS and drought stress. TaMYB80 over-expression leads to increased cellular ABA levels, and in turn, the higher expression of ABA-related stress- responsive genes including MYB15, HSFA6b, DREB2A,

RD22 and RD29b indicating interaction between TaW- RKY80 and ABA signaling network under HS. Recently, it has been reported that AtMYB59 acts as a negative regula- tor of ­Ca2+ signaling and homeostasis during plant growth and stress responses including HS (Fasani et al. 2019). A significant number of genes involve in calcium homeostasis and signaling (including those encoding calmodulins-like proteins and ­Ca2+ transporters) were up-regulated in myb59 mutants. Akhter et al. (2019) reported that OsPL, a MYB

TF, enhances plant HS tolerance by up-regulating expres- sion of several genes involved in anthocyanin biosynthesis, amino acid metabolism and ROS homeostasis. Additionally, increased malondialdehyde activity (MDA), increased total soluble sugar (TSS), ABA, JA and indole acetic acid (IAA) content was observed in OsPL lines. Additional studies are recommended to characterize MYB genes, their upstream regulatory factors and downstream target genes in crop plants to expand strategies for crop improvement through biotechnologies.

NAC TFs NAC TFs are plant-specific proteins that regulate develop- ment and stress responses (Puranik et al. 2012). The NAC proteins contain a highly conserved NAC-domain (approxi- mately 150 amino-acids) present at N-terminal which participates in DNA-binding, and a diversified C-terminal transcriptional regulatory region (Olsen et al. 2005; Puranik et al. 2012). In the past decade, several studies reported the molecular characterization of stress-inducible NAC proteins (Table 1). NAC TFs play an important role in plant HSR and may function as homo-heterodimers. Some NAC proteins may also function as membrane bound TF, allowing plants to rapidly response to HS by skipping the processes of tran- scription and translation.

Role in heat stress tolerance The expression of TaNAC69-1 is strongly induced by high temperature and salinity stress treatments in Durum wheat (Triticum turgidum) (Baloglu et al. 2012). JUB1, a NAC

TF, is induced by ­H2O2, promotes longevity, enhances plant

HS tolerance and affects transcriptional memory. Over- expression of JUB1 induces the expression of HSPs, glu- tathione S-transferase genes and elevates trehalose content.

The expression of JUB1 closely resembles the expression pattern of HSFA2, HSA32 (well-known thermomemory genes) (Shahnejat-Bushehri et al. 2012; Wu et al. 2012).

The expression of SNAC3 is induced under abiotic stress conditions such as HS, drought stress and salinity stress conditions. SNAC3 overexpression improves plant heat and drought stress tolerance through activating ROS associated genes (Fang et al. 2015). Guo et al. (2015) reported that

TaNAC2L confers HS tolerance in Arabidopsis thaliana by regulating HS-responsive gene expression.

You et al. (2015) performed systematic analysis and iden- tified 101 abiotic stress-responsive putative NAC domain encoding genes in Brachypodium distachyon. Promoter anal- ysis of these putative genes reveal the presence of several stress-related cis-acting elements. Out of 101, 34 BdNAC genes were upregulated under HS. Different environmental stresses can generate proteotoxic stress by denaturing pro- teins. Gladman et al. (2016), by combining RNA-sequencing analysis with chemical inhibitors, and with mutants that induce proteotoxic stress by impairing 26S proteasome path- way, reported that a pair of NAC TFs, NAC78 and NAC53, homo-heterodimerize to regulate proteasome stress regulon in Arabidopsis by activating expression of various factors that aid plant survive proteotoxic stress.

Very recently, it has been reported that OsNTL3, a mem- brane-associated NAC TF, is induced by HS, ER stress and relocated from plasma membrane to nucleus under stress conditions (Liu et al. 2020). OsNTL3 is a transcriptional activator and up-regulates the expression of several down- stream genes, particularly those involved in UPR, including

OsbZIP74 by binding directly to its promoter sequence. The up-regulation of OsNTL3 in turn is dependent on OsbZIP74 forming a regulatory circuit. The ntl mutants were more sen- sitive to HS as shown by increase ROS content and higher

Plant Cell Reports 1 3 electrolyte leakage. Very recently, it has been reported that

ONAC127 and ONAC129, two caryopsis-specific, HS- responsive NAC TFs primarily regulate response to environ- mental stimuli, cell wall biosynthesis and nutrient transport in rice (Ren et al. 2021).

DREB TFs The APETALA2 (AP2)/Ethylene Responsive Factors (ERF) are plant-specific TFs and are characterized by an AP2/ERF domain. The AP2/ERF domain consists of 40–70 conserved amino acids and is involved in DNA-binding (Sakuma et al.

2002). The AP2/ERF family is further divided into four major sub-families: the AP2, RAV, ERF and DREB (Xie et al. 2019). Here, we will review reports on the role of

DREBs under HS. For detailed review on functions of AP2/

ERF TF family, reader is referred to Xie et al. (2019). DREB proteins contain a unique DNA-binding domain which inter- acts with DRE/CRT cis-elements (A/GCC​GAC​) present in promoters of dehydration/cold regulated genes (RD/COR) to activate transcription and play a key role in regulation of abiotic stress responses (Mizoi et al. 2012 and references therein). Among DREB sub-family, the DREB2 sub-group members participate in drought, high temperature, salinity and osmotic stress responses (Fig. 1) (Sakuma et al. 2002;

Matsukura et al. 2010).

Role in heat stress tolerance DREB2A is a major transcriptional activator of heat and drought stress-inducible genes and plays a key role in acti- vation of arrays of genes under corresponding stress events (Sato et al. 2014; Kumar et al. 2016). Through yeast two hybrid assay, Sato et al. (2014) identified DREB2A inter- acting proteins that confer stress-specific target selectiv- ity through stress-dependent post-translational regulation of DREB2A genes. These include DPB3-1, NF-YA and

NF-YB. In a previous study, HSFA3 was shown to function downstream of DREB2A activated transcriptional cascade (Yoshida et al. 2008). The activities of HSFA3 under HS are also controlled by DREB2C which interacts with DRE sequences through its C-terminal region (Chen et al. 2010).

The DREB2C overexpression increases the transcription of several HSPs which function downstream of HSFA3. The tissue-specific, HS-inducible activities of DREB2C are dependent on region located between − 204 and − 34 base pairs upstream from transcriptional start site (Chen et al.

2012). Matsukura et al. (2010) performed expression profil- ing of OsDREB2 genes under abiotic stresses and reported that OsDREB2A and OsDREB2B show stress-inducible gene expression. The OsDREB2B was reported to be local- ized in the nucleus and was shown to be most strongly trans- activated DREB2 under stress conditions. Overexpression of OsDREB2B leads to enhanced expression of DREB2A targeted genes revealing a crucial role of this TF under heat- and drought-stress conditions. AtDREB1A over-expression in Chrysanthemum morifolium enhances the expression of genes involved in signal-transduction, transcription, photo- synthesis and metabolism (Hong et al. 2009). ZmDREB2A improves plant drought and HS tolerance by up-regulating the expression of late embryogenesis abundant (LEA) pro- teins (Qin et al. 2007a). The transcripts of OsDREB1B accu- mulate after cold and HS treatment in transgenic Arabidop- sis and contribute to enhance cold/HS tolerance (Qin et al.

2007b).

Recently, it has been reported that AmDREB3 over- expression leads to increase anthocyanin accumulation. This in turn, improves HS and oxidative stress tolerance in plants (Ren et al. 2019). CmDREB6 overexpression enhances

Chrysanthemum morifolium tolerance to HS possibly by ele- vating the expression of CmHSFA4, CmHSP90, CmSOD and

CmCAT​ genes (Du et al. 2018). Overexpression of DPB3-1, the Arabidopsis transcriptional regulator, enhances rice HS tolerance without growth retardation or yield reduction (Sato et al. 2016). The expression of OsHSFA2, OsHSFA3, LOC_

Os03g15960 and LOC_Os03g16020 was significantly higher in transgenic lines. LlDREB1G confers tolerance to multiple stresses and improves AT, freezing resistance and dehydra- tion tolerance in transgenic Arabidopsis (Liu et al. 2019).

Overexpression of LlDREB1G increased proline content and survival rate, decreased electrolyte leakage and reduced

­H2O2 content in transgenic lines after stress treatments. The overexpression of SbDREB2A increases the HS resistance in transgenic tobacco. Transgenic lines show enhanced expression levels of HS-related genes, TFs, signaling com- ponents and dehydrins (Gupta et al. 2014). Recently, it has been reported that TaDREB3 homeologous genes improve plant tolerance to drought, salt and heat stresses (Niu et al.

2020). Expression of RD29A, RD19, HSFA3, LEA, RAS1 and HSP70 was high under stress conditions, indicating

TaDREB3 might improve plant stress tolerance by elevating expression of down-stream stress-responsive genes. bHLH TFs bHLH TF family is second largest TF family in plants and is named based on the presence of highly conserved alka- line/helix–loop–helix (HLH) domains (Feller et al. 2011).

A bHLH TF consists of two motifs, a basic region at N-ter- minal, and HLH region at C-terminal (Song et al. 2013).

The basic region consists of approximately 15 amino acids of which 6 are basic in nature and is involved in DNA-rec- ognition and binding. The HLH region comprises of hydro- phobic residues and is involved in dimerization (Wang et al.

2018 b). Apart from these two regions, the rest of the bHLH

Plant Cell Reports 1 3 proteins are vastly diverged (Wang et al. 2018 b). The bHLH

TFs are involved in response to cold, light, hormone signals and in regulation of the developmental patterns of root and flowers (for review see Wang et al. 2018 b).

Role in heat stress tolerance In recent years, an increasing number of studies have indi- cated the key role of bHLH TF family in plant acclimation to high ambient temperature (temperature below HS). In response to warm temperature, plants modify their morphol- ogy to adapt to changing environment through a number of strategies which are collectively termed as “thermomor- phogenesis” (reviewed by Quint et al. 2016). Since plant developmental responses under high ambient temperature are beyond the scope of this article, we will briefly discuss important factors (belonging to bHLH family) which have been shown to be pivotal for these responses.

Phytochrome interacting factor 4 (PIF4), a bHLH TF mediates high ambient temperature adaptation responses in Arabidopsis thaliana (Koini et al. 2009). Well-known phenotypic responses of Arabidopsis to high ambient tem- peratures include hypocotyl elongation, leaf axis elongation, petiole elongation, leaf hyponasty and early flowering. After exposure at 28 °C, hypocotyl and petiole elongation was completely abolished in pif4 mutants. Similarly, leaf hypo- nastic response (upward movement) was severely hampered in mutants. This suggests the major role of PIF4 in these developmental processes under HS (Koini et al. 2009). In fact, PIF4 has been proposed to act as a major signaling hub under warm temperature conditions (Quint et al. 2016). The expression of PIF4 elevates quickly after exposure of plant to warm ambient temperature which triggers transcriptional changes that promote phytohormones dependent growth responses under these conditions (Koini et al. 2009; Quint et al. 2016). The PIF4 expression in turn, is controlled by phytochrome B (phyB) (Jung et al. 2016). Since the phyB temperature perception is based on dark reversion, the warm-temperature transcriptome that controls development occurs at night (Jung et al. 2016). For comprehensive review on role of PIFs in temperature signaling, reader is refer to

Balcerowicz (2020).

Several bHLH TF genes are up-regulated in Solanum tuberosum under HS (Wang et al. 2018 b). These include

StbHLH65, 76 and 79. Few bHLH TFs such as StbHLH5 in addition to HS, also respond to other abiotic stresses includ- ing drought and salinity. Additionally, some TFs such as

StbHLH60 and StbHLH78 exhibit contrasting expression profiles under these stress conditions. For example, expres- sion of StbHLH78 was up-regulated under drought stress, down-regulated under HS and was insensitive to salt stress.

It has been reported that one bHLH protein may interact with other bHLH or non-bHLH proteins (Feller et al. 2011).

This suggests that StbHLH genes sensitive to different stress cues may form heterodimers with specific bHLH proteins, leading to a wide range of stress responses and expression patterns (Wang et al. 2018 b). Wang et al. (2019a) per- formed genome-wide analysis of bHLH transcription factors in bread wheat and identified 159 bHLH encoding genes.

Among them, expression of TabHLH72 and TabHLH85 was highly induced upon HS treatment while the expression of

TabHLH-4, -11, -22,-29, -40, -55, -74 and -121 was down- regulated after HS treatment. Expression of TabHLH5, Tab- HLH35 and TabHLH95 was significantly up-regulated in response to abiotic stress treatments including HS, drought, cold and salinity stress. This study shows the important role of bHLH TFs in diverse plant stress responses. Very recently,

Bruessow et al. (2021) reported that the TF bHLH059 has characteristics of a temperature-sensitive immunity regulator that are distinct from PIF4. A deep analysis and functional characterization of these regulatory proteins is much needed to decipher their role in regulation of resistance to HS.

Interaction of TFs with small RNAs and chromatin modifiers/remodelers also governs somatic

“priming and thermomemory responses” in plants Several environmental factors often induce chromatin modi- fications at various genomic loci and consequently change their expression. Long viewed as an interface between environment and genome, the flexibility and dynamics of chromatin profoundly impact expression of genes by con- trolling the accessibility of transcriptional machinery to the genomic loci thereby regulating genomic information in

DNA sequence (Badeaux and Shi 2013). Recently, several reports have indicated that memory signatures carried by chromatin marks are induced by diverse range of adverse environmental inputs including HS. In nature, plants often face multitude of stress events which can be continual or recurring and thus have evolved sophisticated adaptive mechanisms to ‘memorize’ past exposures to stress episodes to elicit a much stronger response upon recurring stress.

Among these mechanisms, both the epigenetic and chroma- tin-based alterations have been shown to be actively involved in HS memory establishment and retention. Here we will review the somatic transcriptional memory induced by HS and the role of TFs in it. For an overview of somatic, inter- generational and transgenerational HS memory in plants, reader is refereed to Haider et al. (2021a, b).

Lämke et al. (2016) reported that HSFA2 is responsible for chromatin modification and sustained activation of HS- related genes by methylation (H3K4me2 and H3K4me3) of target loci (Fig. 2). After 1-h heat acclimation at 37 °C, plants were able to withstand higher temperature of 44 °C for a shorter period of time. Chromatin immunoprecipita- tion analysis revealed a higher enrichment of H3K4me3 and

Plant Cell Reports 1 3 H3K4me2 at HS-responsive loci (HSP 18.2, HSP21, and

HSP22.0). These genes showed a pattern of transcriptional memory such that their expression was induced significantly after repeated exposure to HS. A similar pattern of methyla- tion was observed at target loci when Arabidopsis was exposed to mild drought conditions followed by exposure to severe drought stress (Ding et al. 2012). This indicates the methyla- tion of target loci after exposure to mild stress is a mark of transcriptional memory that is associated with the enhanced re-induction of memory genes under multiple stress condi- tions. A recent study by Song et al. (2021) revealed that two

H3K4methyltransferases SDG25 and ATX1 are responsible for maintenance of HS-responsive gene expression during thermos-recovery process. ATX1 was shown to directly bind to chromatins associated with the memory genes. Mutations in either of these two enzymes decreased the H3K4me lev- els at target loci and subsequently reduced expression during stress recovery. Weng et al. (2014) reported that Arabidopsis anti-silencing functions 1A (ASF1A) and ASF1B activate the expression of target genes (HSFs and HSPs) by promoting nucleosome eviction under high temperatures at respective loci. It remains to be seen whether ASF1A and ASF1B par- ticipate in thermomemory responses. Brzezinka et al. (2016) reported that FGT1, a histone chaperone, is responsible for chromatin remodeling, decreased nucleosome occupancy and expression of memory genes after HS in plants (Fig. 2).

Alshareef et al. (2021) reported two NAC TFs, ATAF1 and

ANAC055, negatively regulate thermomemory in plants. The authors identified 64 genes that are likely the target of ATAF1.

The ATAF1 overexpression lines showed a reduced HS mem- ory while ataf1-2 and ataf1-4 mutants showed a phenotype with strong HS memory and higher survival rate. Olas et al. (2021) reported the involvement of HSFA2 in HS memory in

Arabidopsis shoot apical meristem (SAM). The HS memory enables SAM to regain growth after exposure to severe HS.

The microRNA (miRNA) belong to a class of non-coding

RNA that regulate gene expression under range of diverse biological and stressful conditions (Stief et al. 2014a). The miR156 have been reported to extend HS memory in Arabi- dopsis by downregulating squamosa promoter-binding pro- tein-like (SPL) genes (Fig. 2) (Stief et al. 2014b). miR156 is essential for the expression of HSFA2 and other HSPs dur- ing HS (Stief et al. 2014a). The downregulation of SPL genes is an essential step in plant HSR as SPL are master regula- tors of plant growth responses in plants (Huijser and Schmid

2011; Stief et al. 2014b). Therefore, it has been suggested that this miR156-SPL module may control the trade-off between growth and stress responses (Stief et al. 2014b). The miR398 is induced by HS and downregulates ROS scavengers under HS (Guan et al. 2013). The activities of miR398 are controlled by

HSFA1b and HSFA7b. The downregulation of ROS scaven- gers causes the accumulation of ROS which activates HSFA1s.

This then constitutes a positive feedback loop in regulating thermotolerance.

Fig. 2   Role of epigenetic factors and small RNAs in somatic ther- momemory. HS activates HSFA1s and HSFA2 which promote ther- motolerance and thermomemory in plants. HSFA2 is responsible for histone methylation which is the mark of transcriptional memory in plants. HSFA2 also activates SAM genes which promote HS mem- ory. SPLs negatively regulate HSFA2 activities under non-stress conditions. However, miR156 downregulates SPL genes under HS and extends HS memory. ASFA1 is a histone chaperone which pro- motes nucleosome eviction and histone acetylation of target genes under HS. However, the role of ASF1 in HS memory is not analyzed. miR398 downregulates ROS scavengers under HS which results in

ROS production. This then activates HSFA1s thus constituting a posi- tive feedback loop. FGT1 promotes somatic thermomemory through chromatin remodeling at target loci (This image has been modified from Haider et al. (2021a))

Plant Cell Reports 1 3 Conclusion and perspectives

Being sessile organisms, plants cannot avoid adverse envi- ronmental inputs and thus have evolved complex signaling networks composed of multiple pathways. Plant HSR is initiated by stress perception by certain channels in plasma membrane which then transduce this information to the molecules which function as a secondary messengers. TFs act as molecular switches and regulate expression of HS- responsive genes. The stress-inducible expression of TFs in turn is regulated by complex transcriptional regulatory network which allows plants to maintain a fine balance between growth and stress response. To avoid damages caused by recurring stress events, plants have developed sophisticated memory storage mechanisms enabling much faster response on the offset of corresponding stress. This too in part is dependent on action of TFs which strongly suggests that “Transcription factors are molecular switches which regulate plant heat stress tolerance”.

The drastic increase in atmospheric temperature due to global climate change has become a major concern as extreme temperatures limit plant growth, development and geographical distribution (Raza et al. 2019; Haider et al.

2021a). In field, plants are exposed to fluctuating tem- perature during different growth seasons (from seedling to reproductive stage) and also on the day and night cycle (on daily basis). Higher temperatures negatively affect all the growth stages of plant. Here we have reviewed the regula- tory role of TFs in HSR which allow plants to maintain cellular homeostasis under HS conditions or enable them to mitigate the adverse effects of HS. A prerequisite for development of thermotolerance and enhancing produc- tivity in crop plants is a detailed knowledge of tolerance mechanisms activated by plants under HS conditions. To improve plant traits and to provide food security to grow- ing human population, a number of suitable biotechnologi- cal approaches have been adopted. One of them is omics (a combination of genomics, transcriptomics, proteom- ics, and metabolomics) which has revolutionized the field (Raza et al. 2021). Here we will discuss recent reports which indicate the potential of omics for identification of major players in plant HS tolerance (Fig. 3).

Genomics is referred to the study of genomes of liv- ing organisms which provides sufficient information about gene sequence, structure, features and functional anno- tation (Varshney et al. 2018). The era of plant genom- ics began after the sequencing of Arabidopsis genome (Kaul et al. 2000) followed by sequencing of rice genome (IRGSP 2005). Since then, genomes of more than 100 cereal crops have been sequenced providing for the first time unprecedented opportunity to analyze key genes, features associated with stress resistance (Purugganan and Jackson 2021). Functional genomic studies have aided in identification of factors which can be used to breed thermotolerant crop plants (Varshney et al. 2018).

For example, several genome-wide investigative studies have been carried out which have identified important genes responsible for regulation of abiotic stress resist- ance (Nover et al. 2001; Guo et al. 2008; Lin et al. 2011;

Duan et al. 2019; Ahmad et al. 2010, 2019). Guo et al. (2008) performed genome-wide analysis and identified 25 rice HSFs. Similar analysis were performed by Lin et al. (2011) who identified 25 HSFs in maize genome. The sequencing of wheat genome (Appels et al. 2018) enabled the identification of factors conferring thermotolerance.

Kumar et al. (2020) identified a total of 753 HSPs from wheat genome using various computational approaches.

A detailed knowledge of expression patterns and regula- tory networks of stress-responsive genes at genome-wide level contributes to the breeding of climate resilient crops (Varshney et al. 2018). Transcriptomics deals with the functional genome of living organism’s transcript level, abundance, function and modifications (Wang et al. 2020 b). Transcriptome profiling of Spinacia oleracea under HS revealed four differentially expressed genes (DEG) MYB

1, 108, 306 and 811 (Yan et al. 2016). Wang et al. (2019 b) performed transcriptome analysis after HS treatment in

Fig. 3   Omics strategies to study plant HS tolerance mechanisms (This figure has been modified from Khanna et al. (2019))

Plant Cell Reports 1 3 Chieh-Qua (Benincasa hispida) and identified two bHLH

TFs (bHLH128 and bHLH143) participating in plant resistance to HS. In addition, two PIFs were also identified and shown to be highly expressed after HS treatment. Sun et al. (2020) performed transcriptome analysis of Pearl millet under heat and drought stress and identified 6920 and 6484 genes differentially expressed under heat and drought stress conditions. Through transcriptome analysis and RNA-sequencing, Wu et al. (2016) identified several

WRKY TFs (CsWRKY10, − 37, and − 48, 4, − 18, − 28,

− 40, − 38, − 42, and − 45) in Camellia sinensis induced by HS. Qian et al. (2019) performed transcriptome analy- sis of maize seedlings under HS and identified 19 DEG which belong to MYB TF family. As little is known about molecular mechanisms of maize HSR, this study identified important factors which may contribute to HS tolerance and provides an opportunity for in-depth characterization of HS-resistant candidate genes.

Proteomics is referred to study of proteins sequence, structure, function, localization, modifications and interac- tions (Raza et al. 2021). Advances in understanding of stress signaling, key proteins and their biosynthesis pathways has led to expansion in the strategies to improve plants stress tolerance (reviewed by Aslam et al. 2017). Wu et al. (2020) identified 2034 differentially accumulated proteins (DAP) under HS in the leaves of tobacco. These DAPs were mostly involved in sucrose metabolism, energy production and con- version. DAP analysis under HS in banana revealed their role in photosynthesis, energy metabolism and stress signaling (Li et al. 2019 c). HS affected the proteins involved in chlo- rophyll metabolism and hormonal production. Metabolomics approaches help in identification of metabolites associated with stress resilience (Raza 2020). Fragkostefanakis et al. (2016) reported several metabolites such as alcohol, amino- acids, organic acids and phosphatase sugars are linked with improve thermotolerance at reproductive stage. A study by Dhatt et al. (2019) revealed that production of several metabolites such as sugars, tricarboxylic acid and starch was linked with tolerance to HS by rice seedlings.

Meeting the desired agricultural productivity in the sce- nario of climate change will require investigation of factors promoting stress resilience in model plant species as well as crop plants. No doubt the integration of emerging technolo- gies will favor the breeding of much desired thermotolerant crop cultivars.

Author contribution statement  SH conceived the idea, did the litera- ture review and wrote the primary manuscript alongside JI. SN and

MS helped in data collection and write-up. BAA, TY, and SAZ added valuable comments and improved the paper. TA supervised and final- ized the manuscript. All the authors read and approved the finalized manuscript.

Funding  There was no external funding for this research.

Declarations Conflict of interest  The authors declare that there is no conflict of in- terest.

References Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S (2010) Roles of enzymatic and nonenzymatic antioxidants in plants during abi- otic stress. Crit Rev Biotechnol 30(3):161–175

Ahmad P, Tripathi DK, Deshmukh R, Pratap Singh V, Corpas FJ (2019) Revisiting the role of ROS and RNS in plants under changing environment. Environ Exp Bot 161:1–3

Akhter D, Qin R, Nath UK, Eshag J, Jin X, Shi C (2019) A rice gene,

OsPL, encoding a MYB family transcription factor confers anthocyanin synthesis, heat stress response and hormonal sign- aling. Gene 699:62–72

Albihlal WS, Obomighie I, Blein T, Persad R, Chernukhin I, Crespi

M, Bechtold U, Mullineaux PM (2018) Arabidopsis HEAT

SHOCK TRANSCRIPTION FACTORA1b regulates multiple developmental genes under benign and stress conditions. J Exp

Bot 69(11):2847–2862 Alshareef NOH, Woo Y, de Werk T, Kamranfar I, Mueller-Roeber B,

Tester MA, Balazadeh S, Allu AD (2021) NAC transcription fac- tors ATAF1 and ANAC055 negatively regulate thermomemory in arabidopsis

Andrási N, Pettkó-Szandtner A, Szabados L (2021) Diversity of plant heat shock factors: regulation, interactions, and functions. J Exp

Bot 72(5):1558–1575 Anelli T, Sitia R (2008) Protein quality control in the early secretory pathway. EMBO J 27(2):315–327

Appels R, Eversole K, Stein N, Feuillet C, Keller B, Rogers J,

Khurana JP (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science

361(6403):eaar7191 Badeaux AI, Shi Y (2013) Emerging roles for chromatin as a sig- nal integration and storage platform. Nat Rev Mol Cell Biol

14(4):211–224 Balcerowicz M (2020) PHYTOCHROME-INTERACTING FACTORS at the interface of light and temperature signalling. Physiol Plant

169(3):347–356 Baloglu MC, Oz MT, Oktem HA, Yucel M (2012) Expression analysis of TaNAC69-1 and TtNAMB-2, wheat NAC family transcrip- tion factor genes under abiotic stress conditions in durum wheat (Triticum turgidum). Plant Mol Biol Rep 30(5):1246–1252

Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, von

Koskull-DÖring P (2004) Heat stress response in plants: a com- plex game with chaperones and more than twenty heat stress transcription factors. J Biosci 29(4):471–487

Baniwal SK, Chan KY, Scharf KD, Nover L (2007) Role of heat stress transcription factor HSFA5 as specific repressor of HSFA4. J

Biol Chem 282(6):3605–3613 Bratzel F, Turck F (2015) Molecular memories in the regulation of seasonal flowering: from competence to cessation. Genome Biol

16(1):1–14 Bruessow F, Bautor J, Hoffmann G, Yildiz I, Zeier J, Parker JE (2021)

Natural variation in temperature-modulated immunity uncovers transcription factor bHLH059 as a thermoresponsive regulator in

Arabidopsis thaliana. PLoS Genet 17(1):e1009290 Brzezinka K, Altmann S, Czesnick H, Nicolas P, Gorka M, Benke

E, Kabelitz T, Jähne F, Graf A, Kappel C, Bäurle I (2016)

Plant Cell Reports 1 3 Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. elife 5:e17061.

Casaretto JA, El-Kereamy A, Zeng B, Stiegelmeyer SM, Chen X, Bi

YM, Rothstein SJ (2016) Expression of OsMYB55 in maize activates stress-responsive genes and enhances heat and drought tolerance. BMC Genomics 17(1):1–15

Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT (2007) A heat-inducible transcription factor, HSFA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant

Physiol 143(1):251–262 Chen H, Hwang JE, Lim CJ, Kim DY, Lee SY, Lim CO (2010) Arabi- dopsis DREB2C functions as a transcriptional activator of HsfA3 during the heat stress response. Biochem Biophys Res Commun

401(2):238–244 Chen H, Je J, Song C, Hwang JE, Lim CO (2012) A proximal promoter region of Arabidopsis DREB2C confers tissue-specific expres- sion under heat stress. J Integr Plant Biol 54(9):640–651

Cui Y, Lu S, Li Z, Cheng J, Hu P, Zhu T, Wang X, Jin M, Wang X,

Li L, Huang S (2020) CYCLIC NUCLEOTIDE-GATED ION CHANNELs 14 and 16 promote tolerance to heat and chilling in rice. Plant Physiol 183(4):1794–1808

Dang FF, Wang YN, Yu LU, Eulgem T, Lai YA, Liu ZQ, Wang XU,

Qiu AL, Zhang TX, Lin J, Chen YS (2013) CaWRKY40, a

WRKY protein of pepper, plays an important role in the regula- tion of tolerance to heat stress and resistance to Ralstonia solan- acearum infection. Plant Cell Environ 36(4):757–774

Dhatt BK, Abshire N, Paul P, Hasanthika K, Sandhu J, Zhang Q, Obata

T, Walia H (2019) Metabolic dynamics of developing rice seeds under high night-time temperature stress. Front Plant Sci 10:1443

Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought

“train” transcriptional responses in Arabidopsis. Nat Commun

3(1):1–9 Ding Y, Shi Y, Yang S (2020) Molecular regulation of plant responses to environmental temperatures. Mol plant 13(4):544–564.

Du X, Li W, Sheng L, Deng Y, Wang Y, Zhang W, Yu K, Jiang J, Fang

W, Guan Z, Chen S (2018) Over-expression of chrysanthemum

CmDREB6 enhanced tolerance of chrysanthemum to heat stress.

BMC Plant Biol 18(1):1–10 Duan S, Liu B, Zhang Y, Li G, Guo X (2019) Genome-wide identifi- cation and abiotic stress-responsive pattern of heat shock tran- scription factor family in Triticum aestivum L. BMC Genomics

20(1):257 Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant

Sci 15(10):573–581 El-Esawi MA, Al-Ghamdi AA, Ali HM, Ahmad M (2019) Overex- pression of AtWRKY30 transcription factor enhances heat and drought stress tolerance in wheat (Triticum aestivum L.). Genes

10(2):163 El-Kereamy A, Bi YM, Ranathunge K, Beatty PH, Good AG, Rothstein

SJ (2012) The rice R2R3-MYB transcription factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism. PLoS ONE 7(12):e52030

Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci

5(5):199–206 Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress- responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66(21):6803–6817

Fasani E, DalCorso G, Costa A, Zenoni S, Furini A (2019) The Arabi- dopsis thaliana transcription factor MYB59 regulates calcium signalling during plant growth and stress response. Plant Mol

Biol 99(6):517–534 Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66(1):94–116

Feng C, Andreasson E, Maslak A, Mock HP, Mattsson O, Mundy J (2004) Arabidopsis MYB68 in development and responses to environmental cues. Plant Sci 167(5):1099–1107

Finka A, Cuendet AFH, Maathuis FJ, Saidi Y, Goloubinoff P (2012)

Plasma membrane cyclic nucleotide gated calcium channels con- trol land plant thermal sensing and acquired thermotolerance.

Plant Cell 248:3333–3348 Finka A, Goloubinoff P (2014) The CNGCb and CNGCd genes from

Physcomitrella patens moss encode for thermosensory calcium channels responding to fluidity changes in the plasma membrane.

Cell Stress Chaperones 191:83–90 Fragkostefanakis S, Mesihovic A, Simm S, Paupière MJ, Hu Y, Paul P,

Mishra SK, Tschiersch B, Theres K, Bovy A, Scharf KD (2016)

HsfA2 controls the activity of developmentally and stress-regu- lated heat stress protection mechanisms in tomato male reproduc- tive tissues. Plant Physiol 170(4):2461–2477

Fragkostefanakis S, Röth S, Schleiff E, SCHARF KD (2015) Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks.

Plant Cell Environ 38(9):1881–1895 Giri A, Heckathorn S, Mishra S, Krause C (2017) Heat stress decreases levels of nutrient-uptake and-assimilation proteins in tomato roots. Plants 6(1):6

Gladman NP, Marshall RS, Lee KH, Vierstra RD (2016) The protea- some stress regulon is controlled by a pair of NAC transcription factors in Arabidopsis. Plant Cell 28(6):1279–1296

Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR 398 triggers a regulatory loop that is critical for thermotoler- ance in Arabidopsis. Plant J 74(5):840–851

Guan Q, Yue X, Zeng H, Zhu J (2014) The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress- responsive gene regulation and thermotolerance in Arabidopsis.

Plant Cell 26(1):438–453 Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang J (2008) Genome- wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35(2):105–118

Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH (2016) The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 7:114

Guo W, Zhang J, Zhang N, Xin M, Peng H, Hu Z, Du J (2015) The wheat NAC transcription factor TaNAC2L is regulated at the transcriptional and post-translational levels and promotes heat stress tolerance in transgenic Arabidopsis. PLoS ONE

10(8):e0135667 Guo XL, Yuan SN, Zhang HN, Zhang YY, Zhang YJ, Wang GY, Li

GL (2020) Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHSFA2–10.

BMC Plant Biol 20(1):1–18 Gupta K, Jha B, Agarwal PK (2014) A dehydration-responsive ele- ment binding (DREB) transcription factor from the succulent halophyte Salicornia brachiata enhances abiotic stress tolerance in transgenic tobacco. Mar Biotechnol 16(6):657–673

Haider S, Iqbal J, Naseer S, Yaseen T, Shaukat M, Bibi H, Ahmad Y,

Daud H, Abbasi NL, Mahmood T (2021a) Molecular mecha- nisms of plant tolerance to heat stress: current landscape and future perspectives. Plant Cell Reports 1-25

Haider S, Iqbal J, Shaukat M, Naseer S, Mahmood T (2021b). The epigenetic chromatin-based regulation of somatic heat stress memory in plants. Plant Gene, 100318.

Hahn A, Bublak D, Schleiff E, Scharf KD (2011) Crosstalk between

HSP90 and HSP70 chaperones and heat stress transcription fac- tors in tomato. Plant Cell 23(2):741–755

Plant Cell Reports 1 3 Hasanuzzaman M, Nahar K, Alam M, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14(5):9643–9684

Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather Clim Extrem 10:4–10

Hayes S, Schachtschabel J, Mishkind M, Munnik T, Arisz SA (2021) Hot topic: Thermosensing in plants. Plant cell environ

44(7):2018-2033 He GH, Xu JY, Wang YX, Liu JM, Li PS, Chen M, Ma YZ, Xu ZS (2016) Drought-responsive WRKY transcription factor genes

TaWRKY1 and TaWRKY33 from wheat confer drought and/ or heat resistance in Arabidopsis. BMC Plant Biol 16(1):1–16

Hong B, Ma C, Yang Y, Wang T, Yamaguchi-Shinozaki K, Gao

J (2009) Over-expression of AtDREB1A in chrysanthe- mum enhances tolerance to heat stress. Plant Mol Biol

70(3):231–240 Howell SH (2013) Endoplasmic reticulum stress responses in plants.

Annu Rev Plant Biol 64:477–499 Huijser P, Schmid M (2011) The control of developmental phase transi- tions in plants. Development 138(19):4117–4129

International R.G.S.P (2005) The map-based sequence of the rice genome. Nature 436(7052):793

Iwata Y, Ashida M, Hasegawa C, Tabara K, Mishiba KI, Koizumi N (2017) Activation of the Arabidopsis membrane-bound transcrip- tion factor bZIP 28 is mediated by site-2 protease, but not site-1 protease. Plant J 91(3):408–415

Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chap- erone network and multiple stress resistance. Plant Biotechnol

J 15(4):405–414 Jiang Y, Zheng Q, Chen L, Liang Y, Wu J (2018) Ectopic overexpres- sion of maize heat shock transcription factor gene ZmHSF04 confers increased thermo and salt-stress tolerance in transgenic

Arabidopsis. Acta Physiol Plant 40(1):1–12 Jung JH, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Wigge PA (2016) Phytochromes function as thermosensors in Arabidopsis.

Science 354(6314):886–889 Kaul S, Koo HL, Jenkins J, Rizzo M, Rooney T, Tallon LJ, Somerville

C (2000) Analysis of the genome sequence of the flowering plant

Arabidopsis thaliana. Nature 408(6814):796–815 Khanna K, Handa N, Yadav P, Gautam V, Kumar V, Ohri P, Bhardwaj

R (2019) Molecular approaches in enhancing antioxidant defense in plants. In: Reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mecha- nisms, pp 173–193

Kim JS, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, Nakashima K,

Yamaguchi-Shinozaki K (2012) Arabidopsis GROWTH-REG- ULATING FACTOR7 functions as a transcriptional repressor of abscisic acid–and osmotic stress–responsive genes, including

DREB2A. Plant Cell 24(8):3393–3405 Kaur H, Sirhindi G, Bhardwaj R, Alyemeni MN, Siddique KH,

Ahmad P (2018) 28-homobrassinolide regulates antioxidant enzyme activities and gene expression in response to salt-and temperature-induced oxidative stress in Brassica juncea. Sci Rep

8(1):1–13 Kohli SK, Khanna K, Bhardwaj R, Abd-Allah EF, Ahmad P, Corpas

FJ (2019) Assessment of subcellular ROS and NO metabolism in higher plants: multifunctional signaling molecules. Antioxidants

8(12):641 Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC,

Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4.

Curr Biol 19(5):408–413 Kumar RR, Goswami S, Singh K, Dubey K, Rai GK, Singh B, Praveen

S (2018) Characterization of novel heat-responsive transcription factor (TaHSFA6e) gene involved in regulation of heat shock proteins (HSPs)—a key member of heat stress-tolerance network of wheat. J Biotechnol 279:1–12

Kumar R, Singh AK, Lavania D, Siddiqui MH, Al-Whaibi MH, Grover

A (2016) Expression analysis of ClpB/Hsp100 gene in faba bean (Vicia faba L.) plants in response to heat stress. Saudi J Biol Sci

23(2):243–247 Kumar A, Sharma S, Chunduri V, Kaur A, Kaur S, Malhotra N, Garg

M (2020) Genome-wide identification and characterization of heat shock protein family reveals role in development and stress conditions in Triticum aestivum L. Sci rep 10(1):1–12

Lämke J, Bäurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants.

Genome Biol 18(1):1–11 Lämke J, Brzezinka K, Altmann S, Bäurle I (2016) A hit-and-run heat shock factor governs sustained histone methylation and transcrip- tional stress memory. EMBO J 35(2):162–175

Laohavisit A, Brown AT, Cicuta P, Davies JM (2010) Annexins: com- ponents of the calcium and reactive oxygen signaling network.

Plant Physiol 152(4):1824–1829 Lee S, Lee HJ, Huh SU, Paek KH, Ha JH, Park CM (2014) The Arabi- dopsis NAC transcription factor NTL4 participates in a positive feedback loop that induces programmed cell death under heat stress conditions. Plant Sci 227:76–83

Li B, Gao K, Ren H, Tang W (2018) Molecular mechanisms gov- erning plant responsesto high temperatures J integr plant biol

60(9):757–779.

Li Z, Tang J, Srivastava R, Bassham DC, Howell SH (2020) The Tran- scription factor bZIP60 links the unfolded protein response to the heat stress response in maize. Plant Cell 3211:3559–3575

Li G, Zhang Y, Zhang H, Zhang Y, Zhao L, Liu Z, Guo X (2019a)

Characteristics and regulating role in thermotolerance of the heat shock transcription factor ZmHSF12 from Zea mays L. J Plant

Biol 62(5):329–341 Li J, Han G, Sun C, Sui N (2019b) Research advances of MYB tran- scription factors in plant stress resistance and breeding. Plant

Signal Behav 14(8):1613131 Li M, Berendzen KW, Schöffl F (2010a) Promoter specificity and inter- actions between early and late Arabidopsis heat shock factors.

Plant Mol Biol 73(4–5):559–567 Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana

WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233(6):1237–1252

Li S, Fu Q, Huang W, Yu D (2009) Functional analysis of an Arabi- dopsis transcription factor WRKY25 in heat stress. Plant Cell

Rep 28(4):683–693 Li S, Zhou X, Chen L, Huang W, Yu D (2010b) Functional charac- terization of Arabidopsis thaliana WRKY39 in heat stress. Mol

Cells 29(5):475–483 Li T, Wu Q, Duan X, Yun Z, Jiang Y (2019c) Proteomic and transcrip- tomic analysis to unravel the influence of high temperature on banana fruit during postharvest storage. Funct Integr Genomics

19(3):467–486 Li Y, Williams B, Dickman M (2017) Arabidopsis B-cell lymphoma2 (Bcl-2)-associated athanogene 7 (BAG 7)-mediated heat toler- ance requires translocation, sumoylation and binding to WRKY

29. New Phytol 214(2):695–705 Liao C, Zheng Y, Guo Y (2017) MYB30 transcription factor regu- lates oxidative and heat stress responses through ANNEXIN- mediated cytosolic calcium signaling in Arabidopsis. New Phytol

216(1):163–177 Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, Cheng BJ (2011)

Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics

12(1):1–14

Plant Cell Reports 1 3 Lippmann R, Babben S, Menger A, Delker C, Quint M (2019) Devel- opment of wild and cultivated plants under global warming con- ditions. Curr Biol 29(24):R1326–R1338

Liu B, Zhou Y, Lan W, Zhou Q, Li F, Chen F, Liu G (2019)

LlDREB1G, a novel DREB subfamily gene from Lilium longi- florum, can enhance transgenic Arabidopsis tolerance to multiple abiotic stresses. Plant Cell Tissue Organ Cult 138(3):489–506

Liu HC, Charng YY (2013) Common and distinct functions of Arabi- dopsis class A1 and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol 163(1):276–290

Liu JG, Qin QL, Zhang Z, Peng RH, Xiong AS, Chen JM, Yao QH (2009) OsHSF7 gene in rice, Oryza sativa L., encodes a tran- scription factor that functions as a high temperature receptive and responsive factor. BMB Rep 42(1):16–21

Liu XH, Lyu YS, Yang W, Yang ZT, Lu SJ, Liu JX (2020) A mem- brane-associated NAC transcription factor OsNTL3 is involved in thermotolerance in rice. Plant Biotechnol J 18(5):1317–1329

Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, Sun Q (2015) Tem- poral transcriptome profiling reveals expression partition- ing of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol

15(1):1–20 Malini MK, Lekshmy VS, Pal M, Chinnusamy V, Kumar MN (2020)

Unfolded protein response (UPR) mediated under heat stress in plants. Plant Physiol Rep 25:569–582

Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K,

Shinozaki K, Yamaguchi-Shinozaki K (2010) Comprehensive analysis of rice DREB2-type genes that encode transcription fac- tors involved in the expression of abiotic stress-responsive genes.

Mol Genet Genomics 283(2):185–196 Meng X, Wang JR, Wang GD, Liang XQ, Li XD, Meng QW (2015)

An R2R3-MYB gene, LeAN2, positively regulated the thermo- tolerance in transgenic tomato. J Plant Physiol 175:1–8

Meshi T, Iwabuchi M (1995) Plant transcription factors. Plant Cell

Physiol 36(8):1405–1420 Miller GAD, Mittler RON (2006) Could heat shock transcription fac- tors function as hydrogen peroxide sensors in plants? Ann Bot

982:279–288 Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L,

Scharf KD (2002) In the complex family of heat stress transcrip- tion factors, HSFA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16(12):1555–1567

Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat?

Trends Biochem Sci 37(3):118–125 Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim

Biophys Acta Gene Regul Mech 1819(2):86–96 Nagashima Y, Mishiba KI, Suzuki E, Shimada Y, Iwata Y, Koizumi

N (2011) Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci

Rep 1(1):1–10 Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka

S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress.

Plant J 48(4):535–547 Nishizawa-Yokoi A, Nosaka R, Hayashi H, Tainaka H, Maruta T,

Tamoi M, Ikeda M, Ohme-Takagi M, Yoshimura K, Yabuta Y,

Shigeoka S (2011) HSFA1d and HSFA1e involved in the tran- scriptional regulation of HSFA2 function as key regulators for the HSF signaling network in response to environmental stress.

Plant Cell Physiol 52(5):933–945 Niu X, Luo T, Zhao H, Su Y, Ji W, Li H (2020) Identification of wheat

DREB genes and functional characterization of TaDREB3 in response to abiotic stresses. Gene 740:144514

Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf KD (2001)

Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress

Chaperones 6(3):177 Ohama N, Kusakabe K, Mizoi J, Zhao H, Kidokoro S, Koizumi S,

Takahashi F, Ishida T, Yanagisawa S, Shinozaki K, Yamaguchi- Shinozaki K (2016) The transcriptional cascade in the heat stress response of Arabidopsis is strictly regulated at the level of tran- scription factor expression. Plant Cell 28(1):181–201

Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017) Tran- scriptional regulatory network of plant heat stress response.

Trends Plant Sci 22(1):53–65 Olas JJ, Apelt F, Annunziata MG, John S, Richard SI, Gupta S, Kragler

F, Balazadeh S, Mueller-Roeber B (2021) Primary carbohydrate metabolism genes participate in heat stress memory at the shoot apical meristem of Arabidopsis thaliana. Mol Plant. https://​doi.​ org/​10.​1016/j.​molp.​2021.​05.​024

Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant

Sci 10(2):79–87 Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC pro- teins: regulation and role in stress tolerance. Trends Plant Sci

17(6):369–381 Purugganan MD, Jackson SA (2021) Advancing crop genomics from lab to field. Nat Genet 53:595–601

Qian Y, Ren Q, Zhang J, Chen L (2019) Transcriptomic analysis of the maize (Zea mays L.) inbred line B73 response to heat stress at the seedling stage. Gene 692:68–78

Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LSP,

Yamaguchi-Shinozaki K (2007a) Regulation and functional anal- ysis of ZmDREB2A in response to drought and heat stresses in

Zea mays L. Plant J 50(1):54–69 Qin QL, Liu JG, Zhang Z, Peng RH, Xiong AS, Yao QH, Chen JM (2007b) Isolation, optimization, and functional analysis of the cDNA encoding transcription factor OsDREB1B in Oryza sativa

L. Mol Breeding 19(4):329–340 Qu AL, Ding YF, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun

432(2):203–207 Quint M, Delker C, Franklin KA, Wigge PA, Halliday KJ, van Zanten

M (2016) Molecular and genetic control of plant thermomorpho- genesis. Nat Plants 2(1):1–9

Raza A (2020) Metabolomics: a systems biology approach for enhanc- ing heat stress tolerance in plants. Plant Cell Rep. https://​doi.​org/​

10.​1007/​s00299-​020-​02635-8 Raza A, Tabassum J, Kudapa H, Varshney RK (2021) Can omics deliver temperature resilient ready-to-grow crops?. Crit RevBio- technol 1-24

Raza A, Razzaq A, Mehmood SS, Zou X, Zhang X, Lv Y, Xu J (2019)

Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8(2):34

Reddy AS, Ali GS, Celesnik H, Day IS (2011) Coping with stresses: roles of calcium-and calcium/calmodulin-regulated gene expres- sion. Plant Cell 236:2010–2032

Ren M, Wang Z, Xue M, Wang X, Zhang F, Zhang Y, Wang M (2019)

Constitutive expression of an A-5 subgroup member in the DREB transcription factor subfamily from Ammopiptanthus mongolicus enhanced abiotic stress tolerance and anthocyanin accumulation in transgenic Arabidopsis. PLoS ONE 14(10):e0224296

Ren Y, Huang Z, Jiang H, Wang Z, Wu F, Xiong Y, Yao J (2021) A heat stress responsive NAC transcription factor heterodimer plays key roles in rice grain filling. J Exp Bot 72(8):2947–2964

Rushton PJ, Bokowiec MT, Laudeman TW, Brannock JF, Chen X,

Timko MP (2008) TOBFAC: the database of tobacco transcrip- tion factors. BMC Bioinform 9(1):1–7

Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcrip- tion factors. Trends Plant Sci 15(5):247–258

Plant Cell Reports 1 3 Sarwar M, Saleem MF, Ullah N, Ali S, Rizwan M, Shahid MR, Ahmad

P (2019) Role of mineral nutrition in alleviation of heat stress in cotton plants grown in glasshouse and field conditions. Sci

Rep 9(1):1–17 Sarwar M, Saleem MF, Ullah N, Rizwan M, Ali S, Shahid MR, Ahmad

P (2018) Exogenously applied growth regulators protect the cot- ton crop from heat-induced injury by modulating plant defense mechanism. Sci Rep 8(1):1–15

Saidi Y, Finka A, Muriset M, Bromberg Z, Weiss YG, Maathuis FJ,

Goloubinoff P (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21(9):2829–2843

Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi- Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem

Biophys Res Commun 290(3):998–1009 Sato H, Mizoi J, Tanaka H, Maruyama K, Qin F, Osakabe Y, Yamagu- chi-Shinozaki K (2014) Arabidopsis DPB3-1, a DREB2A inter- actor, specifically enhances heat stress-induced gene expression by forming a heat stress-specific transcriptional complex with

NF-Y subunits. Plant Cell 26(12):4954–4973 Siddiqui MH, Alamri SA, Al-Khaishany MY, Al-Qutami MA, Ali HM,

Al-Whaibi MH, Alharby HF (2018) Mitigation of adverse effects of heat stress on Vicia faba by exogenous application of magne- sium. Saudi J Biol Sci 25(7):1393–1401

Siddiqui MH, Al-Khaishany MY, Al-Qutami MA, Al-Whaibi MH,

Grover A, Ali HM, Al-Wahibi MS (2015) Morphological and physiological characterization of different genotypes of faba bean under heat stress. Saudi J Biol Sci 22(5):656–663

Sato H, Todaka D, Kudo M, Mizoi J, Kidokoro S, Zhao Y, Shinozaki K,

Yamaguchi-Shinozaki K (2016) The Arabidopsis transcriptional regulator DPB 3–1 enhances heat stress tolerance without growth retardation in rice. Plant Biotechnol J 14(8):1756–1767

Scharf KD, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (HSF) family: structure, func- tion and evolution. Biochim Biophys Acta Gene Regul Mech

1819(2):104–119 Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D, von

Koskull-Döring P (2006) The heat stress transcription factor

HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol Biol

60(5):759–772 Schwarz DS, Blower MD (2016) The endoplasmic reticulum: structure, function and response to cellular signaling. Cell Mol Life Sci

73(1):79–94 Shah Z, Shah SH, Ali GS, Munir I, Khan RS, Iqbal A, Ahmed N,

Jan A (2020) Introduction of Arabidopsis’s heat shock factor

HSFA1d mitigates adverse effects of heat stress on potato (Sola- num tuberosum L.) plant. Cell Stress Chaperones 25(1):57–63

Shahnejat-Bushehri S, Mueller-Roeber B, Balazadeh S (2012) Arabi- dopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress toler- ance in primed and unprimed conditions. Plant Signal Behav

7(12):1518–1521 Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front

Plant Sci 6:902 Song S, Qi T, Fan M, Zhang X, Gao H, Huang H, Xie D (2013) The bHLH subgroup IIId factors negatively regulate jasmonate-medi- ated plant defense and development. PLoS Genet 9(7):e1003653

Song ZT, Zhang LL, Han JJ, Zhou M, Liu J X (2021) Histone H3K4 methyltransferases SDG25 and ATX1 maintain heat‐stress gene expressionduring recovery in Arabidopsis. The Plant Journal

105(5):1326–1338 Srivastava R, Deng Y, Howell SH (2014) Stress sensing in plants by an

ER stress sensor/transducer, bZIP28. Front Plant Sci 5:59

Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Bäurle I (2014a) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant

Cell 26(4):1792–1807 Stief A, Brzezinka K, Lämke J, Bäurle I (2014b) Epigenetic responses to heat stress at different time scales and the involvement of small

RNAs. Plant Signal Behav 9(10):e970430 Stocker T (ed) (2014) Climate change 2013: the physical science basis:

Working Group I contribution to the Fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge

University Press, Cambridge Sun M, Huang D, Zhang A, Khan I, Yan H, Wang X, Zhang X, Zhang

J, Huang L (2020) Transcriptome analysis of heat stress and drought stress in pearl millet based on Pacbio full-length tran- scriptome sequencing. BMC Plant Biol 20(1):1–15

Suzuki N, Bajad S, Shuman J, Shulaev V, Mittler R (2008) The tran- scriptional co-activator MBF1c is a key regulator of thermotoler- ance in Arabidopsis thaliana. J Biol Chem 283(14):9269–9275

Suzuki N, Rizhsky L, Liang H, Shuman J, Shulaev V, Mittler R (2005)

Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol 139(3):1313–1322

Suzuki N, Sejima H, Tam R, Schlauch K, Mittler R (2011) Identifica- tion of the MBF1 heat-response regulon of Arabidopsis thaliana.

Plant J 66(5):844–851 Tian X, Wang F, Zhao Y, Lan T, Yu K, Zhang L et al (2020) Heat shock transcription factor A1b regulates heat tolerance in wheat and

Arabidopsis through OPR3 and jasmonate signalling pathway.

Plant Biotechnol J 18(5):1109 Tunc-Ozdemir M, Tang C, Ishka MR, Brown E, Groves NR, Myers CT,

Harper JF (2013) A cyclic nucleotide-gated channel (CNGC16) in pollen is critical for stress tolerance in pollen reproductive development. Plant Physiol 1612:1010–1020

United nations department of economic and social affairs, population division (2015) World population prospects: the 2015 revision, key findings and advance tables. Online edition . UNDESA, New

York Varshney RK, Singh VK, Kumar A, Powell W, Sorrells ME (2018)

Can genomics deliver climate-change ready crops? Curr Opin

Plant Biol 45:205–211 Voellmy R, Boellmann F (2007) Chaperone regulation of the heat shock protein response. In: Molecular aspects of the stress response: chaperones, membranes and networks, pp 89–99

Von Koskull-Döring P, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci

12(10):452–457 Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61(3):199–223

Wang CT, Ru JN, Liu YW, Li M, Zhao D, Yang JF, Xu ZS (2018a)

Maize WRKY transcription factor ZmWRKY106 confers drought and heat tolerance in transgenic plants. Int J Mol Sci

19(10):3046 Wang L, Ma KB, Lu ZG, Ren SX, Jiang HR, Cui JW, Jin B (2020a)

Differential physiological, transcriptomic and metabolomic responses of Arabidopsis leaves under prolonged warming and heat shock. BMC Plant Biol 20(1):1–15

Wang L, Xiang L, Hong J, Xie Z, Li B (2019a) Genome-wide analysis of bHLH transcription factor family reveals their involvement in biotic and abiotic stress responses in wheat (Triticum aestivum

L.). 3 Biotech 9(6):1–12 Wang M, Jiang B, Liu W, Lin YE, Liang Z, He X, Peng Q (2019b)

Transcriptome analyses provide novel insights into heat stress responses in Chieh-Qua (Benincasa hispida Cogn. Var. Chieh- Qua How). Int J Mol Sci 20(4):883

Plant Cell Reports 1 3 Wang R, Zhao P, Kong N, Lu R, Pei Y, Huang C, Ma H, Chen Q (2018b) Genome-wide identification and characterization of the potato bHLH transcription factor family. Genes 9(1):54

Wang Y, Yu Y, Huang M, Gao P, Chen H, Liu M, Sun Q (2020b)

Transcriptomic and proteomic profiles of II YOU 838 (Oryza sativa) provide insights into heat stress tolerance in hybrid rice.

PeerJ 8:e8306 Weng M, Yang YUE, Feng H, Pan Z, Shen WH, Zhu YAN, Dong A (2014) Histone chaperone ASF1 is involved in gene transcrip- tion activation in response to heat stress in Arabidopsis thaliana.

Plant Cell Environ 37(9):2128–2138 Wu A, Allu AD, Garapati P, Siddiqui H, Dortay H, Zanor MI, Bala- zadeh S (2012) JUNGBRUNNEN1, a reactive oxygen species- responsive NAC transcription factor, regulates longevity in

Arabidopsis. Plant Cell 24(2):482–506 Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing

OsWRKY11 under the control of HSP101 promoter. Plant Cell

Rep 28(1):21–30 Wu ZJ, Li XH, Liu ZW, Li H, Wang YX, Zhuang J (2016) Transcrip- tome-wide identification of Camellia sinensis WRKY transcrip- tion factors in response to temperature stress. Mol Genet Genom- ics 291(1):255–269

Xie Z, Nolan TM, Jiang H, Yin Y (2019) AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in

Arabidopsis. Front Plant Sci 10:228 Xin H, Zhang H, Zhong X, Lian Q, Dong A, Cao L, Cong R (2017)

Over-expression of LlHSFA2b, a lily heat shock transcription factor lacking trans-activation activity in yeast, can enhance tolerance to heat and oxidative stress in transgenic Arabidopsis seedlings. Plant Cell Tissue Organ Cult 130(3):617–629

Yan J, Yu L, Xuan J, Lu Y, Lu S, Zhu W (2016) De novo transcriptome sequencing and gene expression profiling of spinach (Spinacia oleracea L.) leaves under heat stress. Sci Rep 6(1):1–10

Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima

K, Yamaguchi-Shinozaki K (2011) Arabidopsis HSFA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics

286(5):321–332 Yoshida T, Sakuma Y, Todaka D, Maruyama K, Qin F, Mizoi J, Yama- guchi-Shinozaki K (2008) Functional analysis of an Arabidop- sis heat-shock transcription factor HSFA3 in the transcriptional cascade downstream of the DREB2A stress-regulatory system.

Biochem Biophys Res Commun 368(3):515–521 You J, Zhang L, Song B, Qi X, Chan Z (2015) Systematic analysis and identification of stress-responsive genes of the NAC gene family in Brachypodium distachyon. PLoS ONE 10(3):e0122027

Zanetti ME, Blanco FA, Daleo GR, Casalongué CA (2003) Phospho- rylation of a member of the MBF1transcriptional co‐activator family, St MBF1, is stimulated in potato cell suspensions upon fungal elicitor challenge. J Exp Bot 54383:623–632

Zhang J, Li XM, Lin HX, Chong K (2019a) Crop improvement through temperature resilience. Annu Rev Plant Biol 70:753–780

Zhang T, Cooper S, Brockdorff N (2015) The interplay of histone modifications—writers that read. EMBO Rep 16(11):1467–1481

Zhang Y, Malzahn AA, Sretenovic S, Qi Y (2019b) The emerging and uncultivated potential of CRISPR technology in plant science.

Nat Plants 5(8):778–794 Zhao Y, Tian X, Wang F, Zhang L, Xin M, Hu Z, Peng H (2017)

Characterization of wheat MYB genes responsive to high tem- peratures. BMC Plant Biol 17(1):1–14

Zhao J, Lu Z,Wang L, Jin B (2021) Plant responses to heat stress: physiology, transcription, noncoding RNAs, and epigenetics.

Inter J Mol Sci 22(1):117 Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell

167(2):313–324 Publisher's Note  Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.