REVIEW published: 15 December 2021 doi: 10.3389/fpls.2021.767150
Adaptation Strategies to Improve the Resistance of Oilseed Crops to Heat Stress Under a Changing Climate: An Overview Muhammad Ahmad 1,2 , Ejaz Ahmad Waraich 1*, Milan Skalicky 3 , Saddam Hussain 1 , Usman Zulfiqar 1 , Muhammad Zohaib Anjum 4 , Muhammad Habib ur Rahman 5,6 , Marian Brestic 3,7 , Disna Ratnasekera 8 , Laura Lamilla-Tamayo 3 , Ibrahim Al-Ashkar 9,10 and Ayman EL Sabagh 11,12* 1
Edited by: Rosa M. Rivero, Center for Edaphology and Applied Biology of Segura, Spanish National Research Council (CSIC), Spain Reviewed by: Yong-Goo Kim, Korea Research Institute of Bioscience and Biotechnology (KRIBB), South Korea Nobuhiro Suzuki, Sophia University, Japan *Correspondence: Ejaz Ahmad Waraich uaf_ewarraich@yahoo.com Ayman EL Sabagh aymanelsabagh@agr.kfs.edu.eg Specialty section: This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science Received: 21 September 2021 Accepted: 11 November 2021 Published: 15 December 2021 Citation: Ahmad M, Waraich EA, Skalicky M, Hussain S, Zulfiqar U, Anjum MZ, Habib ur Rahman M, Brestic M, Ratnasekera D, Lamilla-Tamayo L, Al-Ashkar I and EL Sabagh A (2021) Adaptation Strategies to Improve the Resistance of Oilseed Crops to Heat Stress Under a Changing Climate: An Overview. Front. Plant Sci. 12:767150. doi: 10.3389/fpls.2021.767150
Department of Agronomy, University of Agriculture, Faisalabad, Pakistan, 2 Horticultural Sciences Department, Tropical Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Homestead, FL, United States, 3 Department of Botany and Plant Physiology, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Prague, Czechia, 4 Department of Forestry and Range Management, University of Agriculture, Faisalabad, Pakistan, 5 Department of Agronomy, Muhammad Nawaz Shareef University of Agriculture, Multan, Pakistan, 6 Crop Science Group, Institute of Crop Science and Resource Conservation (INRES), University Bonn, Bonn, Germany, 7 Department of Plant Physiology, Slovak University of Agriculture, Nitra, Slovakia, 8 Department of Agricultural Biology, Faculty of Agriculture, University of Ruhuna, Kamburupitiya, Sri Lanka, 9 Department of Plant Production, College of Food and Agriculture, King Saud University, Riyadh, Saudi Arabia, 10 Agronomy Department, Faculty of Agriculture, Al-Azhar University, Cairo, Egypt, 11 Department of Field Crops, Faculty of Agriculture, Siirt University, Siirt, Turkey, 12 Department of Agronomy, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Shaikh, Egypt
Temperature is one of the decisive environmental factors that is projected to increase by 1. 5◦ C over the next two decades due to climate change that may affect various agronomic characteristics, such as biomass production, phenology and physiology, and yield-contributing traits in oilseed crops. Oilseed crops such as soybean, sunflower, canola, peanut, cottonseed, coconut, palm oil, sesame, safflower, olive etc., are widely grown. Specific importance is the vulnerability of oil synthesis in these crops against the rise in climatic temperature, threatening the stability of yield and quality. The natural defense system in these crops cannot withstand the harmful impacts of heat stress, thus causing a considerable loss in seed and oil yield. Therefore, a proper understanding of underlying mechanisms of genotype-environment interactions that could affect oil synthesis pathways is a prime requirement in developing stable cultivars. Heat stress tolerance is a complex quantitative trait controlled by many genes and is challenging to study and characterize. However, heat tolerance studies to date have pointed to several sophisticated mechanisms to deal with the stress of high temperatures, including hormonal signaling pathways for sensing heat stimuli and acquiring tolerance to heat stress, maintaining membrane integrity, production of heat shock proteins (HSPs), removal of reactive oxygen species (ROS), assembly of antioxidants, accumulation of compatible solutes, modified gene expression to enable changes, intelligent agricultural technologies, and several other agronomic techniques for thriving and surviving. Manipulation of multiple genes responsible for thermo-tolerance and exploring their high expressions greatly impacts their potential application using
CRISPR/Cas genome editing and OMICS technology. This review highlights the latest outcomes on the response and tolerance to heat stress at the cellular, organelle, and whole plant levels describing numerous approaches applied to enhance thermostolerance in oilseed crops. We are attempting to critically analyze the scattered existing approaches to temperature tolerance used in oilseeds as a whole, work toward extending studies into the field, and provide researchers and related parties with useful information to streamline their breeding programs so that they can seek new avenues and develop guidelines that will greatly enhance ongoing efforts to establish heat stress tolerance in oilseeds. Keywords: antioxidants, CRISPR/Cas9 technology, heat stress, oilseeds, omics technology, signaling, smart technologies, tolerance
exceeding the threshold level for an extended period that could cause injuries or irreversible damage to crop plants in general (Teixeira et al., 2013). Therefore, heat stress has proven to be a great menace and ever-looming threat to fruitful crop production around the globe (Hatfield and Dold, 2018; Tariq et al., 2018). The consequences of global climate change and spatial, temporal, and regional patterns are of considerable concern in agriculture production (Porter and Moot, 1998). Heat stress speeding up crop growth and not allowing the proper completion of crop growth stages results in immature development (Rahman et al., 2018a), perturbing carbon assimilation. This is an urgent matter, given that the geographical distribution of plant species depends to a large extent on their adaptation to different temperature zones (Keller and Seehausen, 2012). Additionally, the world population is expected to reach 9 billion by 2050. Agriculture production needs to be enhanced up to 70% regardless of climate change and its impacts on agriculture (Rahman et al., 2018b). However, all the growth stages in plants are affected adversely by heat stress right from germination to growth and development, reproductive phase, seed yield (Hasanuzzaman et al., 2013; Ahmad et al., 2016), and seed quality in oilseed crops (Ahmad et al., 2021a). The rise in global temperature will ultimately damage the ecosystem comprehensively (Kanojia and Dijkwel, 2018). Specifically, heat stress is a severe threat to oilseed crops as it impairs the production and quality of the yield; for example, the seed yield decreased up to 39% in camelina and 38% in canola under elevated temperature scenarios (Jumrani and Bhatia, 2018; Ahmad et al., 2021b). The temperature fluctuations have made it imperative to develop climate-resilient varieties that display better adaptability for growth under varied environmental conditions (Bhat et al., 2021). However, achieving this objective will be complicated by the fact that the performance of oilseeds may be hampered by environmental impacts related to climate change and the associated increase in pests and diseases, which are likely to become more challenging in the near future (Jaradat, 2016; Rahman et al., 2019). Therefore, hypothetically, several options can be used to achieve improvements in seed yield and related traits (either alone or in combination), increase seed oil content, or reduce seed yield losses due to abiotic stresses, including high temperature at the sensitive crop stage (Valantin-Morison
Oilseeds are ranked fourth in important food commodities after cereals, vegetables and melons, and fruits and nuts, and they occupy about 213 Mha of the world’s arable land (OECDFAO, 2020). However, the utilization and demand of oil crops continuously increases due to high population pressure, vagaries in dietary choices, cumulative global affluence, and the need for more renewable bio-products (Villanueva-Mejia and Alvarez, 2017). Vegetable oil is used as a biofuel, so it has a great future as an essential energy source (Lu et al., 2011). Factually, the primary sources of vegetable oils are oilseed crops, including rapeseed, soybean, cotton, peanut, palm oil, and sunflower (Abiodun, 2017), which are used in human diets as salad dressings, oil, margarine, frying oil, and numerous other products. Due to their specific chemical and physical properties, vegetable oil is an important feedstock used to produce multiple industrial materials, including promising applications such as biofuel and constituting an alternative to petroleum derivatives (Lu et al., 2011). Oilseed crops are a significant source of animal (Ponnampalam et al., 2019) and human nutrition (Rahman et al., 2018a) and industrial products (Liu et al., 2018a), and biodiesel production (Mohammad et al., 2018) has been increasing day by day. The quality and consumption of oilseed crops have been improved through different genetic engineering techniques (Tan et al., 2011). Numerous environmental stresses affecting plant growth and development have induced grave anxiety in the context of potential climate change. Across the globe, contemporary agriculture is facing unprecedented environmental pressure and stress due to climatic variability (Argosubekti, 2020). Plants’ growth in open environments faces several challenges, including heat, drought, cold, waterlogging, and salinity (Ashraf et al., 2018). Elevated temperature is one of the major concerns for the world as different models have predicted the rise of carbon dioxide (CO2 ), causing an increase in the ambient temperature leading to global warming (NOAA, 2017), which would have severe consequences on agriculture production systems across the globe. The Intergovernmental Panel on Climate Change (IPCC) estimates that the global ambient temperature will increase by 1.5◦ C from 2030 to 2052 (IPCC, 2018). Temperatureinduced heat stress is articulated as the shift in air temperature
membrane that stimulates the activation of Ca+2 channels in the plasma membrane resulting in oscillations of the cytosolic Ca+2 level. Ca+2 acts as a secondary messenger, and signals rely on Ca+2 sensors and others such as calcineurin B-like proteins (CBLs), calmodulin (CaMs), calmodulin-like proteins (CMLs), calcium-dependent protein kinases (CDPKs/CPKs), G proteincoupled receptors (GPCR), mitogen-activated protein kinase (MAPKs), pyrabactin resistance 1-like (PYR/PYL) protein, matrix metalloproteinases (MMPs), and other enzymes. For the most part, this mechanism of calcium detection has been elucidated in several models and also in oilseed plants.
and Meynard, 2008). The resilience of oilseed crops under heat stress is led by conventional breeding techniques, including hybridization, artificial selection, and induced mutagenesis; though, these methods are complicated due to the polyploid nature of oil crops and require extensive time and labor investments to accomplish (Yang et al., 2017). In the coming decades, the growing demand for oilseeds can be achieved by using advanced molecular breeding techniques such as complementary breeding tools, which would be very useful to accelerate all crop improvement programs to produce climateresilient crops. While transgenic approaches have so far been successfully used in oilseeds to improve a wide range of traits (Meesapyodsuk et al., 2018; Na et al., 2018; Shah et al., 2018; Kim et al., 2019; Wang et al., 2019), only a small number of these devices have made it to the market due to poor public perception as well as the disproportionately high cost and length of existing regulatory processes (Mall et al., 2018). Therefore, in this review, we aim to analyze recent results on the response and tolerance to heat stress at the cell, organelle, and whole plant level and describe the numerous approaches used to increase heat tolerance in oilseed crops.
Calmodulin and Calmodulin-Like Proteins CaM and CML-containing helix-loop-helix EF-hand domains are a family of Ca2+ sensors in plants and control downstream targets based on Ca2+ fluctuations (Lohani et al., 2020). Eighteen CAMTAs have been identified in B. napus, the maximum of any plant species reported to date (Rahman et al., 2016). Diversified expression of these BnaCaM/CML genes indicated significant roles in different tissues in response to stress conditions, including heat stress. It was critical in the upregulation of heat stress tolerance (He et al., 2020). These proteins played essential roles in 13 metabolic processes and cellular responses, including protein biosynthesis, carbohydrate metabolism, protein folding, signal transduction, carbon assimilation and assembly, cell cycle, energy pathway, cell defense and rescue, nitrogen metabolism, lipid metabolism, transcription regulation, amino acid metabolism, and secondary metabolite biosynthesis (Wang et al., 2012).
HEAT STRESS AND ITS THRESHOLD IN OILSEEDS In general, the threshold level is defined as a point after which some irreversible changes might occur. Therefore, the threshold level of heat stress is the moment after which plants lose their membrane stability. The scorching impact of high-temperature stress can be defined by the duration of exposure, the intensity of focus, and the degree of elevated temperature. Temperature limits of 35◦ C are considered heat stressors in tropics and subtropics (Bita and Gerats, 2013; Awais et al., 2017a; Ahmad et al., 2021a; Waraich et al., 2021a); however, temperatures above 25◦ C are thought to be stressors in rabi (winter) crops (Wahid et al., 2007; Abbas et al., 2017). The impact of high-temperature stress and the threshold temperatures of important oilseed crops at different growth stages is presented in Table 1.
Calcineurin B-Like Proteins In contrast to calmodulin, which regulates several proteins, calcineurin B-like proteins are apparently linked to calcineurin B-like protein kinases (CIPK) or SNF1-related protein kinases (SnRK3) (Chen et al., 2012). The structural composition of calcineurin B-like interacting protein kinases contains an Nterminal kinase catalytic domain. This junction domain links it to the highly variable C-terminal regulatory part (Chaves-Sanjuan et al., 2014). The C-terminal regulatory environment consists of the FISL motif with a unique 24 amino acid stretch, essential for the CBLCIPK binding (Albrecht et al., 2001). Yuan et al. (2014) stated the description of CBL and CIPK genes in B. napus and revealed the presence of 23 CIPKs and 7 CBLs. Interaction studies of BnCBL1-BnCIPK6 protein were established by bimolecular fluorescence complementation (BiFC) and its regulation under stressed conditions in B. napus (Chen et al., 2012).
HEAT STRESS SENSING AND SIGNALING A healthy plant needs a compact and robust network of interconnected systems that responds rapidly to stimuli, initiates metabolic responses, and exhibits unique plasticity to adapt to adverse conditions. Heat stress can affect plant functioning in various ways by destabilizing membrane fluidity, multiple proteins, transport systems, enzyme efficiency, RNA stability, and de-polymerization of the cytoskeleton (Hasanuzzaman et al., 2013). The adaptation process to stress is complex and occurs mechanistically through genes, metabolites, and proteins that are collectively involved in many regulatory pathways. The initial step of stress perception involves molecular or structural changes through which a signaling cascade is established, leading to membrane fluidity responses, adaptive changes in proteins, and alteration of DNA and RNA sequences (Lohani et al., 2020). The initial site of stress sensing is mostly the plasma
Calcium-Dependent Protein Kinase Calcium-dependent protein kinases act as a third component of the Ca2+ sensing apparatus in plants, functioning as a responder to various sensors with the ability to self-modify authorization through the action of various enzymes (Chen et al., 2012), making calcium-dependent protein kinases very important in their dual function of detecting Ca2+ and responding through phosphorylation events in opposition to high-temperature signals. There are multiple calcium-dependent protein kinase essentials to react to specific stress stimuli under
TABLE 1 | Effect of heat stress in different oilseed crops at different growth stages. Oilseed Heat stress/duration Impact on plant Growth stage