Recent Advances in the Roles of HSFs and HSPs in Heat Stress Response in Woody Plants

A continuous increase in ambient temperature caused by global warming has been considered a worldwide threat. As sessile organisms, plants have evolved sophisticated heat shock response (HSR) to respond to elevated temperatures and other abiotic stresses, thereby minimizing damage and ensuring the protection of cellular homeostasis. In particular, for perennial trees, HSR is crucial for their long life cycle and development. HSR is a cell stress response that increases the number of chaperones including heat shock proteins (HSPs) to counter the negative effects on proteins caused by heat and other stresses. There are a large number of HSPs in plants, and their expression is directly regulated by a series of heat shock transcription factors (HSFs). Therefore, understanding the detailed molecular mechanisms of woody plants in response to extreme temperature is critical for exploring how woody species will be affected by climate changes. In this review article, we summarize the latest findings of the role of HSFs and HSPs in the HSR of woody species and discuss their regulatory networks and cross talk in HSR. In addition, strategies and programs for future research studies on the functions of HSFs and HSPs in the HSR of woody species are also proposed.

Background:

A continuous increase in ambient temperature caused by global warming has been considered a worldwide threat. As sessile organisms, plants have evolved sophisticated heat shock response (HSR) to respond to elevated temperatures and other abiotic stresses, thereby minimizing damage and ensuring the protection of cellular homeostasis. In particular, for perennial trees, HSR is crucial for their long life cycle and development. HSR is a cell stress response that increases the number of chaperones including heat shock proteins (HSPs) to counter the negative effects on proteins caused by heat and other stresses. There are a large number of HSPs in plants, and their expression is directly regulated by a series of heat shock transcription factors (HSFs). Therefore, understanding the detailed molecular mechanisms of woody plants in response to extreme temperature is critical for exploring how woody species will be affected by climate changes.

Methods:

N/A - Review article

Results:

Heat shock proteins are found in all living organisms and are classified into at least six different types based on their molecular weight: sHSPs, HSP40s, HSP60s, HSP70s, HSP90s, and HSP100s. Massive production of HSPs in plants is a major characteristic response for the acquisition of thermotolerance. Small heat stress protein is a class of alpha-crystallin domain (ACD) chaperons with a molecular mass of 15–30 kDa. According to sequence homology and subcellular localization, sHSPs are classified into 11 different classes. Class I–VI sHSPs are localized in the nucleus or cytoplasm, and the rest five classes of sHSPs are localized in mitochondria, chloroplasts, peroxisomes, or ER. Most studies have focused on the class I cytoplasmic sHSP and have divulged that sHSPs are involved in regulating thermotolerance in woody plants, such as RcHSP17.8 in Rosa chinensis, ThHSP18.3 in Tamarix hispida, PtHSP17.8 in Populus trichocarpa, CsHSP17.2 in Camellia sinensis, and MsHSP16.9 in Malus sieversii. Among these genes, RcHSP17.8 confers resistance to various stresses in E. coli, yeast, and Arabidopsis. Overexpression of RcHSP17.8 in transgenic tobacco seedlings exhibits significant resistance to high temperatures and osmotic stresses, manifested by low electrolyte leakage and higher proline content under stress conditions. Heterologous expression of ThHSP18.3 protects yeast cells from salt, drought, heavy metals, and extreme temperatures. Overexpression of PtHSP17.8 in Arabidopsis increases survival rate and root length under heat and salt stresses. The CsHSP17.2 in C. sinensis acts as a molecular chaperone to mediate heat tolerance by maintaining maximum photochemical efficiency and protein synthesis, enhancing the scavenging of reactive oxygen species (ROS), and inducing the expression of heat-responsive (HR) genes. Overexpression of M. sieversii MsHSP16.9 in Arabidopsis improves the tolerance of a plant to heat by alleviating the damages of ROS and regulating the expression levels of stress-related genes. Moreover, cytoplasmic class II and III sHSPs have also been reported to be involved in the HSR in woody species. For example, SpHSP17.3, a cytoplasmic class II sHSP gene from Sorbus pohuashanensis, responds to high temperature, salt, and drought stresses. Overexpression of a Prunus mume cytoplasmic class III sHSP gene (PmHSP17.9) improves the thermotolerance of transgenic plants.

Data Summary:

Heat shock proteins are classified into at least six different types based on molecular weight. Small heat stress proteins have a molecular mass of 15–30 kDa and are classified into 11 different classes. Among the examples, RcHSP17.8 confers resistance to various stresses in E. coli, yeast, and Arabidopsis. Overexpression of PtHSP17.8 increases survival rate and root length under heat and salt stresses. Overexpression of CsHSP17.2 maintains maximum photochemical efficiency and enhances ROS scavenging. Overexpression of MsHSP16.9 alleviates ROS damage and regulates stress-related gene expression.

Conclusions:

In this review article, we summarize the latest findings of the role of HSFs and HSPs in the HSR of woody species and discuss their regulatory networks and cross talk in HSR. Unraveling this underlying interconnected mechanism will help to understand the complex regulatory networks of the fitness and adaptive advantage of higher plants. Strategies and programs for future research studies on the functions of HSFs and HSPs in the HSR of woody species are also proposed.

Practical Significance:

Perennial woody plants are greatly significant components of the global ecosystem and play a key role in limiting the emissions of carbon dioxide (CO2) and other greenhouse gases. In addition, woody plants are the main biomass resources for biofuels. Understanding the detailed molecular mechanisms of woody plants in response to extreme temperature is critical for exploring how woody species will be affected by climate changes, which can inform breeding and management strategies to enhance heat tolerance in economically and ecologically important woody species.