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Plant Responses to Heat Stress: Physiology, Transcription, Noncoding Rnas, and Epigenetics

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Plant Responses to Heat Stress: Physiology, Transcription, Noncoding Rnas, and Epigenetics International Journal of Molecular Sciences Review Plant Responses to Heat Stress: Physiology, Transcription, Noncoding RNAs, and Epigenetics Jianguo Zhao 1,2,†, Zhaogeng Lu 1,†, Li Wang 1 and Biao Jin 1,* 1 College of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, China; [email protected] (J.Z.); [email protected] (Z.L.); [email protected] (L.W.) 2 Guangling College of Yangzhou University, Yangzhou University, Yangzhou 225009, China * Correspondence: [email protected] † These authors contributed equally to this work. Abstract: Global warming has increased the frequency of extreme high temperature events. High temperature is a major abiotic stress that limits the growth and production of plants. Therefore, the plant response to heat stress (HS) has been a focus of research. However, the plant response to HS involves complex physiological traits and molecular or gene networks that are not fully understood. Here, we review recent progress in the physiological (photosynthesis, cell membrane thermostability, oxidative damage, and others), transcriptional, and post-transcriptional (noncoding RNAs) regulation of the plant response to HS. We also summarize advances in understanding of the epigenetic regulation (DNA methylation, histone modification, and chromatin remodeling) and epigenetic memory underlying plant–heat interactions. Finally, we discuss the challenges and opportunities of future research in the plant response to HS. Keywords: heat stress; physiological; molecular; non-coding RNA; epigenetics 1. Introduction Plants as sessile organisms cannot move to favorable environments upon encountering Citation: Zhao, J.; Lu, Z.; Wang, L.; abiotic or biotic stresses; consequently, plant growth, development, and productivity are Jin, B. Plant Responses to Heat Stress: markedly affected [1]. High temperature is an important stress and global warming has Physiology, Transcription, Noncoding RNAs, and Epigenetics. Int. J. Mol. accelerated the increase in air temperature in recent decades [2]. Therefore, the mechanisms Sci. 2021, 22, 117. https://dx.doi.org/ by which plants respond to high temperature are of great interest. Plants exposed to high 10.3390/ijms22010117 temperature (heat stress, HS) suffer from severe, and sometimes lethal, adverse effects. To cope with such conditions, plants have evolved sophisticated mechanisms to respond to HS. Received: 27 October 2020 For example, several basic physiological processes of plants—including photosynthesis, Accepted: 20 November 2020 respiration, and water metabolism—respond to HS [3,4]. Much progress has been made in Published: 24 December 2020 characterizing HS-responsive genes, non-coding RNAs, DNA methylation, and histone modifications. Here, we focus on the physiological, transcriptional, post-transcriptional, Publisher’s Note: MDPI stays neu- and epigenetic mechanisms underlying the plant HS response. tral with regard to jurisdictional claims in published maps and institutional 2. Physiological Responses of Plants under HS affiliations. A variety of physiological processes—such as photosynthesis, respiration, transpira- tion, membrane thermostability, and osmotic regulation—are adversely affected by HS. Some common effects of HS on plant physiological responses, growth and development, Copyright: © 2020 by the authors. Li- and yield are shown in Figure1. censee MDPI, Basel, Switzerland. This 2.1. Photosynthesis article is an open access article distributed under the terms and conditions of the Generally, HS reduces photosynthetic efficiency, thus shortening the plant life cycle Creative Commons Attribution (CC BY) and diminishing productivity [5]. Photosynthesis is also one of the most heat-sensitive license (https://creativecommons.org/ physiological processes. Under HS, photochemical reactions in thylakoid lamellae and licenses/by/4.0/). carbon metabolism in the stroma of chloroplasts are prone to injury [6,7]. Heat stress Int. J. Mol. Sci. 2021, 22, 117. https://dx.doi.org/10.3390/ijms22010117 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 117 2 of 14 causes disruption of thylakoid membranes, thereby inhibiting the activities of membrane- associated electron carriers and enzymes, reducing the rate of photosynthesis. Specifically, photosystem II (PSII) activity is greatly reduced or even stops under HS because PSII complex is the most heat-intolerant [6,8]. In addition, HS influences chloroplast structure and the thermal stability of components of the photosynthetic system, reducing ribulose- 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity, amounts of photosynthetic pigments, and the carbon fixation capacity [6,9,10]. These factors contribute significantly to the reduction of photosynthetic efficiency under HS. Therefore, a fundamental understand- ing of the response of photosynthetic physiology is helpful to study the thermostability of Int. J. Mol. Sci. 2020, 21, x FORplants PEER and REVIEW the adverse effects of warming on crop yield [11]. 2 of 15 Figure 1. EffectsFigure of1. heatEffects stress of onheat plant stress physiological on plant physiologica responses.l Upward-pointing responses. Upward-pointing arrows indicate arrows activated/upregulated indicate physiologicalactivated/upregulated indices. Downward-pointing physiological arrows indicateindice deactivated/downregulateds. Downward-pointing physiologicalarrows indicate indices. Abbrevi- ations: HS,deactivated/downregulated heat stress; PSII, photosystem physiological II; Rubisco, indices. ribulose-1,5-bisphosphate Abbreviations: HS, heat carboxylase/oxygenase; stress; PSII, photosystem ROS, reactive oxygen species.II; Rubisco, ribulose-1,5-bisphosphate carboxylase/oxygenase; ROS, reactive oxygen species. 2.1. Photosynthesis 2.2. Cell Membrane Thermostability Generally, HS reducesMembrane photosynthetic dysfunction efficien is thecy, main thus physiologicalshortening the consequence plant life ofcycle plant and exposure to diminishing productivityHS. Under [5]. Phot extremeosynthesis HS, the is increased also one kinetic of the energy most andheat-sensitive movement physiological of biomolecules across membranes loosens chemical bonds, leading to disintegration of membrane lipids and processes. Under HS, photochemical reactions in thylakoid lamellae and carbon metabolism in the increasing membrane fluidity [12]. HS increases cellular membrane permeability and stroma of chloroplasts are prone to injury [6,7]. Heat stress causes disruption of thylakoid the loss of cellular electrolytes, consequently inhibiting cellular function and decreasing membranes, thereby inhibiting the activities of membrane-associated electron carriers and enzymes, thermotolerance [5]. In addition, the reactive oxygen species (ROS) accumulation caused reducing the rate of photby HSosynthesis. leads to membrane Specifically, damage, photosystem decreasing II (PSII) thermotolerance activity is greatly [13]. reduced In short, or membrane even stops under HS thermostabilitybecause PSII complex plays anis the important most heat-intolerant role in conferring [6,8]. toleranceIn addition, to HSHS ininfluences plants. chloroplast structure and the thermal stability of components of the photosynthetic system, reducing ribulose-1,5-bisphosphate2.3. Oxidative carboxylase/oxygenase Damage (Rubisco) activity, amounts of photosynthetic 1 pigments, and the carbonPlants fixation exposed capacity to HS [6 show,9,10]. accumulation These factors of contribute ROS—singlet significantly oxygen ( Oto2 ),the superoxide − − reduction of photosyntheticradical (O efficiency2 ), hydrogen under peroxideHS. Therefore, (H2O2 ),a andfundamental hydroxyl radicalunderstanding (OH )—generating of the ox- response of photosyntheticidative stressphysiology [14]. The is helpful ROS are to generated study the mainly thermostability in PSI and of PSII. plants In PSII, and excess the energy adverse effects of warmingeneratesg on crop the triplet yield state[11]. of chlorophylls, which pass excitation energy to O2, producing singlet oxygen. Over-reduction of PSI leads to generation of the superoxide anion, pro- − 2.2. Cell Membrane Thermostabilitymoting H2O 2 production [8]. ROS (e.g., O2 ,H2O2) induce oxidative stress by altering membrane properties, degrading proteins, and inactivating enzymes, thus reducing plant Membrane dysfunctioncell viability is the [15 main]. Heat physiological stress induces consequence lipid peroxidation of plant dueexposure to free to radical HS. Under damage of the extreme HS, the increasedcell membrane kinetic energy [6]. Under and move HS, thement content of biomolecules of malondialdehyde across membranes (MAD; an loosens indicator of lipid chemical bonds, leadingperoxidation) to disintegration is significantly of membrane increased lipids in and many increasing plants such membrane as sorghum fluidity [16]. [12]. ROS can also HS increases cellulartrigger membrane programmed permeability cell death and under the loss HS. Onof cellular the other electrolytes, hand, plants consequently have developed mech- inhibiting cellular funcanismstion toand detoxify decreasing ROS andthermotolerance enhance heat tolerance.[5]. In addition, Plants increasethe reactive their oxygen thermotolerance species (ROS) accumulation caused by HS leads to membrane damage, decreasing thermotolerance [13]. In short, membrane thermostability plays an important role in conferring tolerance to HS in plants. 2.3. Oxidative Damage Plants exposed to HS show accumulation of ROS—singlet oxygen (1O2), superoxide radical (O2−), hydrogen peroxide
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