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NFXL1 functions as a transcriptional activator required for thermotolerance at reproductive stage in Arabidopsis

Journal of Integrative Plant Biology 2024年第1期66卷 54-65页

作者： Qiao‐Yun Zhu Lin‐Lin Zhang Jian‐Xiang Liu State Key Laboratory of Plant Environmental Resilience College of Life SciencesZhejiang UniversityHangzhou 310027China

Plants are highly susceptible to abiotic stresses,particularly heat stress during the reproductive stage.However,the specific molecular mechanisms underlying this sensitivity remain largely unknown.In the current study,we demonstrate that the Nuclear Transcription Factor,X-box Binding Protein 1-Like 1(NFXL1),directly regulates the expression of DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEIN 2A(DREB2A),which is crucial for reproductive thermotolerance in Arabidopsis.NFXL1 is upregulated by heat stress,and its mutation leads to a reduction in silique length(seed number)under heat stress conditions.RNA-Seq analysis reveals that NFXL1 has a global impact on the expression of heat stress responsive genes,including DREB2A,Heat Shock Factor A3(HSFA3)and Heat Shock Protein 17.6(HSP17.6)in flower buds.Interestingly,NFXL1 is enriched in the promoter region of DREB2A,but not of either HSFA3 or HSP17.6.Further experiments using electrophoretic mobility shift assay have confirmed that NFXL1 directly binds to the DNA fragment derived from the DREB2A promoter.Moreover,effector-reporter assays have shown that NFXL1 activates the DREB2A promoter.The DREB2A mutants are also heat stress sensitive at the reproductive stage,and DEREB2A is epistatic to NFXL1 in regulating thermotolerance in flower buds.It is known that HSFA3,a direct target of DREB2A,regulates the expression of heat shock proteins genes under heat stress conditions.Thus,our findings establish NFXL1 as a critical upstream regulator of DREB2A in the transcriptional cassette responsible for heat stress responses required for reproductive thermotolerance in Arabidopsis.

关键词： Arabidopsis DREB2A heat stress NFXL1 reproductive thermotolerance

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Heat-inducible SlWRKY3 confers thermotolerance by activating the SlGRXS1 gene cluster in tomato

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Horticultural Plant Journal 2024年第2期10卷 515-531页

作者： Ying Wang Wenxian Gai Liangdan Yuan Lele Shang Fangman Li Zhao Gong Pingfei Ge Yaru Wang Jinbao Tao Xingyu Zhang Haiqiang Dong Yuyang Zhang National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops Huazhong Agricultural UniversityWuhanHubei 430070China Hubei Hongshan Laboratory WuhanHubei 430070China

High temperature stress is one of the major environmental factors that affect the growth and development of plants. Although WRKY transcription factors play a critical role in stress responses, there are few studies on the regulation of heat stress by WRKY transcription factors,especially in tomato. Here, we identified a group I WRKY transcription factor, SlWRKY3, involved in thermotolerance in tomato. First, SlWRKY3 was induced and upregulated under heat stress. Accordingly, overexpression of SlWRKY3 led to an increase, whereas knock-out of SlWRKY3 resulted in decreased tolerance to heat stress. Overexpression of SlWRKY3 accumulated less reactive oxygen species(ROS), whereas knock-out of SlWRKY3 accumulated more ROS under heat stress. This indicated that SlWRKY3 positively regulates heat stress in tomato. In addition,SlWRKY3 activated the expression of a range of abiotic stress-responsive genes involved in ROS scavenging, such as a SlGRXS1 gene cluster.Further analysis showed that SlWRKY3 can bind to the promoters of the SlGRXS1 gene cluster and activate their expression. Collectively, these results imply that SlWRKY3 is a positive regulator of thermotolerance through direct binding to the promoters of the SlGRXS1 gene cluster and activating their expression and ROS scavenging.

关键词： Tomato WRKY transcription factor SlWRKY3 thermotolerance SlGRXS1 Gene cluster Abiotic stress

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两种富含甘氨酸的RNA结合蛋白参与选择性剪接实现对水稻耐热性的昼夜节律调控

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Science Bulletin 2024年第1期69卷 59-71页

作者：杨闯罗安妮芦海平 Seth Jon Davis 刘建祥 State Key Laboratory of Plant Environmental Resilience College of Life SciencesZhejiang UniversityHangzhou 310027China Department of Biology University of YorkYork YO105DDUK

Rice(Oryza sativa L.)production is threatened by global warming associated with extreme high temperatures,and rice heat sensitivity is differed when stress occurs between daytime and nighttime.However,the underlying molecular mechanism are largely unknown.We show here that two glycine-rich RNA binding proteins,Os GRP3 and Os GRP162,are required for thermotolerance in rice,especially at nighttime.The rhythmic expression of Os GRP3/Os GRP162 peaks at midnight,and at these coincident times,is increased by heat stress.This is largely dependent on the evening complex component Os ELF3-2.We next found that the double mutant of Os GRP3/Os GRP162 is strikingly more sensitive to heat stress in terms of survival rate and seed setting rate when comparing to the wild-type plants.Interestingly,the defect in thermotolerance is more evident when heat stress occurred in nighttime than that in daytime.Upon heat stress,the double mutant of Os GRP3/Os GRP162 displays globally reduced expression of heat-stress responsive genes,and increases of m RNA alternative splicing dominated by exon-skipping.This study thus reveals the important role of Os GRP3/Os GRP162 in thermotolerance in rice,and unravels the mechanism on how Os GRP3/Os GRP162 regulate thermotolerance in a diurnal manner.

关键词： Alternative splicing Diurnal regulation Glycine-rich protein Oryza sativa L. thermotolerance

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SYP-5 regulates meiotic thermotolerance in Caenorhabditis elegans

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Journal of Molecular Cell Biology 2021年第9期13卷 662-675页

作者： Yuanyuan Liu Qiuchen Zhao Hui Nie Fengguo Zhang Tingting Fu Zhenguo Zhang Feifei Qi Ruoxi Wang Jun Zhou Jinmin Gao Institute of Biomedical Sciences College of Life SciencesKey Laboratory of Animal Resistance Biology of Shandong ProvinceShandong Normal UniversityJinan 250014China

Meiosis produces the haploid gametes required by all sexually reproducing organisms,occurring in specific temperature ranges in different organisms.However,how meiotic thermotolerance is regulated remains largely unknown.Using the model organism Caenorhabditis elegans,here,we identified the synaptonemal complex(SC)protein SYP-5 as a critical regulator of meiotic thermotolerance.syp-5-null mutants maintained a high percentage of viable progeny at 20℃ but produced significantly fewer viable progeny at 25℃,a permissive temperature in wild-type worms.Cytological analysis of meiotic events in the mutants revealed that while SC assembly and disassembly,as well as DNA double-strand break repair kinetics,were not affected by the elevated temperature,crossover designation,and bivalent formation were significantly affected.More severe homolog segregation errors were also observed at elevated temperature.A temperature switching assay revealed that late meiotic prophase events were not temperature-sensitive and that meiotic defects during pachytene stage were responsible for the reduced viability of syp-5 mutants at the elevated temperature.Moreover,SC polycomplex formation and hexanediol sensitivity analysis suggested that SYP-5 was required for the normal properties of the SC,and charge-interacting elements in SC components were involved in regulating meiotic thermotolerance.Together,these findings provide a novel molecular mechanism for meiotic thermotolerance regulation.

关键词： meiosis thermotolerance synaptonemal complex crossover regulation Caenorhabditis elegans SYP-5

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Overexpression of Sweet Pepper Glycerol-3-Phosphate Acyltransferase Gene Enhanced thermotolerance of Photosynthetic Apparatus in Transgenic Tobacco

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Journal of Integrative Plant Biology 2008年第5期50卷 613-621页

作者： Kun Yan Na Chen Yan-Yan Qu Xin-Chun Dong Qing-Wei Meng Shi-Jie Zhao College of Life Sciences State Key Laboratory of Crop Biology Shandong Agricultural University Tai'an 271018 China

In order to investigate the relationship between the lipid composition in thylakoid membrane and thermostability of photosynthetic apparatus, tobacco transformed with sweet pepper sense glycerol-3-phosphate acyltransferase （GPAT） gene were used to analyze the lipid composition in thylakoid membrane, the net photosynthetic rate and chlorophyll fluorescence parameters under high temperature stress. The results showed that the saturated extent of monogalactosyldiacylglycerol （MGDG）, sulfoquinovosyldiacylglycerol, digalactosyldiacylglycerol and phosphatidylglycerol in thylakoid membrane of transgenic tobacco T1 lines increased generally. Particularly, the saturated extent in MGDG increased obviously by 16.2% and 12.6% in T1-2 and T1-1, respectively. With stress temperature elevating, the maximum efficiency of photosystem Ⅱ （PSⅡ） photochemistry （Fv/Fm）, actual photochemical efficiency of PSll in the light （ФPSⅡ） and net photosynthetic rate （Pn） of the two lines and wild type tobacco plants decreased gradually, but those parameters decreased much less in transgenic plants. Even though the recovery process appeared differently in the donor and acceptor side of PSⅡ in transgenic tobacco compared with wild-type plants, the entire capability of PSⅡ recovered faster in transgenic tobacco, which was shown in the parameters of PI, Fv/Fm and ФPSⅡ, as a result, the recovery of Pn was accelerated. Conclusively, we proposed that the increase in saturated extent of thylakoid membrane lipids in transgenic plants enhanced the stability of photosynthetic apparatus under high temperature stress.

关键词： glycerol-3-phosphate transferase lipids in thylakoid membrane photosynthesis thermotolerance tobacco.

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Brassinosteroids promote thermotolerance through releasing BIN2-mediated phosphorylation and suppression of HsfA1 transcription factors in Arabidopsis

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Plant Communications 2022年第6期3卷 282-298页

作者： Jinyu Luo Jianjun Jiang Shiyong Sun Xuelu Wang College of Life Science and Technology Huazhong Agricultural UniversityWuhan 430070China State Key Laboratory of Crop Stress Adaptation and Improvement Henan UniversityKaifeng 475004China Sanya Institute of Henan University Sanya 572025China

High temperature adversely affects plant growth and development.The steroid phytohormones brassinosteroids(BRs)are recognized to play important roles in plant heat stress responses and thermotolerance,but the underlying mechanisms remain obscure.Here,we demonstrate that the glycogen synthase kinase 3(GSK3)-like kinase BRASSINOSTEROID INSENSITIVE2(BIN2),a negative component in the BR signaling pathway,interacts with the master heat-responsive transcription factors CLASS A1 HEAT SHOCK TRANSCRIPTION FACTORS(HsfA1s).Furthermore,BIN2 phosphorylates HsfA1d on T263 and S56 to suppress its nuclear localization and inhibit its DNA-binding ability,respectively.BR signaling promotes plant thermotolerance by releasing the BIN2 suppression of HsfA1d to facilitate its nuclear localization and DNA binding.Our study provides insights into the molecular mechanisms by which BRs promote plant thermotolerance by strongly regulating HsfA1d through BIN2 and suggests potential ways to improve crop yield under extreme high temperatures.

关键词： brassinosteroids thermotolerance BIN2 HsfA1d phosphorylation

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GABA Enhances thermotolerance of Seeds Germination by Attenuating the ROS Damage in Arabidopsis

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Phyton-International Journal of Experimental Botany 2020年第3期89卷 619-631页

作者： Qili Zhang Danni He Songbei Ying Shiyan Lu Jiali Wei Ping Li Shanghai Key Laboratory of Bio-Energy Crops Research Center for Natural ProductsPlant Science CenterSchool of Life SciencesShanghai UniversityShanghai200444China

Seeds germination is strictly controlled by environment factor such as high temperature(HT)through altering the balance between gibberellin acid(GA)and abscisic acid(ABA).Gama-aminobutyric acid(GABA)is a small molecule with four-carbon amino acid,which plays a crucial role during plant physiological process associated with pollination,wounding or abiotic stress,but its role in seeds germination under HT remains elusive.In this study we found that HT induced the overaccumulation of ROS,mainly H_(2)O_(2) and O_(2)^(-),to suppress seeds germination,meanwhile,HT also activated the enzyme activity of GAD for the rapid accumulation of GABA,hinting the regulatory function of GABA in con-trolling seeds germination against HT stress.Applying GABA directly attenuated HT-induced ROS accumulation,upregulated GA biosynthesis and downregulated ABA biosynthesis,ultimately enhanced seeds germination.Consistently,genetic analysis using the gad1/2 mutant defective in GABA biosynthesis,or pop2-5 mutant with high endogenous GABA content supported the potential function of GABA in improving seeds germination tolerance to HT through scavenging ROS overaccumulation.Based on these data,we propose that GABA acts as a novel signal to enhance thermotolerance of seeds germination through alleviating the ROS damage to seeds viability.

关键词： GABA thermotolerance ROS damage seeds germination

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Co-chaperoning of chlorophyll and carotenoid biosynthesis by ORANGE family proteins in plants

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Molecular Plant 2023年第6期16卷 1048-1065页

作者： Tianhu Sun Peng Wang Sombir Rao Xuesong Zhou Emalee Wrightstone Shan Lu Hui Yuan Yong Yang Tara Fish Theodore Thannhauser Jiping Liu Michael Mazourek Bernhard Grimm Li Li Robert W.Holley Center for Agriculture and Health USDA-ARSCornell UniversityIthacaNY 14853USA Plant Breeding and Genetics Section School of Integrative Plant ScienceCornell UniversityIthacaNY 14853UA Department of Plant Physiology Institute of BiologyHumboldt-Universitat zu Berlin10115 BerlinGermany School of Biological Sciences The University of Hong KongPokfulam RoadHong Kong 999077China State Key Laboratory of Pharmaceutical Biotechnology School of Life SciencesNanjing UniversityNanjng 210023China

Chlorophylls and carotenoids are essential photosynthetic pigments.Plants spatiotemporally coordinate the needs of chlorophylls and carotenoids for optimal photosynthesis and fitness in response to diverse environmental and developmental cues.However,how the biosynthesis pathways of these two pigments are coordinated,particularly at posttranslational level to allow rapid control,remains largely unknown.Here,we report that the highly conserved ORANGE(OR)family proteins coordinate both pathways via posttranslationally mediating the first committed enzyme in each pathway.We demonstrate that OR family proteins physically interact with magnesium chelatase subunit I(CHLI)in chlorophyll biosynthesis pathway in addition to phytoene synthase(PSY)in carotenoid biosynthesis pathway and concurrently stabilize CHLI and PSY enzymes.We show that loss of OR genes hinders both chlorophyll and carotenoid biosynthesis,limits light-harvesting complex assembly,and impairs thylakoid grana stacking in chloroplasts.Overexpression of OR safeguards photosynthetic pigment biosynthesis and enhances thermotolerance in both Arabidopsis and tomato plants.Our findings establish a novel mechanism by which plants coordinate chlorophyll and carotenoid biosynthesis and provide a potential genetic target to generate climate-resilient crops.

关键词： photosynthetic pigments chlorophylls carotenoids OR family proteins CHLl PSY thermotolerance

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The spliceophilin CYP18-2 is mainly involved in the splicing of retained introns under heat stress in Arabidopsis

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Journal of Integrative Plant Biology 2023年第5期65卷 1113-1133页

作者： Areum Lee Hyun Ji Park Seung Hee Jo Haemyeong Jung Hyun-Soon Kim Hyo-Jun Lee Youn-Sung Kim Choonkyun Jung Hye Sun Cho Plant Systems Engineering Research Center Korea Research Institute of Bioscience and Biotechnology(KRIBB)Daejeon 34141Korea Department of Biosystems and Bioengineering KRIBB School of BiotechnologyUniversity of Science and Technology(UST)Daejeon 34141Korea Department of Functional Genomics KRIBB School of BioscienceUSTDaejeon 34113Korea Department of Biotechnology NongWoo BioAnseong 17558Korea Department of International Agricultural Technology and Crop Biotechnology Institute/Green Bio Science and Technology Seoul National UniversityPyeongchang 25354Korea Department of Agriculture Forestryand Bioresources and Integrated Major in Global Smart FarmCollege of Agriculture and Life SciencesSeoul National UniversitySeoul 08826Korea

Peptidyl-prolyl isomerase-like 1(PPIL1)is associated with the human spliceosome complex.However,its function in pre-mRNA splicing remains unclear.In this study,we show that Arabidopsis thaliana CYCLOPHILIN 18-2(AtCYP18-2),a PPIL1 homolog,plays an essential role in heat tolerance by regulating pre-mRNA splicing.Under heat stress conditions,AtCYP18-2 expression was upregulated in mature plants and GFP-tagged AtCYP18-2 redistributed to nuclear and cytoplasmic puncta.We determined that AtCYP18-2 interacts with several spliceosome complex B^(ACT)components in nuclear puncta and is primarily associated with the small nuclear RNAs U5 and U6 in response to heat stress.The AtCYP18-2 loss-of-function allele cyp18-2 engineered by CRISPR/Cas9-mediated gene editing exhibited a hypersensitive phenotype to heat stress relative to the wild type.Moreover,global transcriptome profiling showed that the cyp18-2 mutation affects alternative splicing of heat stress–responsive genes under heat stress conditions,particularly intron retention(IR).The abundance of most intron-containing transcripts of a subset of genes essential for thermotolerance decreased in cyp18-2 compared to the wild type.Furthermore,the intron-containing transcripts of two heat stress-related genes,HEAT SHOCK PROTEIN 101(HSP101)and HEAT SHOCK FACTOR A2(HSFA2),produced functional proteins.HSP101-IR-GFP localization was responsive to heat stress,and HSFA2-Ⅲ-IR interacted with HSF1 and HSP90.1 in plant cells.Our findings reveal that CYP18-2 functions as a splicing factor within the B~(ACT)spliceosome complex and is crucial for ensuring the production of adequate levels of alternatively spliced transcripts to enhance thermotolerance.

关键词： alternative splicing CYP18-2 HSFA2-Ⅲ intron retention spliceophilin spliceosome complex B~(ACT) thermotolerance

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Plant VOCs emission： a new strategy of thermotolerance

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Journal of Forestry Research 2005年第4期16卷 323-326页

作者： CHEN Jun-wen CAO Kun-fang Xishuangbanna Tropical Botanical Garden the Chinese Academy of Sciences Mengla Yunnan 666303 P. R. China Graduate school the Chinese Academy of Sciences Beijing 100039 R R. China

Plant leaves may emit a substantial amount of volatile organic compounds （VOCs） into the atmosphere, which include isoprene, terpene, alkanes, alkenes, alcohols, aldehydes, eters, esters and carboxylic acids. Furthermore, most of these compounds actively participate in tropospheric chemistry. Great progresses have been made in linking emission of these compounds to climate. However, the VOCs emission function in plant is still not clear. Recently, some evidence has emerged that the production and the emission of VOCs, such as isoprene and monoterpenes, which account for 80% of total VOCs, exhibit plant protection against high temperatures. These increases in VOCs emissions could contribule in a significant way to plant thermotolerance. This perspective summarizes some latest literatures regarding the VOCs emission-dependent thermoprotection in plant species subjected to high temperature stress, presents the achievement in studies concerning plant VOCs emission-dependent thermotolerance, and then exhibits the proposed mechanisms of such plant thermotolerance. Finally open questions regarding the plant VOCs emission were shown, and the future researches were proposed.

关键词： Volatile Organic Compounds （VOCs） Isoprene Monoterpene Photosynthesis thermotolerance Thermoprotection

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