Natural variations of HSFA2 enhance thermotolerance in grapevine

Abstract Heat stress limits growth and development of crops including grapevine which is a popular fruit in the world. Genetic variability in crops thermotolerance is not well understood. We identified and characterized heat stress transcription factor HSFA2 in heat sensitive Vitis vinifera ‘Jingxiu’ (named as VvHSFA2) and heat tolerant Vitis davidii ‘Tangwei’ (named as VdHSFA2). The transcriptional activation activities of VdHSFA2 are higher than VvHSFA2, the variation of single amino acid (Thr315Ile) in AHA1 motif leads to the difference of transcription activities between VdHSFA2 and VvHSFA2. Based on 41 Vitis germplasms, we found that HSFA2 is differentiated at coding region among heat sensitive V. vinifera, and heat tolerant Vitis davidii and Vitis quinquangularis. Genetic evidence demonstrates VdHSFA2 and VvHSFA2 are positive regulators in grape thermotolerance, and the former can confer higher thermotolerance than the latter. Moreover, VdHSFA2 can regulate more target genes than VvHSFA2. As a target gene of both VdHSFA2 and VvHSFA2, overexpression of MBF1c enhanced the grape thermotolerance whereas dysfunction of MBF1c resulted in thermosensitive phenotype. Together, our results revealed that VdHSFA2 confers higher thermotolerance than VvHSFA2, and MBF1c acts as their target gene to induce thermotolerance. The VdHSFA2 may be adopted for molecular breeding in grape thermotolerance.

[1]  Myung-hee Kim,et al.  Overexpression of C-Repeat Binding Factor1 (CBF1) Gene Enhances Heat Stress Tolerance in Arabidopsis , 2022, Journal of Plant Biology.

[2]  Jianfu Jiang,et al.  Corrigendum to: Integrating Omics and Alternative Splicing Reveals Insights into Grape Response to High Temperature , 2022, Plant physiology.

[3]  Ewelina M. Sokolowska,et al.  Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis , 2021, Nature Communications.

[4]  D. Wong,et al.  GRAS-domain transcription factor PAT1 regulates jasmonic acid biosynthesis in grape cold stress response. , 2021, Plant physiology.

[5]  E. Gomès,et al.  Molecular Tools for Adapting Viticulture to Climate Change , 2021, Frontiers in Plant Science.

[6]  Xing Cao,et al.  LlWRKY39 is involved in thermotolerance by activating LlMBF1c and interacting with LlCaM3 in lily (Lilium longiflorum) , 2021, Horticulture research.

[7]  J. Gai,et al.  Comparative Transcriptomics Analysis and Functional Study Reveal Important Role of High-Temperature Stress Response Gene GmHSFA2 During Flower Bud Development of CMS-Based F1 in Soybean , 2020, Frontiers in Plant Science.

[8]  G. Banilas,et al.  Grapevine Responses to Heat Stress and Global Warming , 2020, Plants.

[9]  X. Fan,et al.  Identification of Heat Tolerance in Chinese Wildgrape Germplasm Resources , 2020 .

[10]  Chengcai Chu,et al.  Natural variations of SLG1 confer high-temperature tolerance in indica rice , 2020, Nature Communications.

[11]  L. Herrera-Estrella,et al.  Plant abiotic stress response and nutrient use efficiency , 2020, Science China Life Sciences.

[12]  H. Shao,et al.  TaHsfA2-1, a new gene for thermotolerance in wheat seedlings: Characterization and functional roles. , 2020, Journal of plant physiology.

[13]  Ricardo A. Chávez Montes,et al.  The plant MBF1 protein family: a bridge between stress and transcription , 2020, Journal of experimental botany.

[14]  Jigang Li,et al.  IbBBX24 Promotes the Jasmonic Acid Pathway and Enhances Fusarium Wilt Resistance in Sweet Potato , 2020, Plant Cell.

[15]  E. Schleiff,et al.  Natural variation in HsfA2 pre-mRNA splicing is associated with changes in thermotolerance during tomato domestication. , 2020, The New phytologist.

[16]  L. Zou,et al.  Cloning and Expression Analysis of the BocMBF1c Gene Involved in Heat Tolerance in Chinese Kale , 2019, International journal of molecular sciences.

[17]  M. Yi,et al.  Alternative Splicing Provides a Mechanism to Regulate LlHSFA3 Function in Response to Heat Stress in Lily1 , 2019, Plant Physiology.

[18]  A. B. Downie,et al.  Maize HSFA2 and HSBP2 antagonistically modulate raffinose biosynthesis and heat tolerance in Arabidopsis. , 2019, The Plant journal : for cell and molecular biology.

[19]  D. Wong,et al.  The ethylene response factor VaERF092 from Amur grape regulates the transcription factor VaWRKY33, improving cold tolerance. , 2019, The Plant journal : for cell and molecular biology.

[20]  Yucheng Wang,et al.  Arabidopsis heat shock transcription factor HSFA7b positively mediates salt stress tolerance by binding to an E-box-like motif to regulate gene expression , 2019, Journal of experimental botany.

[21]  Shaohua Li,et al.  VvWRKY8 represses stilbene synthase genes through direct interaction with VvMYB14 to control resveratrol biosynthesis in grapevine , 2018, Journal of experimental botany.

[22]  N. Suzuki,et al.  Integration between ROS Regulatory Systems and Other Signals in the Regulation of Various Types of Heat Responses in Plants , 2018, International journal of molecular sciences.

[23]  Xiping Wang,et al.  VlbZIP30 of grapevine functions in dehydration tolerance via the abscisic acid core signaling pathway , 2018, Horticulture Research.

[24]  Kang Gao,et al.  Molecular mechanisms governing plant responses to high temperatures. , 2018, Journal of integrative plant biology.

[25]  Shaohua Li,et al.  Genome-wide Identification and Classification of HSF Family in Grape, and Their Transcriptional Analysis under Heat Acclimation and Heat Stress , 2018, Horticultural Plant Journal.

[26]  E. Gomès,et al.  Dissecting the Biochemical and Transcriptomic Effects of a Locally Applied Heat Treatment on Developing Cabernet Sauvignon Grape Berries , 2017, Front. Plant Sci..

[27]  K. Shinozaki,et al.  Transcriptional Regulatory Network of Plant Heat Stress Response. , 2017, Trends in plant science.

[28]  Jiandong Wu,et al.  Ectopic overexpression of maize heat shock transcription factor gene ZmHsf04 confers increased thermo and salt-stress tolerance in transgenic Arabidopsis , 2017, Acta Physiologiae Plantarum.

[29]  R. Mittler,et al.  ABA is required for the accumulation of APX1 and MBF1c during a combination of water deficit and heat stress , 2016, Journal of experimental botany.

[30]  J. Brillouet,et al.  Temperature desynchronizes sugar and organic acid metabolism in ripening grapevine fruits and remodels their transcriptome , 2016, BMC Plant Biology.

[31]  Xingliang Ma,et al.  CRISPR/Cas9‐Based Multiplex Genome Editing in Monocot and Dicot Plants , 2016, Current protocols in molecular biology.

[32]  E. Schleiff,et al.  HsfA2 Controls the Activity of Developmentally and Stress-Regulated Heat Stress Protection Mechanisms in Tomato Male Reproductive Tissues1[OPEN] , 2016, Plant Physiology.

[33]  N. Movahed,et al.  The grapevine VviPrx31 peroxidase as a candidate gene involved in anthocyanin degradation in ripening berries under high temperature , 2016, Journal of Plant Research.

[34]  M. Mirzaei,et al.  Quantitative proteomic analysis of cabernet sauvignon grape cells exposed to thermal stresses reveals alterations in sugar and phenylpropanoid metabolism , 2015, Proteomics.

[35]  Qi Feng,et al.  Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice , 2015, Nature Genetics.

[36]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[37]  K. Shinozaki,et al.  Soybean DREB1/CBF-type transcription factors function in heat and drought as well as cold stress-responsive gene expression. , 2015, The Plant journal : for cell and molecular biology.

[38]  Xiaoli Geng,et al.  Overexpression of heat stress-responsive TaMBF1c, a wheat (Triticum aestivum L.) Multiprotein Bridging Factor, confers heat tolerance in both yeast and rice , 2014, Plant Molecular Biology.

[39]  Shaohua Li,et al.  Comparison of investigation methods of heat injury in grapevine (Vitis) and assessment to heat tolerance in different cultivars and species , 2014, BMC Plant Biology.

[40]  Xiping Wang,et al.  The grape VvMBF1 gene improves drought stress tolerance in transgenic Arabidopsis thaliana , 2014, Plant Cell, Tissue and Organ Culture (PCTOC).

[41]  Z. Gong,et al.  Reduced tolerance to abiotic stress in transgenic Arabidopsis overexpressing a Capsicum annuum multiprotein bridging factor 1 , 2014, BMC Plant Biology.

[42]  C. Romieu,et al.  Day and night heat stress trigger different transcriptomic responses in green and ripening grapevine (vitis vinifera) fruit , 2014, BMC Plant Biology.

[43]  J. Drenth,et al.  The heat shock factor family from Triticum aestivum in response to heat and other major abiotic stresses and their role in regulation of heat shock protein genes , 2013, Journal of experimental botany.

[44]  H. Hirt,et al.  Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2 , 2013, PeerJ.

[45]  E. Gomès,et al.  VvGOLS1 and VvHsfA2 are involved in the heat stress responses in grapevine berries. , 2012, Plant & cell physiology.

[46]  Marc D. Perry,et al.  ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia , 2012, Genome research.

[47]  I. Ebersberger,et al.  The plant heat stress transcription factor (Hsf) family: structure, function and evolution. , 2012, Biochimica et biophysica acta.

[48]  Y. Charng,et al.  The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. , 2011, Plant, cell & environment.

[49]  C. Casalongué,et al.  The analysis of an Arabidopsis triple knock-down mutant reveals functions for MBF1 genes under oxidative stress conditions. , 2010, Journal of plant physiology.

[50]  S. Delrot,et al.  A Sugar-Inducible Protein Kinase, VvSK1, Regulates Hexose Transport and Sugar Accumulation in Grapevine Cells , 2009, Plant Physiology.

[51]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[52]  Chuang Wang,et al.  Identification and expression analysis of OsHsfs in rice , 2009, Journal of Zhejiang University SCIENCE B.

[53]  Nobuhiro Suzuki,et al.  The Transcriptional Co-activator MBF1c Is a Key Regulator of Thermotolerance in Arabidopsis thaliana* , 2008, Journal of Biological Chemistry.

[54]  K. Oda,et al.  Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis , 2008, Planta.

[55]  Rongcheng Lin,et al.  Transposase-Derived Transcription Factors Regulate Light Signaling in Arabidopsis , 2007, Science.

[56]  K. Yamaguchi,et al.  High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. , 2007, Journal of experimental botany.

[57]  Y. Charng,et al.  A Heat-Inducible Transcription Factor, HsfA2, Is Required for Extension of Acquired Thermotolerance in Arabidopsis1[W][OA] , 2006, Plant Physiology.

[58]  S. Shigeoka,et al.  Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. , 2006, The Plant journal : for cell and molecular biology.

[59]  M. Zanetti,et al.  The potato transcriptional co-activator StMBF1 is up-regulated in response to oxidative stress and interacts with the TATA-box binding protein. , 2006, Journal of biochemistry and molecular biology.

[60]  Nobuhiro Suzuki,et al.  Enhanced Tolerance to Environmental Stress in Transgenic Plants Expressing the Transcriptional Coactivator Multiprotein Bridging Factor 1c1[w] , 2005, Plant Physiology.

[61]  Kenichi Tsuda,et al.  Three Arabidopsis MBF1 homologs with distinct expression profiles play roles as transcriptional co-activators. , 2004, Plant & cell physiology.

[62]  H. Nyunoya,et al.  Cloning of a tobacco cDNA coding for a putative transcriptional coactivator MBF1 that interacts with the tomato mosaic virus movement protein. , 2002, Journal of experimental botany.

[63]  K. Scharf,et al.  Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? , 2001, Cell stress & chaperones.

[64]  Pech,et al.  Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display , 1999, The Plant journal : for cell and molecular biology.

[65]  S. Harashima,et al.  Yeast Coactivator MBF1 Mediates GCN4-Dependent Transcriptional Activation , 1998, Molecular and Cellular Biology.

[66]  H. Ueda,et al.  Mediators of activation of fushi tarazu gene transcription by BmFTZ-F1 , 1994, Molecular and cellular biology.