A class B heat shock factor selected for during soybean domestication contributes to salt tolerance by promoting flavonoid biosynthesis.

Soybean (Glycine max) production is severely affected in unfavorable environments. Identification of regulatory factors conferring stress tolerance would facilitate soybean breeding. In this study, through coexpression network analysis of salt-tolerant wild soybeans, together with molecular and genetic approaches, we unraveled a previously unidentified function of a class B heat shock factor, HSFB2b, in soybean salt stress response. We showed that HSFB2b improves salt tolerance through the promotion of flavonoid accumulation by activating one subset of flavonoid biosynthesis-related genes and by inhibiting the repressor gene GmNAC2 to release another subset of genes in the flavonoid biosynthesis pathway. Moreover, four promoter haplotypes of HSFB2b were identified from wild and cultivated soybeans. Promoter haplotype II from salt-tolerant wild soybean Y20, with high promoter activity under salt stress, is likely selected for during domestication. Another promoter haplotype, haplotype III, from salt-tolerant wild soybean Y55, had the highest promoter activity under salt stress, had a low distribution frequency and may be subjected to the next wave of selection. Together, our results revealed the mechanism of HSFB2b in soybean salt stress tolerance. Its promoter variations were identified, and the haplotype with high activity may be adopted for breeding better soybean cultivars that are adapted to stress conditions. This article is protected by copyright. All rights reserved.

[1]  Zheng Wang,et al.  Parallel selection on a dormancy gene during domestication of crops from multiple families , 2018, Nature Genetics.

[2]  Bingru Huang,et al.  Characterization and Functional Analysis of FaHsfC1b from Festuca arundinacea Conferring Heat Tolerance in Arabidopsis , 2018, International journal of molecular sciences.

[3]  Feng Ming,et al.  OsNAC2 positively affects salt‐induced cell death and binds to the OsAP37 and OsCOX11 promoters , 2018, The Plant journal : for cell and molecular biology.

[4]  J. Bowman,et al.  Genetic analysis of the liverwort Marchantia polymorpha reveals that R2R3MYB activation of flavonoid production in response to abiotic stress is an ancient character in land plants. , 2018, The New phytologist.

[5]  Chuang Ma,et al.  Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution , 2018, Front. Plant Sci..

[6]  Junna He,et al.  Overexpression of lily HsfA3s in Arabidopsis confers increased thermotolerance and salt sensitivity via alterations in proline catabolism , 2018, Journal of experimental botany.

[7]  R. Nelson,et al.  Elevation of soybean seed oil content through selection for seed coat shininess , 2018, Nature Plants.

[8]  Fan Zhang,et al.  Histone Deacetylases SRT1 and SRT2 Interact with ENAP1 to Mediate Ethylene-Induced Transcriptional Repression[OPEN] , 2018, Plant Cell.

[9]  Yan Guo,et al.  Elucidating the molecular mechanisms mediating plant salt-stress responses. , 2018, The New phytologist.

[10]  G. Muday,et al.  Abscisic Acid-Induced Reactive Oxygen Species Are Modulated by Flavonols to Control Stomata Aperture1[OPEN] , 2017, Plant Physiology.

[11]  S. Chen,et al.  A Histone Code Reader and a Transcriptional Activator Interact to Regulate Genes for Salt Tolerance1[OPEN] , 2017, Plant Physiology.

[12]  A. Cantero,et al.  Advances in the MYB-bHLH-WD Repeat (MBW) Pigment Regulatory Model: Addition of a WRKY Factor and Co-option of an Anthocyanin MYB for Betalain Regulation. , 2017, Plant & cell physiology.

[13]  Zheng Wang,et al.  Genome-wide association studies dissect the genetic networks underlying agronomical traits in soybean , 2017, Genome Biology.

[14]  Ping Li,et al.  A Natural Allele of a Transcription Factor in Rice Confers Broad-Spectrum Blast Resistance , 2017, Cell.

[15]  S. Chen,et al.  A PP2C-1 Allele Underlying a Quantitative Trait Locus Enhances Soybean 100-Seed Weight. , 2017, Molecular plant.

[16]  S. Chen,et al.  Ethylene-Inhibited Jasmonic Acid Biosynthesis Promotes Mesocotyl/Coleoptile Elongation of Etiolated Rice Seedlings[OPEN] , 2017, Plant Cell.

[17]  Meng Yuan,et al.  uORF-mediated translation allows engineered plant disease resistance without fitness costs , 2017, Nature.

[18]  Xinnian Dong,et al.  Global translational reprogramming is a fundamental layer of immune regulation in plants , 2017, Nature.

[19]  R. Reiter,et al.  HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants , 2017, Journal of pineal research.

[20]  Heribert Hirt,et al.  The heat‐shock protein/chaperone network and multiple stress resistance , 2017, Plant biotechnology journal.

[21]  S. Chen,et al.  Selection for a Zinc-Finger Protein Contributes to Seed Oil Increase during Soybean Domestication1[OPEN] , 2017, Plant Physiology.

[22]  B. Ruperti,et al.  A Grapevine TTG2-Like WRKY Transcription Factor Is Involved in Regulating Vacuolar Transport and Flavonoid Biosynthesis , 2017, Front. Plant Sci..

[23]  Fan Zhang,et al.  Histone Deacetylases SRT 1 and SRT 2 Interact with ENAP 1 To Mediate 3 Ethylene-Induced Transcriptional Repression 4 5 , 2017 .

[24]  A. Hammerbacher,et al.  Overexpression of PaNAC03, a stress induced NAC gene family transcription factor in Norway spruce leads to reduced flavonol biosynthesis and aberrant embryo development , 2017, BMC Plant Biology.

[25]  Guodong Wang,et al.  Functional conservation and divergence of GmCHLI genes in polyploid soybean. , 2016, The Plant journal : for cell and molecular biology.

[26]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[27]  S. Chen,et al.  Soybean GmDREBL Increases Lipid Content in Seeds of Transgenic Arabidopsis , 2016, Scientific Reports.

[28]  J. Ecker,et al.  EIN2-dependent regulation of acetylation of histone H3K14 and non-canonical histone H3K23 in ethylene signalling , 2016, Nature Communications.

[29]  S. Chen,et al.  Soybean miR172a Improves Salt Tolerance and Can Function as a Long-Distance Signal. , 2016, Molecular plant.

[30]  Jianbing Yan,et al.  Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings , 2016, Nature Genetics.

[31]  Kazuki Saito,et al.  Hydrogen Rearrangement Rules: Computational MS/MS Fragmentation and Structure Elucidation Using MS-FINDER Software. , 2016, Analytical chemistry.

[32]  R. Mittler,et al.  Accumulation of Flavonols over Hydroxycinnamic Acids Favors Oxidative Damage Protection under Abiotic Stress , 2016, Front. Plant Sci..

[33]  J. Lämke,et al.  A hit‐and‐run heat shock factor governs sustained histone methylation and transcriptional stress memory , 2016, The EMBO journal.

[34]  Klaas Vandepoele,et al.  CoExpNetViz: Comparative Co-Expression Networks Construction and Visualization Tool , 2016, Front. Plant Sci..

[35]  Jun You,et al.  ROS Regulation During Abiotic Stress Responses in Crop Plants , 2015, Front. Plant Sci..

[36]  B. Mueller‐Roeber,et al.  The Arabidopsis Transcription Factor MYB112 Promotes Anthocyanin Formation during Salinity and under High Light Stress1[OPEN] , 2015, Plant Physiology.

[37]  Biao Wang,et al.  The soybean R2R3 MYB transcription factor GmMYB100 negatively regulates plant flavonoid biosynthesis , 2015, Plant Molecular Biology.

[38]  Z. Wang,et al.  Genomics progress will facilitate molecular breeding in soybean , 2015, Science China Life Sciences.

[39]  Biao Ma,et al.  GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants. , 2015, The Plant journal : for cell and molecular biology.

[40]  S. Chen,et al.  MAOHUZI6/ETHYLENE INSENSITIVE3-LIKE1 and ETHYLENE INSENSITIVE3-LIKE2 Regulate Ethylene Response of Roots and Coleoptiles and Negatively Affect Salt Tolerance in Rice1[OPEN] , 2015, Plant Physiology.

[41]  J. T. Matus,et al.  The Phenylpropanoid Pathway Is Controlled at Different Branches by a Set of R2R3-MYB C2 Repressors in Grapevine1 , 2015, Plant Physiology.

[42]  Y. Liu,et al.  Salinity tolerance in soybean is modulated by natural variation in GmSALT3. , 2014, The Plant journal : for cell and molecular biology.

[43]  S. Kay,et al.  HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock , 2014, Proceedings of the National Academy of Sciences.

[44]  S. Chen,et al.  Ethylene-Induced Inhibition of Root Growth Requires Abscisic Acid Function in Rice (Oryza sativa L.) Seedlings , 2014, PLoS genetics.

[45]  Y. Wang,et al.  Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing , 2014, Nature Communications.

[46]  C. Foyer,et al.  The Roles of Reactive Oxygen Metabolism in Drought: Not So Cut and Dried[1][C][W] , 2014, Plant Physiology.

[47]  Kazuki Saito,et al.  Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids , 2013, The Plant journal : for cell and molecular biology.

[48]  Biao Wang,et al.  GmFNSII-controlled soybean flavone metabolism responds to abiotic stresses and regulates plant salt tolerance. , 2014, Plant & cell physiology.

[49]  S. Chen,et al.  Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants , 2013, Journal of experimental botany.

[50]  Xiaoping Zhou,et al.  Heat shock factor OsHsfB2b negatively regulates drought and salt tolerance in rice , 2013, Plant Cell Reports.

[51]  Ziv Bar-Joseph,et al.  Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis , 2013, eLife.

[52]  B. Mueller‐Roeber,et al.  Transcription factor OsHsfC1b regulates salt tolerance and development in Oryza sativa ssp. japonica , 2012, AoB PLANTS.

[53]  R. Mittler,et al.  How do plants feel the heat? , 2012, Trends in biochemical sciences.

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

[55]  Karolina M. Pajerowska-Mukhtar,et al.  The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition , 2012, Current Biology.

[56]  Biao Ma,et al.  Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. , 2011, The Plant journal : for cell and molecular biology.

[57]  Nobutaka Mitsuda,et al.  Arabidopsis HsfB1 and HsfB2b Act as Repressors of the Expression of Heat-Inducible Hsfs But Positively Regulate the Acquired Thermotolerance1[C][W][OA] , 2011, Plant Physiology.

[58]  J. Roberts,et al.  The role of the pod in seed development: strategies for manipulating yield. , 2011, The New phytologist.

[59]  Nathan D. Miller,et al.  Auxin and Ethylene Induce Flavonol Accumulation through Distinct Transcriptional Networks1[C][W][OA] , 2011, Plant Physiology.

[60]  Nobutaka Mitsuda,et al.  Arabidopsis HsfB 1 and HsfB 2 b Act as Repressors of the Expression of Heat-Inducible Hsfs But Positively Regulate the Acquired Thermotolerance 1 [ C ] [ W ] [ OA ] , 2011 .

[61]  K. Niehaus,et al.  Analysis of PRODUCTION OF FLAVONOL GLYCOSIDES-dependent flavonol glycoside accumulation in Arabidopsis thaliana plants reveals MYB11-, MYB12- and MYB111-independent flavonol glycoside accumulation. , 2010, The New phytologist.

[62]  N. Tuteja,et al.  Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. , 2010, Plant physiology and biochemistry : PPB.

[63]  S. Chen,et al.  Plant NAC-type transcription factor proteins contain a NARD domain for repression of transcriptional activation , 2010, Planta.

[64]  G. King,et al.  A SQUAMOSA MADS Box Gene Involved in the Regulation of Anthocyanin Accumulation in Bilberry Fruits1[W][OA] , 2010, Plant Physiology.

[65]  T. Cuin,et al.  Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death , 2010, Journal of Cell Science.

[66]  R. Stracke,et al.  The Arabidopsis bZIP transcription factor HY5 regulates expression of the PFG1/MYB12 gene in response to light and ultraviolet-B radiation. , 2010, Plant, cell & environment.

[67]  M. Djordjevic,et al.  Flavonoids: new roles for old molecules. , 2010, Journal of integrative plant biology.

[68]  S. Chen,et al.  Soybean GmPHD-Type Transcription Regulators Improve Stress Tolerance in Transgenic Arabidopsis Plants , 2009, PloS one.

[69]  Qi Xie,et al.  Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses , 2009, Cell Research.

[70]  W. Busch,et al.  Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. , 2009, Molecular plant.

[71]  Biao Ma,et al.  Soybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants , 2008, Cell Research.

[72]  S. Chen,et al.  Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. , 2008, Plant biotechnology journal.

[73]  S. Chen,et al.  Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis , 2008, Planta.

[74]  Dongxue Li,et al.  Agrobacterium rhizogenes-mediated transformation of soybean to study root biology , 2007, Nature Protocols.

[75]  H. Kranz,et al.  The Arabidopsis Transcription Factor MYB12 Is a Flavonol-Specific Regulator of Phenylpropanoid Biosynthesis1 , 2005, Plant Physiology.

[76]  R. Mittler.  Oxidative stress, antioxidants and stress tolerance. , 2002, Trends in plant science.

[77]  D. Inzé,et al.  Signal transduction during oxidative stress. , 2002, Journal of experimental botany.

[78]  W. Fehr,et al.  Stages of soybean development , 1977 .

[79]  Howard C. Berg,et al.  Genetic analysis , 1957, Nature Biotechnology.