Genome-wide analysis of the Hsf family in soybean and functional identification of GmHsf-34 involvement in drought and heat stresses

BMC Genomics

You-Zhi Ma¹  Zhao-Shi Xu¹  Shou-Cheng Chai²  Yong-Bin Zhou¹  Ming Chen¹  Guan-Hua He¹  Tai-Fei Yu¹  Pan-Song Li¹ 

[1] Chinese Academy of Agricultural Sciences (CAAS)/National Key Facility for Crop Gene Resources and Genetic Improvement, Key Laboratory of Biology and Genetic Improvement of Triticeae Crops, Ministry of Agriculture, Institute of Crop Science, Beijing 100081, China;College of Agronomy, Northwest A & F University, Yangling 712100, China

关键词: Soybean;    Functional identification;    Subcellular localization;    Expression pattern;    Genome-wide identification;    Hsfs;   

Others  :  1091542
DOI  :  10.1186/1471-2164-15-1009

 received in 2014-08-29, accepted in 2014-10-08,  发布年份 2014

【 摘 要 】

Background

High temperature affects organism growth and metabolic activity. Heat shock transcription factors (Hsfs) are key regulators in heat shock response in eukaryotes and prokaryotes. Under high temperature conditions, Hsfs activate heat shock proteins (Hsps) by combining with heat stress elements (HSEs) in their promoters, leading to defense of heat stress. Since the first plant Hsf gene was identified in tomato, several plant Hsf family genes have been thoroughly characterized. Although soybean (Glycine max), an important oilseed crops, genome sequences have been available, the Hsf family genes in soybean have not been characterized accurately.

Result

We analyzed the Hsf genetic structures and protein function domains using the GSDS, Pfam, SMART, PredictNLS, and NetNES online tools. The genome scanning of dicots (soybean and Arabidopsis) and monocots (rice and maize) revealed that the whole-genome replication occurred twice in soybean evolution. The plant Hsfs were classified into 3 classes and 16 subclasses according to protein structure domains. The A8 and B3 subclasses existed only in dicots and the A9 and C2 occurred only in monocots. Thirty eight soybean Hsfs were systematically identified and grouped into 3 classes and 12 subclasses, and located on 15 soybean chromosomes. The promoter regions of the soybean Hsfs contained cis-elements that likely participate in drought, low temperature, and ABA stress responses. There were large differences among Hsfs based on transcriptional levels under the stress conditions. The transcriptional levels of the A1 and A2 subclass genes were extraordinarily high. In addition, differences in the expression levels occurred for each gene in the different organs and at the different developmental stages. Several genes were chosen to determine their subcellular localizations and functions. The subcellular localization results revealed that GmHsf-04, GmHsf-33, and GmHsf-34 were located in the nucleus. Overexpression of the GmHsf-34 gene improved the tolerances to drought and heat stresses in Arabidopsis plants.

Conclusions

This present investigation of the quantity, structural features, expression characteristics, subcellular localizations, and functional roles provides a scientific basis for further research on soybean Hsf functions.

【 授权许可】

   
2014 Li et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】

• [1]Wahid A, Gelani S, Ashraf M, Foolad MR: Heat tolerance in plants: an overview. Environ Exp Bot 2007, 61:199-223.
• [2]Boston RS, Viitanen PV, Vierling E: Molecular chaperones and protein folding in plants. Plant Mol Biol 1996, 32:191-222.
• [3]Bukau B, Weissman J, Horwich A: Molecular chaperones and protein quality control. Cell 2006, 125:443-451.
• [4]Nakamoto H, Vigh L: The small heat shock proteins and their clients. Cell Mol Life Sci 2007, 64:294-306.
• [5]Morimoto RI: Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev 2008, 22:1427-1438.
• [6]Hartl FU, Hayer-Hartl M: Converging concepts of protein folding in vitro and in vivo. Nat Struct Mol Biol 2009, 16:574-581.
• [7]Pratt WB, Morishima Y, Peng HM, Osawa Y: Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Exp Biol Med (Maywood) 2010, 235:278-289.
• [8]Xu ZS, Li ZY, Chen Y, Chen M, Li LC, Ma YZ: Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses. Int J Mol Sci 2012, 13:15706-15723.
• [9]Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf KD: Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 2001, 6:177-189.
• [10]Heerklotz D, Döring P, Bonzelius F, Winkelhaus S, Nover L: The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2. Mol Cell Biol 2001, 21:1759-1768.
• [11]Wang F, Dong Q, Jiang H, Zhu S, Chen B, Xiang Y: Genome-wide analysis of the heat shock transcription factors in Populus trichocarpa and Medicago truncatula. Mol Biol Rep 2012, 39:1877-1886.
• [12]Pelham HR: A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell 1982, 30:517-528.
• [13]Santoro N, Johansson N, Thiele DJ: Heat shock element architecture is an important determinant in the temperature and transactivation domain requirements for heat shock transcription factor. Mol Cell Biol 1998, 18:6340-6352.
• [14]Guo L, Chen S, Liu K, Liu Y, Ni L, Zhang K, Zhang L: Isolation of heat shock factor HsfA1a-binding sites in vivo revealed variations of heat shock elements in Arabidopsis thaliana. Plant Cell Physiol 2008, 49:1306-1315.
• [15]Akerfelt M, Morimoto RI, Sistonen L: Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 2010, 11:545-555.
• [16]Scharf KD, Rose S, Zott W, Schöffl F, Nover L: Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast Hsf. EMBO J 1990, 9:4495-4501.
• [17]Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang Y, Wang J: Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 2008, 35:105-118.
• [18]Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, Cheng BJ: Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 2011, 12:76. BioMed Central Full Text
• [19]Scharf KD, Berberich T, Ebersberger I, Nover L: The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochim Biophys Acta 2012, 1819:104-119.
• [20]Zhu ZF, Sun CQ, Fu YC, Qian XY, Yang JS, Wang XK: Isolation and analysis of a novel MYC gene from rice. Yi Chuan Xue Bao 2005, 32:393-398. (in Chinese)
• [21]Li W, Cui X, Meng Z, Huang X, Xie Q, Wu H, Jin H, Zhang D, Liang W: Transcriptional regulation of Arabidopsis MIR168a and ARGONAUTE1 homeostasis in ABA and abiotic stress responses. Plant Physiol 2012, 158:1279-1292.
• [22]Zhang Y, Chen C, Jin XF, Xiong AS, Peng RH, Hong YH, Yao QH, Chen JM: Expression of a rice DREB1 gene, OsDREB1D, enhances cold and high-salt tolerance in transgenic Arabidopsis. BMB Rep 2009, 42:486-492.
• [23]Maestrini P, Cavallini A, Rizzo M, Giordani T, Bernardi R, Durante M, Natali L: Isolation and expression analysis of low temperature-induced genes in white poplar (Populus alba). J Plant Physiol 2009, 166:1544-1556.
• [24]Baniwal SK, Bharti K, Chan KY, Fauth M, Ganguli A, Kotak S, Mishra SK, Nover L, Port M, Scharf KD, Tripp J, Weber C, Zielinski D, Döring P: Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors. J Biosci 2004, 29:471-487.
• [25]Scharf KD, Heider H, Hohfeld I, Lyck R, Schmidt E, Nover L: The tomato Hsf system: HsfA2 needs interaction with HsfA1 for efficient nuclear import and may be localized in cytoplasmic heat stress granules. Mol Cell Biol 1998, 18:2240-2251.
• [26]Kotak S, Port M, Ganguli A, Bicker F, Döring P: Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J 2004, 39:98-112.
• [27]Chung E, Kim KM, Lee JH: Genome-wide analysis and molecular characterization of heat shock transcription factor family in Glycine max. J Genet Genomics 2013, 40:127-135.
• [28]Schlueter JA, Dixon P, Granger C, Grant D, Clark L, Doyle JJ, Shoemaker RC: Mining EST databases to resolve evolutionary events in major crop species. Genome 2004, 47:868-876.
• [29]Blanc G, Barakat A, Guyot R, Cooke R, Delseny M: Extensive duplication and reshuffling in the Arabidopsis genome. Plant Cell 2000, 12:1093-1101.
• [30]Rose AB: Intron-mediated regulation of gene expression. Curr Top Microbiol Immunol 2008, 326:277-290.
• [31]Ikeda M, Ohme-Takagi M: A novel group of transcriptional repressors in Arabidopsis. Plant Cell Physiol 2009, 50:970-975.
• [32]Kumar M, Busch W, Birke H, Kemmerling B, Nürnberger T, Schöffl F: Heat shock factors HsfB1 and HsfB2b are involved in the regulation of Pdf1.2 expression and pathogen resistance in Arabidopsis. Mol Plant 2009, 2:152-165.
• [33]Kim JS, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, Todaka D, Nakashima K, Hirayama T, Shinozaki K, Yamaguchi-Shinozaki K: An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 2011, 52:2136-2146.
• [34]He Y, Li W, Lv J, Jia Y, Wang M, Xia G: Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. J Exp Bot 2012, 63:1511-1522.
• [35]Yang A, Dai X, Zhang WH: A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 2012, 63:2541-2556.
• [36]Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD: In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 2002, 16:1555-1567.
• [37]Nishizawa-Yokoi A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S: Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 2006, 48:535-547.
• [38]Ogawa D, Yamaguchi K, Nishiuchi T: High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 2007, 58:3373-3383.
• [39]Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS: Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 2012, 40(Database issue):D1178-D1186. [http://www.phytozome.net/index.php webcite]
• [40]Huala E, Dickerman AW, Garcia-Hernandez M, Weems D, Reiser L, LaFond F, Hanley D, Kiphart D, Zhuang M, Huang W, Mueller LA, Bhattacharyya D, Bhaya D, Sobral BW, Beavis W, Meinke DW, Town CD, Somerville C, Rhee SY: The Arabidopsis information resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res 2001, 29:102-105. [http://arabidopsis.org webcite]
• [41]Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaud-Nissen F, Malek RL, Lee Y, Zheng L, Orvis J, Haas B, Wortman J, Buell CR: The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 2007, 35(Database issue):D883-D887. [http://rice.plantbiology.msu.edu webcite]
• [42]Grant D, Nelson RT, Cannon SB, Shoemaker RC: SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 2010, 38(Database issue):D843-D846. [http://www.soybase.org webcite]
• [43]Letunic I, Doerks T, Bork P: SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 2012, 40(Database issue):D302-D305. [http://smart.embl-heidelberg.de/ webcite]
• [44]Liu RH, Meng JL: MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas 2003, 25:317-321. (in Chinese)
• [45]Guo AY, Zhu QH, Chen X, Luo JC: GSDS: a gene structure display server. Hereditas 2007, 29:1023-1026. (in Chinese). [http://gsds.cbi.pku.edu.cn webcite]
• [46]Knudsen S: Promoter2.0: for the recognition of PolII promoter sequences. Bioinformatics 1999, 15:356-361. [http://www.cbs.dtu.dk/services/Promoter/ webcite]
• [47]Higo K, Ugawa Y, Iwamoto M, Korenaga T: Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 1999, 27:297-300. [http://www.dna.affrc.go.jp/PLACE/signalscan.html webcite]
• [48]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
• [49]Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A: Pfam: clans, web tools and services. Nucleic Acids Res 2006, 34(Database issue):D247-D251. [http://pfam.xfam.org/ webcite]
• [50]PredictNLS. [https://rostlab.org/owiki/index.php/Predict-NLS webcite]
• [51]NetNES. [http://www.cbs.dtu.dk/services/NetNES/ webcite]
• [52]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739. [http://megasoftware.net webcite]
• [53]Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L, Qiu ZG, Ma YZ: Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 2007, 65:719-732.
• [54]Li ZY, Xu ZS, He GY, Yang GX, Chen M, Li LC, Ma YZ: Overexpression of soybean GmCBL1 enhances abiotic stress tolerance and promotes hypocotyl elongation in Arabidopsis. Biochem Biophys Res Commun 2012, 427:731-736.
• [55]Li ZY, Xu ZS, He GY, Yang GX, Chen M, Li LC, Ma YZ: A mutation in Arabidopsis BSK5 encoding a brassinosteroid-signaling kinase. Biochem Biophys Res Commun 2012, 426:522-527.
• [56]Yoo SD, Cho YH, Sheen J: Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2007, 2:1565-1572.