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Identification of the grape basic helix–loop–helix transcription factor family and characterization of expression patterns in response to different stresses

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Abstract

Basic helix–loop–helix (bHLH) proteins comprise one of the largest transcription factors (TFs) families in plants and members have been identified in model plant species, such as Arabidopsis thaliana and Oryza sativa. However, far less is known about the evolutionary history and expression patterns of bHLH proteins in woody species, such as grape (Vitis vinifera). In this study, we identified a total of 126 bHLH genes (VvbHLH) in grape genome, which were classified into 24 subfamilies based on the phylogenetic analysis included homologs from four plant species. The VvbHLH genes belonging to the same subfamilies have similar protein motifs and exon/intron structures and synteny analysis indicated that tandem and segmental duplication events have been major contributors to the expansion of the VvbHLH family. Synteny analysis between grape and A. thaliana suggested that some bHLH members shared a common ancestor. Expression analysis of 26 VvbHLH genes, representing members of the III and IV subfamilies, revealed profiles that were tissue-specific, hormone-responsive, and responsive to abiotic and biotic stresses. Taken together, the genome-wide identification and characterization of the grape bHLH TFs provide insights into their evolutionary history and represents a resource for further functional characterization in the context of crop improvement and stress tolerance.

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References

  • Atchley WR, Fitch WM (1997) A natural classification of the basic helix–loop–helix class of transcription factors. PNAS 94(10):5172–5176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atchley WR, Terhalle W, Dress A (1999) Positional dependence, cliques, and predictive motifs in the bHLH protein domain. J Mol Evol 48(5):501–516

    Article  CAS  PubMed  Google Scholar 

  • Boneh U, Biton I, Zheng C, Schwartz A, Ben-Ari G (2012) Characterization of potential ABA receptors in Vitis vinifera. Plant Cell Rep 31(2):311–321

    Article  CAS  PubMed  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153(3):1398–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng C, Xu X, Gao M, Li J, Guo C, Song J, Wang X (2013) Genome-wide analysis of respiratory burst oxidase homologs in grape (Vitis vinifera L.). Int J Mol Sci 14(12):24169–24186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du H, Wang YB, Xie Y, Liang Z, Jiang SJ, Zhang SS, Huang YB, Tang YX (2013) Genome-wide identification and evolutionary and expression analyses of MYB-related genes in land plants. DNA Res 20(5):437–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fairchild CD, Schumaker MA, Quail PH (2000) HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev 14:2377–2391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fairman R, Beran-Steed RK, Anthony-Cahill SJ, Lear JD, Stafford WF, DeGrado WF, Benfield PA, Brenner SL (1993) Multiple oligomeric states regulate the DNA binding of helix-loop-helix peptides. PNAS 90(22):10429–10433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66(1):94–116

    Article  CAS  PubMed  Google Scholar 

  • Feng XM, Zhao Q, Zhao LL, Qiao Y, Xie XB, Li HF, Yao YX, You CX, Hao YJ (2012) The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biol 12:22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao M, Niu J, Zhao S, Jiao C, Xu W, Fei Z, Wang X (2012a) Characterization of Erysiphe necator-responsive genes in Chinese wild Vitis quinquangularis. Int J Mol Sci 13(9):11497–11519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao M, Wang Q, Wan R, Fei Z, Wang X (2012b) Identification of genes differentially expressed in grapevine associated with resistance to Elsinoe ampelina through suppressive subtraction hybridization. Plant Physiol Biochem 58:253–268

    Article  CAS  PubMed  Google Scholar 

  • Gao M, Zhang H, Guo C, Cheng C, Guo R, Mao L, Fei Z, Wang X (2014) Evolutionary and expression analyses of basic zipper transcription factors in the highly homozygous model grape PN40024 (Vitis vinifera L.). Plant Mol Biol Rep 32(5):1085–1102

    Article  CAS  Google Scholar 

  • Guo R, Xu X, Carole B, Li X, Gao M, Zheng Y, Wang X (2013) Genome-wide identification, evolutionary and expression analysis of the aspartic protease gene superfamily in grape. BMC Genom 14:554

    Article  CAS  Google Scholar 

  • Guo C, Guo R, Xu X, Gao M, Li X, Song J, Zheng Y, Wang X (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 65(6):1513–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix–loop–helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20(5):735–747

    Article  CAS  PubMed  Google Scholar 

  • Hou H, Li J, Gao M, Singer SD, Wang H, Mao L, Fei Z, Wang X (2013) Genomic organization, phylogenetic comparison and differential expression of the SBP-box family genes in grape. PLoS ONE 8(3):e59358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang XS, Wang W, Zhang Q, Liu JH (2013) A basic helix-loop-kelix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiol 162(2):1178–1194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huq E, Quail PH (2002) PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J 21:2441–2450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeda M, Fujiwara S, Mitsuda N, Ohme-Takagi M (2012) A triantagonistic basic helix-loop-helix system regulates cell elongation in Arabidopsis. Plant Cell 24(11):4483–4497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmstead RG, Imaizumi T (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. PNAS 109(9):3582–3587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6(3):686–703

    Article  CAS  PubMed  Google Scholar 

  • Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338

    Article  CAS  PubMed  Google Scholar 

  • Larkin M, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Ledent V, Vervoort M (2001) The basic helix-loop-helix protein family: comparative genomics and phylogenetic analysis. Genome Res 11(5):754–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ledent V, Paquet O, Vervoort M (2002) Phylogenetic analysis of the human basic helix–loop–helix proteins. Genome Biol 3(6):1–18

    Article  Google Scholar 

  • Leivar P, Tepperman JM, Cohn MM, Monte E, Al-Sady B, Erikson E, Quail PH (2012) Dynamic antagonism between phytochromes and PIF family basic helix–loop–helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell 24(4):1398–1419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40(D1):D302–D305

    Article  CAS  PubMed  Google Scholar 

  • Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Yin J (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141(4):1167–1184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Xu Y, Xiao Y, Zhu Z, Xie X, Zhao H, Wang Y (2010) Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata. Planta 232(6):1325–1337

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zhu Y, Yao J, Zhang S, Wang L, Guo C, van S Nocker, Wang X (2017) Genome-wide identification and expression analyses of the homeobox transcription factor family during ovule development in seedless and seeded grapes. Sci Rep 7:12638

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liang G, Zhang H, Li X, Ai Q, Yu D (2017) bHLH transcription factor bHLH115 regulates iron homeostasis in Arabidopsis thaliana. J Exp Bot 68(7):1743–1755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Zhao Z, Wei G, Zhang P, Lan H, Zhang S, Li C, Cao M (2018) Characterization of the ZmbHLH122 transcription factor and its potential collaborators in maize male reproduction. Plant Growth Regul 85(1):113–122

    Article  CAS  Google Scholar 

  • Ludwig SR, Habera LF, Dellaporta SL, Wessler SR (1989) Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. PNAS 86(18):7092–7096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyons E, Pedersen B, Kane J, Alam M, Ming R, Tang H, Wang X, Bowers J, Paterson A, Lisch D, Freeling M (2008) Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol 148(4):1772–1781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20(2):429–440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, Lepiniec L (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12(10):1863–1878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95:657–667

    Article  CAS  PubMed  Google Scholar 

  • Ohno S, Hosokawa M, Hoshino A, Kitamura Y, Morita Y, Park K-I, Nakashima A, Deguchi A, Tatsuzawa F, Doi M (2011) A bHLH transcription factor, DvIVS, is involved in regulation of anthocyanin synthesis in dahlia (Dahlia variabilis). J Exp Bot 62(14):5105–5116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paris S, Longhi R, Santambrogio P, de Curtis I (2003) Leucine-zipper- mediated homo- and hetero-dimerization of GIT family p95-ARF GTPase-activating protein, PIX-, paxillin-interacting proteins 1 and 2. Biochem J 372:391–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paterson A, Wang X, Tang H, Lee T (2012) Synteny and genomic rearrangements. Plant Genome Divers 1:195–207

    Article  Google Scholar 

  • Peng S, Zhu Z, Zhao K, Shi J, Yang Y, He M, Wang Y (2013) A novel heat shock transcription factor, VpHsf1, from Chinese wild Vitis pseudoreticulata is involved in biotic and abiotic stresses. Plant Mol Biol Rep 31(1):240–247

    Article  CAS  Google Scholar 

  • Pillitteri LJ, Torii KU (2007) Breaking the silence three bHLH proteins direct cell-fate decisions during stomatal development. Bioessays 29(9):861–870

    Article  CAS  PubMed  Google Scholar 

  • Pires N, Dolan L (2010) Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol 27(4):862–874

    Article  CAS  PubMed  Google Scholar 

  • Qi S, Liu K, Gao C, Li D, Jin C, Duan S, Ma H, Hai J, Chen M (2017) The effect of BnTT8 on accumulation of seed storage reserves and tolerance to abiotic stresses during Arabidopsis seedling establishment. Plant Growth Regul 82(2):271–280

    Article  CAS  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16(6):276–277

    Article  CAS  PubMed  Google Scholar 

  • Satou Y, Imai KS, Levine M, Kohara Y, Rokhsar D, Satoh N (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis I. Genes for bHLH transcription factors. Dev Genes Evol 213(5–6):213–221

    Article  CAS  PubMed  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. PNAS 95(11):5857–5864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65:907–921

    Article  CAS  PubMed  Google Scholar 

  • Simionato E, Ledent V, Richards G, Thomas-Chollier M, Kerner P, Coornaert D, Degnan BM, Vervoort M (2007) Origin and diversification of the basic helix-loop-helix gene family in metazoans: insights from comparative genomics. BMC Evol Biol 7(1):33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20(4):403–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sivitz AB, Hermand V, Curie C, Vert G (2012) Arabidopsis bHLH100 and bHLH101 control iron homeostasis via a FIT-independent pathway. PLoS ONE 7(9):e44843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • This P, Lacombe T, Thomas MR (2006) Historical origins and genetic diversity of wine grapes. Trends Genet 22(9):511–519

    Article  CAS  PubMed  Google Scholar 

  • Tian H, Guo H, Dai X, Cheng Y, Zheng K, Wang X, Wang S (2015) An ABA down-regulated bHLH transcription repressor gene, bHLH129 regulates root elongation and ABA response when overexpressed in Arabidopsis. Sci Rep 5:17587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15(8):1749–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tominaga-Wada R, Iwata M, Nukumizu Y, Sano R, Wada T (2012) A full length R-like basic-helix-loop-helix transcription factor is required for anthocyanin upregulation whereas the N-terminal region regulates epidermal hair formation. Plant Sci 183:115–122

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Liu Y, He P, Chen J (1995) Evaluation of foliar resistance to Uncinula necator in Chinese wild Vitis species. Vitis 34(3):159–164

    Google Scholar 

  • Wang Y, Chen K, Yao Q, Wang W, Zhu Z (2007) The basic helix-loop-helix transcription factor family in Bombyx mori. Dev Genes Evol 217(10):715–723

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Chen KP, Yao Q (2008) Progress of studies on bHLH transcription factor families. Hereditas 30(7):821–830

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Zhu Y, Fujioka S, Asami T, Li J, Li J (2009) Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell 21(12):3781–3791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Xiang Y, Fang L, Wang Y, Xin H, Li S (2013) Patterns of gene duplication and their contribution to expansion of gene families in grapevine. Plant Mol Biol Rep 31(4):852–861

    Article  CAS  Google Scholar 

  • Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon-intron structure. PNAS 109:1187–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada Y, Kokabu Y, Chaki K, Yoshimoto T, Ohgaki M, Yoshida S, Kato N, Koyama T, Sato F (2011) Isoquinoline alkaloid biosynthesis is regulated by a unique bHLH-type transcription factor in Coptis japonica. Plant Cell Physiol 52(7):1131–1141

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2013) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18(5):267–276

    Article  CAS  PubMed  Google Scholar 

  • Yang DL, Yang Y, He Z (2013) Role of plant hormones and their cross-talks in rice immunity. Mol Plant 6:675–685

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Gao M, Yang J, Gao M, Huang L, Wang Y, van Nocker S, Wan R, Guo C, Wang X, Gao H (2017) Identification and expression analysis of the apple (Malus × domestica) basic helix-loop-helix transcription factor family. Sci Rep 7(1):28

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang LY, Bai MY, Zhu JY, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, Yang H, Xu Y, Kim H, Fujioka S, Lin WH, Chong K, Lu T, Wang ZY (2009) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21(12):3767–3780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Mao L, Wang H, Brocker C, Yin X, Vasiliou V, Fei Z, Wang X (2012a) Genome-wide identification and analysis of grape aldehyde dehydrogenase (ALDH) gene superfamily. PLoS ONE 7(2):e32153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X (2012b) Genome-wide identification and analysis of the TIFY gene family in grape. PLoS ONE 7(9):e44465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China Grant No. 31572110 and the Program for Innovative Research Team of Grape Germplasm Resources and Breeding Grant No. 2013KCT-25 to X.W. We thank PlantScribe (http://www.plantscribe.com) for editing this manuscript.

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XW and MG: designed the study. MG, JY, HZ: contributed to the most of experiment. YZ, CC, RW: performed data analysis. YZ: assisted with the analysis of the results. XW and ZF: provided guidance on the study. MG and XW: wrote the manuscript. All of the authors approved the ultimate manuscript.

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Correspondence to Xiping Wang.

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Gao, M., Zhu, Y., Yang, J. et al. Identification of the grape basic helix–loop–helix transcription factor family and characterization of expression patterns in response to different stresses. Plant Growth Regul 88, 19–39 (2019). https://doi.org/10.1007/s10725-019-00485-3

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