Genome-wide identification, characterization and expression analysis of the expansin gene family under drought stress in tea (Camellia sinensis L.)

Authors

DOI:

https://doi.org/10.14719/pst.2021.8.1.923

Keywords:

Expansin, Identification, Camellia sinensis, Drought, In-silico, Differential gene expression

Abstract

During several developmental processes, expansins contribute to cell enlargement by promoting cell wall loosening. To explore the biological roles of expansins during drought stress response and to characterize different expansins in tea, we performed a detailed analysis of the expansin gene family covering phylogeny, gene structure, profiling of gene expression and co-expression network analysis. We identified a total of 40 expansin genes in the tea genome belonging to 3 subfamilies, out of which 29 tea expansins belong to EXPA, 9 to EXLA and 2 to EXPB subfamilies. A minimum of 3 and a maximum of 13 exons are present in the gene structure of expansins. Presence of drought stress responsive cis-acting elements in the upstream of promoter regions of 40% of the identified expansins shows that the putative expansins may have been involved in tea plant’s response to drought stress. At least 15 out of the 40 expansin genes are found to be differentially expressed in response to drought in each of the drought stress related public datasets analysed in-silico. TEA022767 belonging to EXPA subfamily is seen to be upregulated during drought stress, as revealed from the analysis of all three publicly available bio-projects. Co-expression network analysis shows that TEA022767 and TEA032954 form a connecting link between two expression correlation groups that further signifies their role in drought stress response in tea. This study helps to interpret and to understand the biological roles of diverse expansin genes in tea plants under drought stress conditions.

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References

McQueen-Mason S, Cosgrove DJ. Disruption of hydrogen bonding between plant cell wall polymers by proteins that induce wall extension. Proc Natl Acad Sci. 1994;91(14):6574-78. https://doi.org/10.1073/pnas.91.14.6574

Choi D, Cho HT, Lee Y. Expansins: expanding importance in plant growth and development. Physiol Plant. 2006;126:511–18. https://doi.org/10.1111/j.1399-3054.2006.00612.x

Cho HT, Cosgrove DJ. Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell. 2002;14:3237–53. https://doi.org/10.1105/tpc.006437

Che J, Yamaji N, Shen RF, Ma JF. An Al-inducible expansin gene, OsEXPA10 is involved in root cell elongation of rice. Plant J. 2016;88:132–42. https://doi.org/10.1111/tpj.13237

Balestrini R, Cosgrove DJ, Bonfante P. Differential location of ?-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta. 2005;220:889–99. https://doi.org/10.1007/s00425-004-1431-2

Flemetakis E, Efrose RC, Desbrosses G, Dimou M, Delis C, Aivalakis G, Udvardi MK, Katinakis P. Induction and spatial organization of polyamine biosynthesis during nodule development in Lotus japonicus. Mol Plant Microbe Interact. 2004;17:1283–93. https://doi.org/10.1094/MPMI.2004.17.12.1283

Belfield EJ, Ruperti B, Roberts JA, McQueen-Mason S. Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. J Exp Bot. 2005;56(413):817–23. https://doi.org/10.1093/jxb/eri076

Goh HH, Sloan J, Dorca-Fornell C, Fleming A. Inducible repression of multiple expansin genes leads to growth suppression during leaf development. Plant Physiol. 2012;159(4):1759–70. https://doi.org/10.1104/pp.112.200881

Kuluev BR, Knyazev AV, Mikhaylova EV et al. The role of expansin genes PtrEXPA3 and PnEXPA3 in the regulation of leaf growth in poplar. Russ J Genet. 2017;53: 651–60. https://doi.org/10.1134/S1022795417060084

Saito T, Tuan PA, Katsumi-Horigane A et al. Development of flower buds in the Japanese pear (Pyrus pyrifolia) from late autumn to early spring, Tree Physiol. 2015;35(6):653–62. https://doi.org/10.1093/treephys/tpv043

Cho HT, Kende H. Expression of expansin genes is correlated with growth in deepwater rice. Plant Cell. 1997;9:1661–71. https://doi.org/10.1105/tpc.9.9.1661

Tabuchi A, Li LC, Cosgrove DJ. Matrix solubilization and cell wall weakening by b-expansin (group-1 allergen) from maize pollen. Plant J. 2011;68:546–59. https://doi.org/10.1111/j.1365-313X.2011.04705.x

Harmer S, Orford S, Timmis J. Characterisation of six ?-expansin genes in Gossypium hirsutum (upland cotton). Mol Gen Genomics. 2002;268:1–9. https://doi.org/10.1007/s00438-002-0721-2

Palapol Y, Kunyamee S, Thongkhum M, Ketsa S, Ferguson IB, Van Doorn WG. Expression of expansin genes in the pulp and the dehiscence zone of ripening durian (Durio zibethinus) fruit. J Plant Physiol. 2015;182:33–39. https://doi.org/10.1016/j.jplph.2015.04.005

Nardi CF, Villarreal NM, Rossi FR, Martínez S, Martínez GA, Civello PM. Over expression of the carbohydrate binding module of strawberry expansin2 in Arabidopsis thaliana modifies plant growth and cell wall metabolism. Plant Mol Biol. 2015;88:101–17. https://doi.org/10.1007/s11103-015-0311-4

Brummell DA, Harpster MH, Dunsmuir P. Differential expression of expansin gene family members during growth and ripening of tomato fruit. Plant Mol Biol. 1999;39:161–69. https://doi.org/10.1023/A:1006130018931

Perini MA, Sin IN, Villarreal NM, Marina M, Powell AL, Martínez GA, Civello PM. Over expression of the carbohydrate binding module from Solanum lycopersicum expansin 1 (Sl-EXP1) modifies tomato fruit firmness and Botrytis cinerea susceptibility. Plant Physiol Biochem. 2017;113:122–32. https://doi.org/10.1016/j.plaphy.2017.01.029

Chen Y, Han Y, Zhang M, Zhou S, Kong X, Wang W. Over expression of the wheat expansin gene TaEXPA2 improved seed production and drought tolerance in transgenic tobacco plants. PLoS One. 2016;11:e0153494. https://doi.org/10.1371/journal.pone.0153494

Shcherban TY, Shi J, Durachko DM, Guiltinan MJ, McQueen-Mason SJ et al. Molecular cloning and sequence analysis of expansins-a highly conserved, multigene family of proteins that mediate cell wall extension in plants. Proc Natl Acad Sci U S A. 1995;92:9245–49. https://doi.org/10.1073/pnas.92.20.9245

Sampedro J, Cosgrove DJ. The expansin superfamily. Genome Biol. 2005;6(12):242. https://doi.org/10.1186/gb-2005-6-12-242

Cosgrove DJ. Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol. 1997;13:171-201. 10.1146/annurev.cellbio.13.1.171

Yennawar NH, Li LC, Dudzinski DM, Tabuchi A, Cosgrove DJ. Crystal structure and activities of EXPB1 (Zea m 1), a ?-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci. 2006;103(40):14664-71. https://doi.org/10.1073/pnas.0605979103

Cosgrove DJ. Loosening of plant cell walls by expansins. Nature. 2000;407:321–26. https://doi.org/10.1038/35030000

Cheruiyot EK, Mumera LM, Ngetich WK, Hassanali A, Wachira FN. High fertilizer rates increase susceptibility of tea to water stress. J Plant Nutr. 2009;33:115–29. https://doi.org/10.1080/01904160903392659

Yang J, Zhang G, An J, Li Q, Chen Y, Zhao X, Wu J, Wang Y, Hao Q, Wang W, Wang W. Expansin gene TaEXPA2 positively regulates drought tolerance in transgenic wheat (Triticum aestivum L.). Plant Sci. 2020;298:110596. https://doi.org/10.1016/j.plantsci.2020.110596

Lü P, Kang M, Jiang X, Dai F, Gao J, Zhang C. RhEXPA4, a rose expansin gene, modulates leaf growth and confers drought and salt tolerance to Arabidopsis. Planta. 2013;237(6):1547-59. https://doi.org/10.1007/s00425-013-1867-3

Lee Y, Choi D, Kende H. Expansins: ever-expanding numbers and functions. Curr Opin Plant Biol. 2001;4:527-32. https://doi.org/10.1016/s1369-5266(00)00211-9

Zhang W, Yan H, Chen W, Liu J, Jiang C, Jiang H, Zhu S, Cheng B. Genome-wide identification and characterization of maize expansin genes expressed in endosperm. Mol Genet Genomics. 2014;289(6):1061-74. https://doi.org/10.1007/s00438-014-0867-8

Li N, Pu Y, Gong Y et al. Genomic location and expression analysis of expansin gene family reveals the evolutionary and functional significance in Triticum aestivum. Genes Genom. 2016;38:1021–30. https://doi.org/10.1007/s13258-016-0446-y

Zhu Y, Wu N, Song W, Yin G, Qin Y, Yan Y, Hu Y. Soybean (Glycine max) expansin gene superfamily origins: segmental and tendem duplication events followed by divergent selection among subfamilies. BMC Plant Biol. 2014;14:93. https://doi.org/10.1186/1471-2229-14-93

Ding A, Marowa P, Kong Y. Genome-wide identification of the expansin gene family in tobacco (Nicotiana tabacum). Mol Genet Genomics. 2016;291:1891–907. https://doi.org/10.1007/s00438-016-1226-8

Lu Y, Liu Lifeng, Wang X, Han Z,Ouyang B, Zhang J, Li H. Genome-wide identification and expression analysis of the expansin gene family in tomato. Mol Genet Genomics. 2016;291:597-608. https://doi.org/10.1007/s00438-015-1133-4

Zhang S, Xu R, Gao Z et al. A genome-wide analysis of the expansin genes in Malus × Domestica. Mol Genet Genomics. 2014;225–36 (2014). https://doi.org/10.1007/s00438-013-0796-y

Dal Santo S, Vannozzi A, Tornielli GB, Fasoli M, Venturini L, Pezzotti M et al. Genome-wide analysis of the expansin gene superfamily reveals grapevine-specific structural and functional characteristics. PLoS One. 2013;8(4):e62206. https://doi.org/10.1371/journal.pone.0062206

Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A. Protein identification and analysis tools on the ExPASy server. The Proteomics Protocols Handbook. 2005; (edited) Walker, J.M., Totowa, N.J.: Humana Press. Available from https://link.springer.com/protocol/10.1385/1-59259-890-0:571

Wan S, Mak MW, Kung SY. FUEL-mLoc: feature-unified prediction and explanation of multi-localization of cellular proteins in multiple organisms. Bioinformatics. 2017;33:749–50. https://doi.org/10.1093/bioinformatics/btw717

Petersen TN, Brunak S, Von Heijne G, Nielsen H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785. https://doi.org/10.1038/nmeth.1701

Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics. 2015;31:1296–97. https://doi.org/10.1093/bioinformatics/btu817

Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Noble WS. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–08. https://doi.org/10.1093/nar/gkp335

Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30:325-27. https://doi.org/10.1093/nar/30.1.325

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–49. https://doi.org/10.1093/molbev/msy096

Goodstein DM, Shu SQ, Howson R, Neupane R, Hayes RD, Fazo J et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40:D1178–86. https://doi.org/10.1093/nar/gkr944

Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34:W609–12. https://doi.org/10.1093/nar/gkl315

Wei C, Yang H, Wang S et al. Draft genome sequence of Camellia sinensis var. sinensis provides insights into the evolution of the tea genome and tea quality. Proc Natl Acad Sci. 2018;115(18):E4151-58. https://doi.org/10.1073/pnas.1719622115

Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016;11:1650–67. https://doi.org/10.1038/nprot.2016.095

Anders S, Huber W. Differential expression analysis for sequence countdata. Genome Biol. 2010;11:R106. https://doi.org/10.1186/gb-2010-11-10-r106

Metsalu T, Vilo J. ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res. 2015;43:W566-70. https://doi.org/10.1093/nar/gkv468

Shannon P, Markiel A, Ozier O, Baliga NS, Wan JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504. https://dx.doi.org/10.1101%2Fgr.1239303

Marowa P, Ding A, Kong Y. Expansins: roles in plant growth and potential applications in crop improvement. Plant Cell Rep. 2016;35:949-65. https://doi.org/10.1007/s00299-016-1948-4

Koech RK, Malebe PM, Nyarukowa C et al. Functional annotation of putative QTL associated with black tea quality and drought tolerance traits. Sci Rep. 2019;9:1465. https://doi.org/10.1038/s41598-018-37688-z

Krishnamurthy P, Hong JK, Kim JA, Jeong MJ, Lee YH, Lee SI. Genome-wide analysis of the expansin gene superfamily reveals Brassica rapa-specific evolutionary dynamics upon whole genome triplication. Mol Genet Genomics. 2015;290(2):521-30. https://doi.org/10.1007/s00438-014-0935-0

Hou L, Zhang Z, Dou S, Zhang Y, Pang X, Li Y Genome-wide identification, characterization, and expression analysis of the expansin gene family in Chinese jujube (Ziziphus jujuba Mill.). Planta. 2019;249(3):815-29. https://doi.org/10.1007/s00425-018-3020-9

Santiago TR, Pereira M, de Souza WR, Steindorff A, Cunha B, Gaspar M, Favaro LC, Formighieri EF, Kobayashi AK, Molinari HB. Genome-wide identification, characterization and expression profile analysis of expansins gene family in sugarcane (Saccharum spp.). PLoS One. 2001;13:e0191081. https://doi.org/10.1371/journal.pone.0191081

Gao WLD, Fan X, Sun Y, Han B, Wan X, Xu G. Genome-wide identification, characterization, and expression analysis of the expansin gene family in watermelon (Citrullus lanatus). 3 Biotech. 2020;10(7). https://doi.org/10.1007/s13205-020-02293-3

Guimaraes LA, Mota APZ, Araujo ACG, de Alencar Figueiredo LF, Pereira B, de Passos Saraiva MA, Brasileiro ACM. Genome-wide analysis of expansin super family in wild Arachis discloses a stress-responsive expansin-like B gene. Plant Mol Biol. 2017;94(1-2):79–96. https://doi.org/10.1007/s11103-017-0594-8

Zhang JF, Xu YQ, Dong JM, Peng LN, Feng X, Wang X, Li FL. Genome-wide identification of wheat (Triticum aestivum) expansins and expansin expression analysis in cold-tolerant and cold-sensitive wheat cultivars. PLoS One. 2018;13(3):e0195138. https://doi.org/10.1371/journal.pone.0195138

Lv LM, Zuo DY, Wang XF, Cheng HL, Zhang YP, Wang QL, Ma ZY. Genome-wide identification of the expansin gene family reveals that expansin genes are involved in fibre cell growth in cotton. BMC Plant Biol. 2020;20:1. https://doi.org/10.1186/s12870-020-02362-y

Han Z, Liu Y, Deng X, Liu D, Liu Y, Hu1Y and Yan Y. Genome-wide identification and expression analysis of expansin gene family in common wheat (Triticum aestivum L.). BMC Genom. 2019;20:101. https://doi.org/10.1186/s12864-019-5455-1

Liu S-C, Jin J-Q, Ma J-Q, Yao M-Z, Ma C-L, Li C-F, et al. Transcriptomic analysis of tea plant responding to drought stress and recovery. PLos One. 2016;11:1–21. https://doi.org/10.1371/journal.pone.0147306

Sun J, Qiu C, Ding Y, Wang Y, Sun L, Fan K, et al. Fulvic acid ameliorates drought stress-induced damage in tea plants by regulating the ascorbate metabolism and flavonoids biosynthesis. BMC Genom. 2020;21:411. https://doi.org/10.1186/s12864-020-06815-4

Published

01-01-2021

How to Cite

1.
Bordoloi K, Dihingia P, Krishnatreya D, Agarwala N. Genome-wide identification, characterization and expression analysis of the expansin gene family under drought stress in tea (Camellia sinensis L.). Plant Sci. Today [Internet]. 2021 Jan. 1 [cited 2024 Nov. 21];8(1):32-44. Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/923

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Research Articles