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MaMPK2 enhances MabZIP93-mediated transcriptional activation of cell wall modifying genes during banana fruit ripening

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Abstract

Transcriptional regulation is an essential molecular machinery in controlling gene expression in diverse plant developmental processes including fruit ripening. This involves the interaction of transcription factors (TFs) and promoters of target genes. In banana, although a number of fruit ripening-associated TFs have been characterized, their number is relatively small. Here we identified a nuclear-localized basic leucine zipper (bZIP) TF, MabZIP93, associated with banana ripening. MabZIP93 activated cell wall modifying genes MaPL2, MaPE1, MaXTH23 and MaXGT1 by directly binding to their promoters. Transient over-expression of MabZIP93 in banana fruit resulted in the increased expression of MaPL2, MaPE1, MaXTH23 and MaXGT1. Moreover, a mitogen-activated protein kinase MaMPK2 and MabZIP93 were found to interact with MabZIP93. The interaction of MabZIP93 with MaMPK2 enhanced MabZIP93 activation of cell wall modifying genes, which was likely due to the phosphorylation of MabZIP93 mediated by MaMPK2. Overall, this study shows that MaMPK2 interacts with and phosphorylates MabZIP93 to promote MabZIP93-mediated transcriptional activation of cell wall modifying genes, thereby expanding our understanding of gene networks associated with banana fruit ripening.

Key Message

MaMPK2 interacts with and phosphorylates MabZIP93, which enhances MabZIP93 activation of cell wall modifying genes including MaPL2, MaPE1, MaXTH23 and MaXGT1 during banana ripening.

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Abbreviations

1-MCP :

1-Methylcyclopropene

bHLH :

Basic helix–loop–helix

BiFC :

Bimolecular fluorescence complementation

bZIP :

Basic leucine zipper

EMSA :

Electrophroretic mobility shift assay

ERF :

Ethylene response factor

MAPK :

Mitogen-activated protein kinase

PCR :

Polymerase chain reaction

PE :

Pectin esterase

PL :

Pectate lyase

SDS-PAGE :

Sodium dodecyl sulfate-poly acrylamide gel electrophoresis

TF :

Transcription factor

XGT :

Xyloglucan galactosyltransferase

XTH :

Xyloglucan endo-transglycosylase/hydrolase

Y2H :

Yeast two-hybrid

References

  • Asif MH, Lakhwani D, Pathak S, Gupta P, Bag SK, Nath P, Trivedi PK (2014) Transcriptome analysis of ripe and unripe fruit tissue of banana identifies major metabolic networks involved in fruit ripening process. BMC Plant Biol 14:316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ba LJ, Shan W, Xiao YY, Chen JY, Lu WJ, Kuang JF (2014a) A ripening-induced transcription factor MaBSD1 interacts with promoters of MaEXP1/2 from banana fruit. Plant Cell Rep 33:1913–1920

    Article  CAS  PubMed  Google Scholar 

  • Ba LJ, Shan W, Kuang JF, Feng BH, Xiao YY, Lu WJ, Chen JY (2014b) The banana MaLBD (LATERAL ORGAN BOUNDARIES DOMAIN) transcription factors regulate EXPANSIN expression and are involved in fruit ripening. Plant Mol Biol Rep 32:1103–1113

    Article  CAS  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–339

    Article  CAS  PubMed  Google Scholar 

  • Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P (1999) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11:2203–2216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Century K, Reuber TL, Ratcliffe OJ (2008) Regulating the regulators: the future rrospects for transcription-factor-based agricultural biotechnology products. Plant Physiol 147:20–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Zhong HY, Kuang JF, Li JG, Lu WJ, Chen JY (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234:377–390

    Article  CAS  PubMed  Google Scholar 

  • Choi HI, Park HJ, Park JH, Kim S, Im MY, Seo HH, Kim YW, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139:1750–1761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dröge-Laser W, Snoek BL, Snel B, Weiste C (2018) The Arabidopsis bZIP transcription factor family—an update. Curr Opin Plant Biol 45:36–49

    Article  CAS  PubMed  Google Scholar 

  • Fan ZQ, Kuang JF, Fu CC, Shan W, Han YC, Xiao YY, Ye YJ, Lu WJ, Lakshmanan P, Duan XW, Chen JY (2016) The banana transcriptional repressor MaDEAR1 negatively regulates cell wall-modifying genes involved in fruit ripening. Front Plant Sci 7:1021

    PubMed  PubMed Central  Google Scholar 

  • Fan ZQ, Chen JY, Kuang JF, Lu WJ, Shan W (2017) The banana fruit SINA ubiquitin ligase MaSINA1 regulates the stability of MaICE1 to be negatively involved in cold stress response. Front Plant Sci 8:995

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan ZQ, Ba LJ, Shan W, Xiao YY, Lu WJ, Kuang JF, Chen JY (2018) A banana R2R3-MYB transcription factor MaMYB3 is involved in fruit ripening through modulation of starch degradation by repressing starch degradation-related genes and MabHLH6. Plant J 96:1191–1205

    Article  CAS  PubMed  Google Scholar 

  • Feng BH, Han YC, Xiao YY, Kuang JF, Fan ZQ, Chen JY, Lu WJ (2016) The banana fruit Dof transcription factor MaDof23 acts as a repressor and interacts with MaERF9 in regulating ripening-related genes. J Exp Bot 67:2263–2275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu CC, Han YC, Qi XY, Shan W, Chen JY, Lu WJ, Kuang JF (2016) Papaya CpERF9 acts as a transcriptional repressor of cell-wall-modifying genes CpPME1/2 and CpPG5 involved in fruit ripening. Plant Cell Rep 35:2341–2352

    Article  CAS  PubMed  Google Scholar 

  • Fujisawa M, Nakano T, Shima Y, Ito Y (2013) A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25:371–386

    Article  PubMed  PubMed Central  Google Scholar 

  • Fujisawa M, Shima Y, Nakagawa H, Kitagawa M, Kimbara J, Nakano T, Kasumi T, Ito Y (2014) Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS box proteins. Plant Cell 26:89–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo YF, Zhang YL, Shan W, Cai YJ, Liang SM, Chen JY, Lu WJ, Kuang JF (2018) Identification of two transcriptional activators MabZIP4/5 in controlling aroma biosynthetic genes during banana ripening. J Agric Food Chem 66:6142–6150

    Article  CAS  PubMed  Google Scholar 

  • Gwanpua SG, Mellidfou I, Boeckx J, Kyomugasho C, Bessemans N, Verlinden BE, Geeraerd AH (2016) Expression analysis of candidate cell wall-related genes associated with changes in pectin biochemistry during postharvest apple softening. Postharvest Biol Technol 112:176–185

    Article  CAS  Google Scholar 

  • Han YC, Kuang JF, Chen JY, Liu XC, Xiao YY, Fu CC, Wang JN, Wu KQ, Lu WJ (2016) Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and Expansins during fruit ripening. Plant Physiol 171:1070–1084

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Meth 1:13

    Article  CAS  Google Scholar 

  • Hu W, Wang L, Tie W, Yan Y, Ding Z, Liu J, Li M, Peng M, Xu Y, Jin Z (2016) Genome-wide analyses of the bZIP family reveal their involvement in the development, ripening and abiotic stress response in banana. Sci Rep 6:30203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irfan M, Ghosh S, Meli VS, Kumar A, Kumar V, Chakraborty N, Chakraborty S, Datta A (2016) Fruit ripening regulation of α-Mannosidase expression by the MADS box transcription factor RIPENING INHIBITOR and ethylene. Front Plant Sci 7:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Iven T, Strathmann A, Böttner S, Zwafink T, Heinekamp T, Guivarc’h A, Roitsch T, Dröge-Laser W (2010) Homo- and heterodimers of tobacco bZIP proteins counteract as positive or negative regulators of transcription during pollen development. Plant J 63:155–166

    CAS  PubMed  Google Scholar 

  • Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  Google Scholar 

  • Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14:3177–3189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuang JF, Chen JY, Liu XC, Han YC, Xiao YY, Shan W, Tang Y, Wu KQ, He JX, Lu WJ (2017) The transcriptional regulatory network mediated by banana (Musa acuminata) dehydration-responsive element binding (MaDREB) transcription factors in fruit ripening. New Phytol 214:762–781

    Article  CAS  PubMed  Google Scholar 

  • Li D, Fu F, Zhang H, Song F (2015) Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genomics 16:771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Mao B, Ou S, Wang W, Liu L, Wu Y, Chu C, Wang X (2014a) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 84:19–36

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Chen N, Chen F, Cai B, Santo SD, Tornielli GB, Pezzotti M, Cheng ZM (2014b) Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics 15:687–694

    Article  CAS  Google Scholar 

  • Liu H, Cao X, Liu X, Xin R, Wang J, Gao J, Wu B, Gao L, Xu C, Zhang B, Grierson D, Chen K (2017) UV-B irradiation differentially regulates terpene synthases and terpene content of peach. Plant Cell Environ 40:2261–2275

    Article  CAS  PubMed  Google Scholar 

  • Liu CC, Chi C, Jin LJ, Zhu J, Yu JQ, Zhou YH (2018) The bZip transcription factor HY5 mediates CRY1a-induced anthocyanin biosynthesis in tomato. Plant Cell Environ 41:1762–1775

    Article  CAS  PubMed  Google Scholar 

  • Mair A, Pedrotti L, Wurzinger B, Anrather D, Simeunovic A, Weiste C, Valerio C, Dietrich K, Kirchler T, Nagele T, Carbajosa JV, Hanson J, Baena-González E, Chaban C, Weckwerth W, Dröge-Laser W, Teige M (2015) SnRK1-triggered switch of bZIP63 dimerization mediates the low energy response in plants. eLife 4:e05828

    Article  PubMed Central  Google Scholar 

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul P, Singh SK, Patra B, Sui X, Pattanaik S, Yuan L (2016) A differentially regulated AP2/ERF transcription factor gene cluster acts downstream of a MAP kinase cascade to modulate terpenoid indole alkaloid biosynthesis in Catharanthus roseus. New Phytol 213:1107–1123

    Article  CAS  PubMed  Google Scholar 

  • Pruneda-Paz JL, Breton G, Nagel DH, Kang SE, Bonaldi K, Doherty CJ, Ravelo S, Galli M, Ecker JR, Kay SA (2014) A genome-scale resource for the functional characterization of Arabidopsis transcription factors. Cell Rep 8:622–632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez K, Perales M, Snipes S, Yadav RK, Diaz-Mendoza M, Reddy GV (2016) DNA-dependent homodimerization, sub-cellular partitioning, and protein destabilization control WUSCHEL levels and spatial patterning. Proc Natl Acad Sci USA 113:E6307–E6315

    Article  CAS  PubMed  Google Scholar 

  • Sainsbury F, Thuenemann EC, Lomonossoff GP (2009) pEAQ: versatile expression vectors for easy and quick transient expression of heterologous proteins in plants. Plant Biotechnol J 7:682–693

    Article  CAS  PubMed  Google Scholar 

  • Shaikhali J (2015) GIP1 protein is a novel cofactor that regulates DNA-binding affinity of redox-regulated members of bZIP transcription factors involved in the early stages of Arabidopsis development. Protoplasma 252:867–883

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Singh JP, Kaur A, Singh N (2016) Bioactive compounds in banana and their associated health benefits—a review. Food Chem 206:1–11

    Article  CAS  PubMed  Google Scholar 

  • Song QX, Li QT, Liu YF, Zhang FX, Ma B, Zhang WK, Man WQ, Du WG, Wang GD, Chen SY, Zhang JS (2013) Soybean GmbZIP123 gene enhances lipid content in the seeds of transgenic Arabidopsis plants. J Exp Bot 64:4329–4341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song L, Wang Z, Wang Z, Meng G, Zhai R, Cai M, Ma F, Xu L (2016) Screening of cell wall-related genes that are expressed differentially during ripening of pears with different softening characteristics. Postharvest Biol Technol 115:1–8

    Article  CAS  Google Scholar 

  • Song CB, Shan W, Yang YY, Tan XL, Fan ZQ, Chen JY, Lu WJ, Kuang JF (2018) Heterodimerization of MaTCP proteins modulates the transcription of MaXTH10/11 genes during banana fruit ripening. Biochim Biophys Acta Gene Regul Mech 1861:613–622

    Article  CAS  PubMed  Google Scholar 

  • Sornaraj P, Luang S, Lopato S, Hrmova M (2016) Basic leucine zipper (bZIP) transcription factors involved in abiotic stresses: a molecular model of a wheat bZIP factor and implications of its structure in function. Biochim Biophys Acta 1860:46–56

    Article  CAS  PubMed  Google Scholar 

  • Tucker G, Yin X, Zhang A, Wang M, Zhu Q, Liu X, Xie X, Chen K, Grierson D (2017) Ethylene and fruit softening. Food Qual Saf 1:253–267

    Article  CAS  Google Scholar 

  • Uluisik S, Chapman NH, Smith R, Poole M, Adams G, Gillis RB, Besong TM, Sheldon J, Stiegelmeyer S, Perez L, Samsulrizal N, Wang D, Fisk ID, Yang N, Baxter C, Rickett D, Fray R, Blanco-Ulate B, Powell AL, Harding SE, Craigon J, Rose JK, Fich EA, Sun L, Domozych DS, Fraser PD, Tucker GA, Grierson D, Seymour GB (2016) Genetic improvement of tomato by targeted control of fruit softening. Nat Biotechnol 34:950–952

    Article  CAS  PubMed  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  CAS  PubMed  Google Scholar 

  • Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci USA 105:9829–9834

    Article  PubMed  Google Scholar 

  • Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438

    Article  CAS  Google Scholar 

  • Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12

    Article  CAS  PubMed  Google Scholar 

  • Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiste C, Pedrotti L, Selvanayagam J, Muralidhara P, Fröschel C, Novák O, Ljung K, Hanson J, Dröge-Laser W (2017) The Arabidopsis bZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth. PLoS Genet 13:e1006607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao YY, Chen JY, Kuang JF, Shan W, Xie H, Jiang YM, Lu WJ (2013) Molecular characterization of banana NAC transcription factors and their interactions with ethylene signaling component EIL during fruit ripening. J Exp Bot 64:2499–2510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao YY, Kuang JF, Qi XN, Ye YJ, Wu ZX, Chen JY, Lu WJ (2018) A comprehensive investigation of starch degradation process and identification of a transcriptional activator MabHLH6 during banana fruit ripening. Plant Biotechnol J 16:151–164

    Article  CAS  PubMed  Google Scholar 

  • Xie Z, Zhang ZL, Zou X, Yang G, Komatsu S, Shen QJ (2006) Interactions of two abscisic-acid induced WRKY genes in repressing gibberellin signaling in aleurone cells. Plant J 46:231–242

    Article  CAS  PubMed  Google Scholar 

  • Yin X, Allan AC, Chen K, Ferguson IB (2010) Kiwifruit EIL and ERF genes involved in regulating fruit ripening. Plant Physiol 153:1280–1292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu F, Wu Y, Xie Q (2015) Precise protein post-translational modifications modulate ABI5 activity. Trends Plant Sci 20:569–575

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Xiang L, Yu Q, Zhang H, Zhang T, Zeng J, Geng C, Li L, Fu X, Shen Q, Yang C, Lan X, Chen M, Tang K, Liao Z (2018) ARTEMISININ BIOSYNTHESIS PROMOTING KINASE 1 positively regulates artemisinin biosynthesis through phosphorylating AabZIP1. J Exp Bot 69:1109–1123

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Guo R, Guo C, Hou H, Wang X, Gao H (2016) Evolutionary and expression analyses of the apple basic Leucine zipper transcription factor family. Front Plant Sci 7:376

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to thank Professor George P. Lomonossoff (Department of Biological Chemistry, John Innes Centre, Norwich Research Park) for the generous gifts of pEAQ vectors, and Professor Prakash Lakshmanan (Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, China) for English language editing. This work was supported by the National Natural Science Foundation of China (Grant Nos. 31772021 and 31401922), Guangdong Special Support Program (Grant No. 2017TQ04N512) and China Agriculture Research System (Grant No. CARS-31-11).

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JK and XS conceived and designed the experiments; CW performed most of the experiments; WS, SL, LZ and YG performed some of the experiments; JK and XS wrote the manuscript; QL, JC and WL gave advices and revised the manuscript. All authors read and approved the manuscript.

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Correspondence to Xinguo Su or Jianfei Kuang.

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Wu, C., Shan, W., Liang, S. et al. MaMPK2 enhances MabZIP93-mediated transcriptional activation of cell wall modifying genes during banana fruit ripening. Plant Mol Biol 101, 113–127 (2019). https://doi.org/10.1007/s11103-019-00895-x

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