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Genome-Wide Analysis of Soybean Vacuolar Processing Enzyme Gene Family Reveals Their Roles in Plant Development and Response to Stress Conditions

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Abstract

Vacuolar processing enzymes (VPEs) are important proteases for the processing and maturation of vacuolar proteins. The VPEs in model plant Arabidopsis have been well researched. However, less is known about this gene family in the crop plant soybean (Glycine max). This study performed genome-wide identification of soybean VPE genes and 7 members were isolated. Their sequence information was firstly collected, and then phylogenetic relationship, chromosome distribution, gene duplication, conserved motifs as well as gene structure were analyzed for further insight into this gene family. The 7 GmVPEs were located on 6 chromosomes, and their encoding proteins were classified into three groups. Collinearity analysis indicated that 5 GmVPEs were involved in gene duplication events and they have undergone purifying selection during evolution. Conserved motif and gene structure analysis revealed the similarity and diversity among the sequences of different GmVPEs. To uncover the possible functions of soybean VPEs, cis-acting elements and TF binding sites on their promoters were identified, the results implied soybean VPE genes might participate in various biological processes and transcriptional regulation pathways. Through analyzing the RNA-Seq data, expression of the soybean VPE genes were found to exhibit spatiotemporal differences, with some being expressed almost ubiquitously, while others being expressed uniquely in seed. Finally, the expression profile analysis indicated that two VPE members, namely GmVPE4 and GmVPE7, likely play key roles in plant response to both biotic and abiotic stresses.

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Data used or analyzed during the current study are available from the corresponding author on reasonable request.

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References

  • Almagro Armenteros JJ, Tsirigos KD, Sonderby CK, Petersen TN, Winther O, Brunak S, von Heijne G, Nielsen H (2019) SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 37(4):420–423

    Article  CAS  PubMed  Google Scholar 

  • Amalraj A, Luang S, Kumar MY, Sornaraj P, Eini O, Kovalchuk N, Bazanova N, Li Y, Yang N, Eliby S, Langridge P, Hrmova M, Lopato S (2016) Change of function of the wheat stress-responsive transcriptional repressor TaRAP2.1L by repressor motif modification. Plant Biotechnol J 14(2):820–832

    Article  CAS  PubMed  Google Scholar 

  • Ariizumi T, Higuchi K, Arakaki S, Sano T, Asamizu E, Ezura H (2011) Genetic suppression analysis in novel vacuolar processing enzymes reveals their roles in controlling sugar accumulation in tomato fruits. J Exp Bot 62(8):2773–2786

    Article  CAS  PubMed  Google Scholar 

  • Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43(W1):W39–W49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belamkar V, Weeks NT, Bharti AK, Farmer AD, Graham MA, Cannon SB (2014) Comprehensive characterization and RNA-Seq profiling of the HD-Zip transcription factor family in soybean (Glycine max) during dehydration and salt stress. BMC Genomics 15:950

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Lin JY, Wu X, Apuya NR, Henry KF, Le BH, Bui AQ, Pelletier JM, Cokus S, Pellegrini M, Harada JJ, Goldberg RB (2021) Comparative analysis of embryo proper and suspensor transcriptomes in plant embryos with different morphologies. Proc Natl Acad Sci USA 118(6):e2024704118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeMers LC, Redekar NR, Kachroo A, Tolin SA, Li S, Saghai Maroof MA (2020) A transcriptional regulatory network of Rsv3-mediated extreme resistance against Soybean mosaic virus. PLoS ONE 15(4):e0231658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng M, Bian H, Xie Y, Kim Y, Wang W, Lin E, Zeng Z, Guo F, Pan J, Han N, Wang J, Qian Q, Zhu M (2011) Bcl-2 suppresses hydrogen peroxide-induced programmed cell death via OsVPE2 and OsVPE3, but not via OsVPE1 and OsVPE4, in rice. FEBS J 278(24):4797–4810

    Article  CAS  PubMed  Google Scholar 

  • Deng H, Cao S, Zhang G, Xiao Y, Liu X, Wang F, Tang W, Lu X (2024) OsVPE2, a member of vacuolar processing enzyme family, decreases chilling tolerance of rice. Rice 17(1):5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong C, Li R, Wang N, Liu Y, Zhang Y, Bai S (2022) Apple vacuolar processing enzyme 4 is regulated by cysteine protease inhibitor and modulates fruit disease resistance. J Exp Bot 73(11):3758–3773

    Article  CAS  PubMed  Google Scholar 

  • Duan X, Zhang K, Duanmu H, Yu Y (2023) Genome-wide identification and expression characteristics of cytokinin response factors in soybean. J Plant Growth Regul 42:4484–4496

    Article  CAS  Google Scholar 

  • Ferreira DO, Fraga OT, Pimenta MR, Caetano HDN, Machado JPB, Carpinetti PA, Brustolini OJB, Quadros IPS, Reis PAB, Fontes EPB (2020) GmNAC81 inversely modulates leaf senescence and drought tolerance. Front Genet 11:601876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong P, Li Y, Tang Y, Wei R, Huijun Z, Wang Y, Zhang C (2018) Vacuolar processing enzyme (VvbetaVPE) from Vitis vinifera, processes seed proteins during ovule development, and accelerates seed germination in VvbetaVPE heterologously over-expressed Arabidopsis. Plant Sci 274:420–431

    Article  CAS  PubMed  Google Scholar 

  • Grant D, Nelson RT, Cannon SB, Shoemaker RC (2010) SoyBase, the USDA-ARS soybean genetics and genomics database. Nucleic Acids Res 38:D843-846

    Article  CAS  PubMed  Google Scholar 

  • Hara-Nishimura I, Nishimura M (1987) Proglobulin processing enzyme in vacuoles isolated from developing pumpkin cotyledons. Plant Physiol 85(2):440–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hara-Nishimura I, Inoue K, Nishimura M (1991) A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms. FEBS Lett 294(1–2):89–93

    Article  CAS  PubMed  Google Scholar 

  • Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305(5685):855–858

    Article  CAS  PubMed  Google Scholar 

  • Hatsugai N, Yamada K, Goto-Yamada S, Hara-Nishimura I (2015) Vacuolar processing enzyme in plant programmed cell death. Front Plant Sci 6:234

    Article  PubMed  PubMed Central  Google Scholar 

  • Hiraiwa N, Nishimura M, Hara-Nishimura I (1997) Expression and activation of the vacuolar processing enzyme in Saccharomyces cerevisiae. Plant J 12(4):819–829

    Article  CAS  PubMed  Google Scholar 

  • Huai B, Liang M, Bai M, He H, Chen J, Wu H (2022) Localization of CgVPE1 in secondary cell wall formation during tracheary element differentiation in the pericarp of Citrus grandis “Tomentosa” fruits. Planta 256(5):89

    Article  CAS  PubMed  Google Scholar 

  • Huai B, Liang M, Lin J, Tong P, Bai M, He H, Liang X, Chen J, Wu H (2023) Involvement of vacuolar processing enzyme CgVPE1 in vacuole rupture in the programmed cell death during the development of the secretory cavity in Citrus grandis ‘Tomentosa’ fruits. Int J Mol Sci 24(14):11681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang J, Hu J, Tan R, Han Y, Li Z (2019) Expression of IbVPE1 from sweet potato in Arabidopsis affects leaf development, flowering time and chlorophyll catabolism. BMC Plant Biol 19(1):184

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim Y, Wang M, Bai Y, Zeng Z, Guo F, Han N, Bian H, Wang J, Pan J, Zhu M (2014) Bcl-2 suppresses activation of VPEs by inhibiting cytosolic Ca2+ level with elevated K+ efflux in NaCl-induced PCD in rice. Plant Physiol Biochem 80:168–175

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita T, Yamada K, Hiraiwa N, Kondo M, Nishimura M, Hara-Nishimura I (1999) Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J 19(1):43–53

    Article  CAS  PubMed  Google Scholar 

  • Kooiker M, Drenth J, Glassop D, McIntyre CL, Xue G-P (2013) TaMYB13-1, a R2R3 MYB transcription factor, regulates the fructan synthetic pathway and contributes to enhanced fructan accumulation in bread wheat. J Exp Bot 64(12):3681–3696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumamaru T, Uemura Y, Inoue Y, Takemoto Y, Siddiqui SU, Ogawa M, Hara-Nishimura I, Satoh H (2010) Vacuolar processing enzyme plays an essential role in the crystalline structure of glutelin in rice seed. Plant Cell Physiol 51(1):38–46

    Article  CAS  PubMed  Google Scholar 

  • Kuroyanagi M, Nishimura M, Hara-Nishimura I (2002) Activation of Arabidopsis vacuolar processing enzyme by self-catalytic removal of an auto-inhibitory domain of the C-terminal propeptide. Plant Cell Physiol 43(2):143–151

    Article  CAS  PubMed  Google Scholar 

  • Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I (2005) Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J Biol Chem 280(38):32914–32920

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Khedkar S, Bork P (2021) SMART: recent updates, new developments and status in 2020. Nucleic Acids Res 49(D1):D458–D460

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Zhao Y, Rahman S, She M, Zhang J, Yang R, Islam S, O’Hara G, Varshney R, Liu H, Ma H, Ma W (2023) The putative vacuolar processing enzyme gene TaVPE3cB is a candidate gene for wheat stem pith-thickness. Theoret Appl Genet 136(6):138

    Article  CAS  Google Scholar 

  • Lu W, Deng M, Guo F, Wang M, Zeng Z, Han N, Yang Y, Zhu M, Bian H (2016) Suppression of OsVPE3 enhances salt tolerance by attenuating vacuole rupture during programmed cell death and affects stomata development in rice. Rice 9(1):65

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinoia E, Mimura T, Hara-Nishimura I, Shiratake K (2018) The multifaceted roles of plant vacuoles. Plant Cell Physiol 59(7):1285–1287

    CAS  PubMed  Google Scholar 

  • Mendes GC, Reis PA, Calil IP, Carvalho HH, Aragao FJ, Fontes EP (2013) GmNAC30 and GmNAC81 integrate the endoplasmic reticulum stress- and osmotic stress-induced cell death responses through a vacuolar processing enzyme. Proc Natl Acad Sci USA 110(48):19627–19632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Misas-Villamil JC, Toenges G, Kolodziejek I, Sadaghiani AM, Kaschani F, Colby T, Bogyo M, van der Hoorn RA (2013) Activity profiling of vacuolar processing enzymes reveals a role for VPE during oomycete infection. Plant J 73(4):689–700

    Article  CAS  PubMed  Google Scholar 

  • Nakaune S, Yamada K, Kondo M, Kato T, Tabata S, Nishimura M, Hara-Nishimura I (2005) A vacuolar processing enzyme, deltaVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17(3):876–887

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quadros IPS, Madeira NN, Loriato VAP, Saia TFF, Silva JC, Soares FAF, Carvalho JR, Reis PAB, Fontes EPB (2022) Cadmium-mediated toxicity in plant cells is associated with the DCD/NRP-mediated cell death response. Plant Cell Environ 45(2):556–571

    Article  CAS  PubMed  Google Scholar 

  • Radchuk V, Tran V, Hilo A, Muszynska A, Gündel A, Wagner S, Fuchs J, Hensel G, Ortleb S, Munz E, Rolletschek H, Borisjuk L (2021) Grain filling in barley relies on developmentally controlled programmed cell death. Commun Biol 4(1):428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reis PAB, Carpinetti PA, Freitas PPJ, Santos EGD, Camargos LF, Oliveira IHT, Silva JCF, Carvalho HH, Dal-Bianco M, Soares-Ramos JRL, Fontes EPB (2016) Functional and regulatory conservation of the soybean ER stress-induced DCD/NRP-mediated cell death signaling in plants. BMC Plant Biol 16(1):156

    Article  PubMed  PubMed Central  Google Scholar 

  • Severin AJ, Woody JL, Bolon YT, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10:160

    Article  PubMed  PubMed Central  Google Scholar 

  • Sherman BT, Hao M, Qiu J, Jiao X, Baseler MW, Lane HC, Imamichi T, Chang W (2022) DAVID: a web server for functional enrichment analysis and functional annotation of gene lists (2021 update). Nucleic Acids Res 50(W1):W216–W221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimada T, Yamada K, Kataoka M, Nakaune S, Koumoto Y, Kuroyanagi M, Tabata S, Kato T, Shinozaki K, Seki M, Kobayashi M, Kondo M, Nishimura M, Hara-Nishimura I (2003) Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J Biol Chem 278(34):32292–32299

    Article  CAS  PubMed  Google Scholar 

  • Shimada T, Takagi J, Ichino T, Shirakawa M, Hara-Nishimura I (2018) Plant vacuoles. Annu Rev Plant Biol 69:123–145

    Article  CAS  PubMed  Google Scholar 

  • Song J, Yang F, Xun M, Xu L, Tian X, Zhang W, Yang H (2020) Genome-wide identification and characterization of vacuolar processing enzyme gene family and diverse expression under stress in apple (Malus x Domestic). Front Plant Sci 11:626

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang Y, Wang R, Gong P, Li S, Wang Y, Zhang C (2016) Gene cloning, expression and enzyme activity of Vitis vinifera vacuolar processing enzymes (VvVPEs). PLoS ONE 11(8):e0160945

    Article  PubMed  PubMed Central  Google Scholar 

  • Teper-Bamnolker P, Buskila Y, Lopesco Y, Ben-Dor S, Saad I, Holdengreber V, Belausov E, Zemach H, Ori N, Lers A, Eshel D (2012) Release of apical dominance in potato tuber is accompanied by programmed cell death in the apical bud meristem. Plant Physiol 158(4):2053–2067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian F, Yang DC, Meng YQ, Jin J, Gao G (2020) PlantRegMap: charting functional regulatory maps in plants. Nucleic Acids Res 48(D1):D1104–D1113

    CAS  PubMed  Google Scholar 

  • Van K, Kim DH, Cai CM, Kim MY, Shin JH, Graham MA, Shoemaker RC, Choi BS, Yang TJ, Lee SH (2008) Sequence level analysis of recently duplicated regions in soybean [Glycine max (L.) Merr] genome. DNA Res 15(2):93–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Wyk SG, Du Plessis M, Cullis CA, Kunert KJ, Vorster BJ (2014) Cysteine protease and cystatin expression and activity during soybean nodule development and senescence. BMC Plant Biol 14:294

    Article  PubMed  PubMed Central  Google Scholar 

  • Vorster BJ, Cullis CA, Kunert KJ (2019) Plant vacuolar processing enzymes. Front Plant Sci 10:479

    Article  PubMed  PubMed Central  Google Scholar 

  • Wan Abdullah WMAN, Saidi NB, Yusof MT, Wee CY, Loh HS, Ong-Abdullah J, Lai KS (2022) Vacuolar processing enzymes modulating susceptibility response to Fusarium oxysporum f. sp. cubense tropical race 4 infections in banana. Front Plant Sci 12:769855

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Rehmani MS, Chen Q, Yan J, Zhao P, Li C, Zhai Z, Zhou N, Yang B, Jiang YQ (2022) Rapeseed NAM transcription factor positively regulates leaf senescence via controlling senescence-associated gene expression. Plant Sci 323:111373

    Article  CAS  PubMed  Google Scholar 

  • Wleklik K, Borek S (2023) Vacuolar processing enzymes in plant programmed cell death and autophagy. Int J Mol Sci 24(2):1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada K, Shimada T, Nishimura M, Hara-Nishimura I (2005) A VPE family supporting various vacuolar functions in plants. Physiol Plantarum 123(4):369–375

    Article  CAS  Google Scholar 

  • Yamada K, Basak AK, Goto-Yamada S, Tarnawska-Glatt K, Hara-Nishimura I (2020) Vacuolar processing enzymes in the plant life cycle. New Phytol 226(1):21–31

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki Y, Randall SK (2016) Functionality of soybean CBF/DREB1 transcription factors. Plant Sci 246:80–90

    Article  CAS  PubMed  Google Scholar 

  • Yan D, Duermeyer L, Leoveanu C, Nambara E (2014) The functions of the endosperm during seed germination. Plant Cell Physiol 55(9):1521–1533

    Article  CAS  PubMed  Google Scholar 

  • Zakharov A, Muntz K (2004) Seed legumains are expressed in stamens and vegetative legumains in seeds of Nicotiana tabacum L. J Exp Bot 55(402):1593–1595

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Zheng X, Zhang Z (2010) The role of vacuolar processing enzymes in plant immunity. Plant Signal Behav 5(12):1565–1567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Li QF, Huang WW, Xu XY, Zhang XL, Hui MX, Zhang MK, Zhang LG (2013) A vacuolar processing enzyme RsVPE1 gene of radish is involved in floral bud abortion under heat stress. Int J Mol Sci 14(7):13346–13359

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Wang S, Yu F, Tang J, Shan X, Bao K, Yu L, Wang H, Fei Z, Li J (2019) Genome-wide characterization and expression profiling of SWEET genes in cabbage (Brassica oleracea var. capitata L.) reveal their roles in chilling and clubroot disease responses. BMC Genomics 20(1):93

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xiao Y, Deng X, Feng H, Li Z, Zhang L, Chen H (2020) OsVPE3 mediates GA-induced programmed cell death in rice aleurone layers via interacting with actin microfilaments. Rice 13(1):22

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng P, Zheng C, Otegui MS, Li F (2022) Endomembrane mediated-trafficking of seed storage proteins: from Arabidopsis to cereal crops. J Exp Bot 73(5):1312–1326

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Wang X, Tian J, Zhang X, Yu T, Li Y, Li D (2022) Genome-wide analysis of VPE family in four Gossypium species and transcriptional expression of VPEs in the upland cotton seedlings under abiotic stresses. Funct Integr Genomics 22(2):179–192

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research was funded by National Natural Science Foundation of China (32201730) and the funding project of Northeast Geological S&T Innovation Center of China Geological Survey (QCJJ2022-44).

Funding

This research was funded by National Natural Science Foundation of China (32201730) and the funding project of Northeast Geological S&T Innovation Center of China Geological Survey (QCJJ2022-44).

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X. D. and Y. Y. conceived and designed the work; Y. Y. and Z. L. contributed to funding acquisition and supervision; X. D. and K. Z. collected the experimental data and conducted bioinformatic analysis; X. D. wrote the original draft; K. Z., Y. Y., and Z. L. revised and edited the manuscript. All authors have read and agreed the published version of the manuscript.

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Correspondence to Yang Yu.

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Duan, X., Zhang, K., Yu, Y. et al. Genome-Wide Analysis of Soybean Vacuolar Processing Enzyme Gene Family Reveals Their Roles in Plant Development and Response to Stress Conditions. J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11309-8

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