Abstract
Background
The plant-specific valine-glutamine (VQ) motif containing proteins tightly regulate plant growth, development, and stress responses. However, the genome-wide identification and functional analysis of Brassica oleracea (B. oleracea) VQ genes have not been reported.
Objective
To identify the VQ gene family in B. oleracea and analyze the function of Bo25-1 in pollen germination.
Methods
The Hidden Markov Model (HMM) of VQ family was used to query the BoVQ genes in the B. oleracea genome. The BoVQ genes preferentially expressed in anthers were screened by qRT-PCR. Subcellular localization of VQ25-1 was observed in Nicotiana benthamiana (N. benthamiana) leaves. To analysis the role of BoVQ25-1 in pollen germination, the expression of BoVQ25-1 was suppressed using antisense-oligonucleotides (AS-ODN).
Results
A total of 64 BoVQ genes were identified in the B. oleracea genome. BoVQ25-1 was found to be preferentially expressed in the B. oleracea anthers. BoVQ25-1 was cloned from the anthers of the B. oleracea cultivar ‘Fast Cycle’. BoVQ25-1 is localized to the nucleus. The pollen germination rate significantly decreased after AS-ODN treatment.
Conclusion
Sixty-four BoVQ genes were identified in the B. oleracea genome, of which BoVQ25-1 plays an important role in pollen germination.
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Data availability
The original contributions presented in the study are publicly available.
References
Artimo P, Jonnalagedda M, Arnold K et al (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40:W597-603. https://doi.org/10.1093/nar/gks400
Bailey TL, Boden M, Buske FA et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-208. https://doi.org/10.1093/nar/gkp335
Berger F, Twell D (2011) Germline specification and function in plants. Annu Rev Plant Biol 62:461–484. https://doi.org/10.1146/annurev-arplant-042110-103824
Chen C, Chen H, Zhang Y et al (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen S, Cao H, Huang B et al (2022) The WRKY10-VQ8 module safely and effectively regulates rice thermotolerance. Plant Cell Environ 45:2126–2144. https://doi.org/10.1111/pce.14329
Cheng Y, Zhou Y, Yang Y et al (2012) Structural and functional analysis of VQ motif-containing proteins in arabidopsis as interacting proteins of wrky transcription factors. Plant Physiol 159:810–825. https://doi.org/10.1104/pp.112.196816
Cheng X, Wang Y, Xiong R et al (2020) A Moso bamboo gene VQ28 confers salt tolerance to transgenic Arabidopsis plants. Planta 251:99. https://doi.org/10.1007/s00425-020-03391-5
Ding H, Yuan G, Mo S et al (2019) Genome-wide analysis of the plant-specific VQ motif-containing proteins in tomato (Solanum lycopersicum) and characterization of SlVQ6 in thermotolerance. Plant Physiol Biochem 143:29–39. https://doi.org/10.1016/j.plaphy.2019.08.019
Dong Q, Zhao S, Duan D et al (2018) Structural and functional analyses of genes encoding VQ proteins in apple. Plant Sci 272:208–219. https://doi.org/10.1016/j.plantsci.2018.04.029
El-Gebali S, Mistry J, Bateman A et al (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432. https://doi.org/10.1093/nar/gky995
Guan Y, Meng X, Khanna R et al (2014) Phosphorylation of a WRKY transcription factor by MAPKs is required for pollen development and function in Arabidopsis. PLoS Genet 10:e1004384. https://doi.org/10.1371/journal.pgen.1004384
Guo J, Chen J, Yang J et al (2018) Identification, characterization and expression analysis of the VQ motif-containing gene family in tea plant (Camellia sinensis). BMC Genomics 19:710. https://doi.org/10.1186/s12864-018-5107-x
Hafidh S, Fíla J, Honys D (2016) Male gametophyte development and function in angiosperms: a general concept. Plant Reprod 29:31–51. https://doi.org/10.1007/s00497-015-0272-4
Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85. https://doi.org/10.1186/gb-2004-5-11-r85
Horton P, Park K-J, Obayashi T et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585-587. https://doi.org/10.1093/nar/gkm259
Hu Y, Chen L, Wang H et al (2013) Arabidopsis transcription factor WRKY8 functions antagonistically with its interacting partner VQ9 to modulate salinity stress tolerance. Plant J 74:730–745. https://doi.org/10.1111/tpj.12159
Jiang S-Y, Sevugan M, Ramachandran S (2018) Valine-glutamine (VQ) motif coding genes are ancient and non-plant-specific with comprehensive expression regulation by various biotic and abiotic stresses. BMC Genomics 19:342. https://doi.org/10.1186/s12864-018-4733-7
Jing Y, Lin R (2015) The VQ motif-containing protein family of plant-specific transcriptional regulators. Plant Physiol 169:371–378. https://doi.org/10.1104/pp.15.00788
Kim DY, Kwon SI, Choi C et al (2013) Expression analysis of rice VQ genes in response to biotic and abiotic stresses. Gene 529:208–214. https://doi.org/10.1016/j.gene.2013.08.023
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lei R, Li X, Ma Z et al (2017) Arabidopsis WRKY2 and WRKY34 transcription factors interact with VQ20 protein to modulate pollen development and function. Plant J 91:962–976. https://doi.org/10.1111/tpj.13619
Lei R, Ma Z, Yu D (2018) WRKY2/34-VQ20 modules in arabidopsis thaliana negatively regulate expression of a trio of related MYB transcription factors during pollen development. Front Plant Sci 9:331. https://doi.org/10.3389/fpls.2018.00331
Li Y, Jing Y, Li J et al (2014) Arabidopsis VQ MOTIF-CONTAINING PROTEIN29 represses seedling deetiolation by interacting with PHYTOCHROME-INTERACTING FACTOR1. Plant Physiol 164:2068–2080. https://doi.org/10.1104/pp.113.234492
Liu C, Liu H, Zhou C, Timko MP (2020) Genome-Wide Identification of the VQ Protein Gene Family of Tobacco (Nicotiana tabacum L.) and Analysis of Its Expression in Response to Phytohormones and Abiotic and Biotic Stresses. Genes (Basel) 11:E284. https://doi.org/10.3390/genes11030284
Luo M, Dennis ES, Berger F et al (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci USA 102:17531–17536. https://doi.org/10.1073/pnas.0508418102
Ma H, Sundaresan V (2010) Development of flowering plant gametophytes. Curr Top Dev Biol 91:379–412. https://doi.org/10.1016/S0070-2153(10)91013-2
Marchler-Bauer A, Lu S, Anderson JB et al (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225-229. https://doi.org/10.1093/nar/gkq1189
McCormick S (2004) Control of male gametophyte development. Plant Cell 16(Suppl):S142-153. https://doi.org/10.1105/tpc.016659
Mistry J, Finn RD, Eddy SR et al (2013) Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res 41:e121. https://doi.org/10.1093/nar/gkt263
Motomura K, Arae T, Araki-Uramoto H et al (2020) AtNOT1 is a novel regulator of gene expression during pollen development. Plant Cell Physiol 61:712–721. https://doi.org/10.1093/pcp/pcz235
Niu Q-K, Liang Y, Zhou J-J et al (2013) Pollen-expressed transcription factor 2 encodes a novel plant-specific TFIIB-related protein that is required for pollen germination and embryogenesis in arabidopsis. Mol Plant 6:1091–1108. https://doi.org/10.1093/mp/sst083
Perruc E, Charpenteau M, Ramirez BC et al (2004) A novel calmodulin-binding protein functions as a negative regulator of osmotic stress tolerance in Arabidopsis thaliana seedlings. Plant J 38:410–420. https://doi.org/10.1111/j.1365-313X.2004.02062.x
Shan N, Xiang Z, Sun J et al (2021) Genome-wide analysis of valine-glutamine motif-containing proteins related to abiotic stress response in cucumber (Cucumis sativus L.). BMC Plant Biol 21:492. https://doi.org/10.1186/s12870-021-03242-9
Song W, Zhao H, Zhang X et al (2015) Genome-wide identification of VQ motif-containing proteins and their expression profiles under abiotic stresses in Maize. Front Plant Sci 6:1177. https://doi.org/10.3389/fpls.2015.01177
Wang A, Garcia D, Zhang H et al (2010) The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63:670–679. https://doi.org/10.1111/j.1365-313X.2010.04271.x
Wang M, Vannozzi A, Wang G et al (2015) A comprehensive survey of the grapevine VQ gene family and its transcriptional correlation with WRKY proteins. Front Plant Sci 6:417. https://doi.org/10.3389/fpls.2015.00417
Wang Y, Liu H, Zhu D et al (2017) Genome-wide analysis of VQ motif-containing proteins in Moso bamboo (Phyllostachys edulis). Planta 246:165–181. https://doi.org/10.1007/s00425-017-2693-9
Xia C, Wang Y-J, Li W-Q et al (2010) The Arabidopsis eukaryotic translation initiation factor 3, subunit F (AteIF3f), is required for pollen germination and embryogenesis. Plant J 63:189–202. https://doi.org/10.1111/j.1365-313X.2010.04237.x
Ye Y-J, Xiao Y-Y, Han Y-C et al (2016) Banana fruit VQ motif-containing protein5 represses cold-responsive transcription factor MaWRKY26 involved in the regulation of JA biosynthetic genes. Sci Rep 6:23632. https://doi.org/10.1038/srep23632
Yuan G, Qian Y, Ren Y et al (2021) The role of plant-specific VQ motif-containing proteins: an ever-thickening plot. Plant Physiol Biochem 159:12–16. https://doi.org/10.1016/j.plaphy.2020.12.005
Zhang G, Wang F, Li J et al (2015) Genome-wide identification and analysis of the VQ motif-containing protein family in Chinese cabbage (Brassica rapa L. ssp. Pekinensis). IJMS 16:28683–28704. https://doi.org/10.3390/ijms161226127
Zheng J, Li H, Guo Z, Zhuang X, Huang W, Mao C, Feng H, Zhang Y, Wu H, Zhou Y (2022) Comprehensive identification and expression profiling of the vq motif-containing gene family in brassica juncea. Biology 11:1814. https://doi.org/10.3390/biology11121814
Zhou Y, Yang Y, Zhou X et al (2016) Structural and functional characterization of the VQ protein family and VQ protein variants from soybean. Sci Rep 6:34663. https://doi.org/10.1038/srep34663
Zhu H, Zhou Y, Zhai H et al (2020) A novel sweetpotato WRKY transcription factor, IbWRKY2, positively regulates drought and salt tolerance in transgenic arabidopsis. Biomolecules 10:E506. https://doi.org/10.3390/biom10040506
Zou Z, Liu F, Huang S, Fernando WGD (2021) Genome-wide identification and analysis of the valine-glutamine motif-containing gene family in brassica napus and functional characterization of BnMKS1 in response to leptosphaeria maculans. Phytopathology 111:281–292. https://doi.org/10.1094/PHYTO-04-20-0134-R
Acknowledgements
This work was supported by the Chongqing Natural Science Foundation (cstc2019jcyj-msxmX0340) and the Chongqing Science and Technology Commission (cstc2021jscx-tpyzxX0003). The funding body was not involved in the experimental design of the study, data collection, analysis, and interpretation, and in writing the manuscript.
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MY and ZL performed the experiments and processed the pictures. MY and YY drafted and revised the manuscript. MY, LG, XH, XM and ZH contributed to the data analysis. QG provided plant tissues, laboratory facilities, and project supervision. All authors approved the final draft of the manuscript.
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Yang, M., Liu, Z., Yu, Y. et al. Genome-wide identification of the valine-glutamine motif containing gene family and the role of VQ25-1 in pollen germination in Brassica oleracea. Genes Genom 45, 921–934 (2023). https://doi.org/10.1007/s13258-023-01375-9
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DOI: https://doi.org/10.1007/s13258-023-01375-9