The grapevine kinome: annotation, classification and expression patterns in developmental processes and stress responses

Kaikai Zhu , Xiaolong Wang , Jinyi Liu , Jun Tang , Qunkang Cheng , Jin-Gui Chen , Zong-Ming (Max) Cheng

Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) : 19

PDF (4382KB)
Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) :19 DOI: 10.1038/s41438-018-0027-0
Article
research-article
The grapevine kinome: annotation, classification and expression patterns in developmental processes and stress responses
Author information +
History +
PDF (4382KB)

Abstract

Protein kinases (PKs) have evolved as the largest family of molecular switches that regulate protein activities associated with almost all essential cellular functions. Only a fraction of plant PKs, however, have been functionally characterized even in model plant species. In the present study, the entire grapevine kinome was identified and annotated using the most recent version of the grapevine genome. A total of 1168 PK-encoding genes were identified and classified into 20 groups and 121 families, with the RLK-Pelle group being the largest, with 872 members. The 1168 kinase genes were unevenly distributed over all 19 chromosomes, and both tandem and segmental duplications contributed to the expansion of the grapevine kinome, especially of the RLK-Pelle group. Ka/Ks values indicated that most of the tandem and segmental duplication events were under purifying selection. The grapevine kinome families exhibited different expression patterns during plant development and in response to various stress treatments, with many being coexpressed. The comprehensive annotation of grapevine kinase genes, their patterns of expression and coexpression, and the related information facilitate a more complete understanding of the roles of various grapevine kinases in growth and development, responses to abiotic stress, and evolutionary history.

Cite this article

Download citation ▾
Kaikai Zhu, Xiaolong Wang, Jinyi Liu, Jun Tang, Qunkang Cheng, Jin-Gui Chen, Zong-Ming (Max) Cheng. The grapevine kinome: annotation, classification and expression patterns in developmental processes and stress responses. Horticulture Research, 2018, 5 (1) : 19 DOI:10.1038/s41438-018-0027-0

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Bennett, J. Protein phosphorylation in green plant chloroplasts. Annu. Rev. Plant Biol. 42, 281-311 (1991).

[2]

Lehti-Shiu, M. D. & Shiu, S. H. Diversity, classification and function of the plant protein kinase superfamily. Philos. Trans. R Soc. Lond. B Biol. Sci. 367, 2619-2639 (2012).

[3]

Liu, J. et al. Soybean kinome: functional classification and gene expression patterns. J. Exp. Bot. 66, 1919-1934 (2015).

[4]

Ben-David, Y., Letwin, K., Tannock, L., Bernstein, A. & Pawson, T. A mammalian protein kinase with potential for serine/threonine and tyrosine phosphorylation is related to cell cycle regulators. EMBO J. 10, 317-325 (1991).

[5]

Zulawski, M., Schulze, G., Braginets, R., Hartmann, S . & Schulze, W. X. The Arabidopsis kinome: phylogeny and evolutionary insights into functional diversification. BMC Genomics 15, 548 (2014).

[6]

Keates, R. Cyclic nucleotide-independent protein kinase from pea shoots. Biochem. Biophys. Res. Commun. 54, 655-661 (1973).

[7]

Lawton, M. A., Yamamoto, R. T., Hanks, S. K. & Lamb, C. J. Molecular cloning of plant transcripts encoding protein kinase homologs. Proc. Natl Acad. Sci. USA 86, 3140-3144 (1989).

[8]

Ichimura, K., Mizoguchi, T., Yoshida, R., Yuasa, T. & Shinozaki, K. Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24, 655-665 (2000).

[9]

Tran, L.-S. P. et al. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl Acad. Sci. USA 104, 20623-20628 (2007).

[10]

Pan, J. et al. ZmMPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235, 661-676 (2012).

[11]

Zhu, K. et al. Evolution of an intron-poor cluster of the CIPK gene family and expression in response to drought stress in soybean. Sci. Rep. 6, 28225 (2016).

[12]

Yang, K.-Y., Liu, Y. & Zhang, S. Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc. Natl Acad. Sci. USA 98, 741-746 (2001).

[13]

Wang, X. J. et al. Two coupled components of the mitogen-activated protein kinase cascade MdMPK1 and MdMKK1 from apple function in ABA signal transduction. Plant Cell Physiol. 51, 754-766 (2010).

[14]

Champion, A., Kreis, M., Mockaitis, K., Picaud, A. & Henry, Y. Arabidopsis kinome: after the casting. Funct. Integr. Genomics 4, 163-187 (2004).

[15]

Dardick, C., Chen, J., Richter, T., Ouyang, S. & Ronald, P. The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol. 143, 579-586 (2007).

[16]

Chandran, A. K. N. et al. Updated Rice Kinase Database RKD 2.0: enabling transcriptome and functional analysis of rice kinase genes. Rice 9, 40 (2016).

[17]

Caenepeel, S., Charydczak, G., Sudarsanam, S., Hunter, T. & Manning, G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc. Natl Acad. Sci. USA 101, 11707-11712 (2004).

[18]

Manning, G., Whyte, D. B., Martinez, R., Hunter, T. & Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934 (2002).

[19]

Hanada, K., Zou, C., Lehti-Shiu, M. D., Shinozaki, K. & Shiu, S. H. Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol. 148, 993-1003 (2008).

[20]

Hanks, S. K. & Hunter, T. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9, 576-596 (1995).

[21]

Fasoli, M. et al. The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24, 3489-3505 (2012).

[22]

Ferrandino, A. & Lovisolo, C. Abiotic stress effects on grapevine (Vitis vinifera L.): Focus on abscisic acid-mediated consequences on secondary metabolism and berry quality . Environ. Exp. Bot. 103, 138-147 (2014).

[23]

Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463-467 (2007).

[24]

Wang, G. et al. Validation by isolation and expression analyses of the mitogen-activated protein kinase gene family in the grapevine (Vitis vinifera L.) . Aust. J. Grape Wine Res. 20, 255-262 (2014).

[25]

Chen, F. et al. The evolutionary history and diverse physiological roles of the grapevine calcium-dependent protein kinase gene family. PLoS ONE 8, e80818 (2013).

[26]

Liu, J. Y., Chen, N. N., Cheng, Z. M. & Xiong, J. S. Genome-wide identification, annotation and expression profile analysis of SnRK2 gene family in grapevine. Aust. J. Grape Wine Res. 22, 478-488 (2016).

[27]

Finn, R. D. et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res. 44, D279-D285 (2016).

[28]

Eddy, S. R. Profile hidden Markov models. Bioinformatics 14, 755-763 (1998).

[29]

Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 (2013).

[30]

Gasteiger, E. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31, 3784-2788 (2003).

[31]

Horton, P. et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585-W587 (2007).

[32]

Yang, X. et al. The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol. 148, 1189-1200 (2008).

[33]

Wang, Y., Li, J. & Paterson, A. H. MCScanX-transposed: detecting transposed gene duplications based on multiple colinearity scans. Bioinformatics 29, 1458-1460 (2013).

[34]

Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948 (2007).

[35]

Gaut, B. S., Morton, B. R., McCaig, B. C. & Clegg, M. T. Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc. Natl Acad. Sci. USA 93, 10274-10279 (1996).

[36]

Tang, J. et al. Characterization and co-expression analysis of WRKY orthologs involved in responses to multiple abiotic stresses in Pak-choi (Brassica campestris ssp. chinensis) . BMC Plant Biol. 13, 188 (2013).

[37]

Lehti-Shiu, M. D., Zou, C., Hanada, K. & Shiu, S. H. Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol. 150, 12-26 (2009).

[38]

Zhang, Z. et al. KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 4, 259-263 (2006).

[39]

Clouse, S. D. Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23, 1219-1230 (2011).

[40]

Wei, K., Wang, Y. & Xie, D. Identification and expression profile analysis of the protein kinase gene superfamily in maize development. Mol. Breed. 33, 155-172 (2014).

[41]

Du, D., Rawat, N., Deng, Z. & Gmitter, F. G. Jr. Construction of citrus gene coexpression networks from microarray data using random matrix theory. Hortic. Res. 2, 15026 (2015).

[42]

Liang, Y.-H. et al. Construction and validation of a gene co-expression network in grapevine (Vitis vinifera. L.) . Hortic. Res. 1, 14040 (2014).

[43]

Shiu, S. H. et al. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220-1234 (2004).

[44]

Singh, D. K. et al. The tomato kinome and the tomato kinase library ORFeome: novel resources for the study of kinases and signal transduction in tomato and solanaceae species. Mol. Plant Microbe Interact. 27, 7-17 (2014).

[45]

Epelboin, Y. et al. The kinome of pacific oyster Crassostrea gigas, its expression during development and in response to environmental factors . PLoS ONE 11, e0155435 (2016).

[46]

Wei, W., Shu, S., Zhu, W., Xiong, Y. & Peng, F. The kinome of edible and medicinal fungus Wolfiporia cocos . Front. Microbiol. 7, 1495 (2016).

[47]

Kong, H. et al. Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J. 50, 873-885 (2007).

[48]

Shiu, S.-H. & Bleecker, A. B. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132, 530-543 (2003).

[49]

Becraft, P. W. Receptor kinase signaling in plant development. Annu. Rev. Cell Dev. Biol. 18, 163-192 (2002).

[50]

Xiong, L. Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15, 745-759 (2003).

[51]

Yu, X. C. et al. Expression of a grape calcium-dependent protein kinase ACPK1 in Arabidopsis thaliana promotes plant growth and confers abscisic acid-hypersensitivity in germination, postgermination growth, and stomatal movement . Plant Mol. Biol. 64, 531-538 (2007).

[52]

Dubrovina, A. S., Kiselev, K. V., Khristenko, V. S. & Aleynova, O. A. VaCPK20, a calcium-dependent protein kinase gene of wild grapevine Vitis amurensis Rupr., mediates cold and drought stress tolerance . J. Plant Physiol. 185, 1-12 (2015).

[53]

Gao, L.-L. & Xue, H.-W. Global analysis of expression profiles of rice receptor-like kinase genes. Mol. Plant 5, 143-153 (2012).

[54]

Ouyang, S. Q. et al. Receptor-like kinase OsSIK1 improves drought and salt stress tolerance in rice (Oryza sativa) plants . Plant J. 62, 316-329 (2010).

[55]

Chae, L., Sudat, S., Dudoit, S., Zhu, T. & Luan, S. Diverse transcriptional programs associated with environmental stress and hormones in the Arabidopsis receptor-like kinase gene family. Mol. Plant 2, 84-107 (2009).

[56]

Osakabe, Y. et al. Overproduction of the membrane-bound receptor-like protein kinase 1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J. Biol. Chem. 285, 9190-9201 (2010).

[57]

Zhang, H. et al. Identification and characterization of CBL and CIPK gene families in canola (Brassica napus L.) . BMC Plant Biol. 14, 8 (2014).

[58]

Tang, J. et al. Characterization of CIPK family in Asian pear (Pyrus bretschneideri Rehd) and co-expression analysis related to salt and osmotic stress responses . Front. Plant Sci. 7, 1361 (2016).

PDF (4382KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/