Skip to main content
SpringerLink
Log in

Genome-wide identification and homeolog-specific expression analysis of the SnRK2 genes in Brassica napus guard cells

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Sucrose non-fermenting-1-related protein kinase 2 (SnRK2) proteins constitute a small plant-specific serine/threonine kinase family involved in abscisic acid (ABA) signaling and plant responses to biotic and abiotic stresses. Although SnRK2s have been well-studied in Arabidopsis thaliana, little is known about SnRK2s in Brassica napus. Here we identified 30 putative sequences encoding 10 SnRK2 proteins in the B. napus genome and the expression profiles of a subset of 14 SnRK2 genes in guard cells of B. napus. In agreement with its polyploid origin, B. napus maintains both homeologs from its diploid parents. The results of quantitative real-time PCR (qRT-PCR) and reanalysis of RNA-Seq data showed that certain BnSnRK2 genes were commonly expressed in leaf tissues in different varieties of B. napus. In particular, qRT-PCR results showed that 12 of the 14 BnSnRK2s responded to drought stress in leaves and in ABA-treated guard cells. Among them, BnSnRK2.4 and BnSnRK2.6 were of interest because of their robust responsiveness to ABA treatment and drought stress. Notably, BnSnRK2 genes exhibited up-regulation of different homeologs, particularly in response to abiotic stress. The homeolog expression bias in BnSnRK2 genes suggests that parental origin of genes might be responsible for efficient regulation of stress responses in polyploids. This work has laid a foundation for future functional characterization of the different BnSnKR2 homeologs in B. napus and its parents, especially their functions in guard cell signaling and stress responses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Akama S, Shimizu-Inatsugi R, Shimizu KK, Sese J (2014) Genome-wide quantification of homeolog expression ratio revealed nonstochastic gene regulation in synthetic allopolyploid Arabidopsis. Nucleic Acids Res 42:e46. doi:10.1093/nar/gkt1376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  • Belin C, de Franco PO, Bourbousse C, Chaignepain S, Schmitter JM, Vavasseur A, Giraudat J, Barbier-Brygoo H, Thomine S (2006) Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol 141:1316–1327. doi:10.1104/pp.106.079327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bohmer M, Schroeder JI (2011) Quantitative transcriptomic analysis of abscisic acid-induced and reactive oxygen species-dependent expression changes and proteomic profiling in Arabidopsis suspension cells. Plant J 67:105–118. doi:10.1111/j.1365-313X.2011.04579.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boudsocq M, Barbier-Brygoo H, Lauriere C (2004) Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J Biol Chem 279:41758–41766. doi:10.1074/jbc.M405259200

    Article  CAS  PubMed  Google Scholar 

  • Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Correa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier MC, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee TH, Thi VH, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CH, Wang X, Canaguier A, Chauveau A, Berard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury JM, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953. doi:10.1126/science.1253435

    Article  CAS  PubMed  Google Scholar 

  • Chen ZJ, Ni Z (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. BioEssays 28:240–252. doi:10.1002/bies.20374

    Article  PubMed  Google Scholar 

  • Cho YH, Hong JW, Kim EC, Yoo SD (2012) Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol 158:1955–1964. doi:10.1104/pp.111.189829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coello P, Hey SJ, Halford NG (2011) The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. J Exp Bot 62:883–893. doi:10.1093/jxb/erq331

    Article  CAS  PubMed  Google Scholar 

  • Combes MC, Cenci A, Baraille H, Bertrand B, Lashermes P (2012) Homeologous gene expression in response to growing temperature in a recent allopolyploid (Coffea arabica L.). J Hered 103:36–46. doi:10.1093/jhered/esr120

    Article  CAS  PubMed  Google Scholar 

  • de Carvalho K, Petkowicz CL, Nagashima GT, Bespalhok Filho JC, Vieira LG, Pereira LF, Domingues DS (2014) Homeologous genes involved in mannitol synthesis reveal unequal contributions in response to abiotic stress in Coffea arabica. Mol Genet Genomics 289:951–963. doi:10.1007/s00438-014-0864-y

    Article  PubMed  Google Scholar 

  • Dong S, Adams KL (2011) Differential contributions to the transcriptome of duplicated genes in response to abiotic stresses in natural and synthetic polyploids. New Phytol 190:1045–1057. doi:10.1111/j.1469-8137.2011.03650.x

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Fisher RA (1922) On the interpretation of χ2 from contingency tables, and the calculation of P. J R Stat Soc 85:87–94

    Article  Google Scholar 

  • Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385. doi:10.1073/pnas.0903144106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19:485–494. doi:10.1105/tpc.106.048538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50:2123–2132. doi:10.1093/pcp/pcp147

    Article  CAS  PubMed  Google Scholar 

  • Gan X, Stegle O, Behr J, Steffen JG, Drewe P, Hildebrand KL, Lyngsoe R, Schultheiss SJ, Osborne EJ, Sreedharan VT, Kahles A, Bohnert R, Jean G, Derwent P, Kersey P, Belfield EJ, Harberd NP, Kemen E, Toomajian C, Kover PX, Clark RM, Ratsch G, Mott R (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477:419–423. doi:10.1038/nature10414

    Article  CAS  PubMed  Google Scholar 

  • Gao G, Li J, Li H, Li F, Xu K, Yan G, Chen B, Qiao J, Wu X (2014) Comparison of the heat stress induced variations in DNA methylation between heat-tolerant and heat-sensitive rapeseed seedlings. Breed Sci 64:125–133. doi:10.1270/jsbbs.64.125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halford NG, Hardie DG (1998) SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant Mol Biol 37:735–748

    Article  CAS  PubMed  Google Scholar 

  • Halford NG, Hey SJ (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem J 419:247–259. doi:10.1042/BJ20082408

    Article  CAS  PubMed  Google Scholar 

  • Halford NG, Hey S, Jhurreea D, Laurie S, McKibbin RS, Paul M, Zhang Y (2003) Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J Exp Bot 54:467–475

    Article  CAS  PubMed  Google Scholar 

  • Higgins J, Magusin A, Trick M, Fraser F, Bancroft I (2012) Use of mRNA-seq to discriminate contributions to the transcriptome from the constituent genomes of the polyploid crop species Brassica napus. BMC Genom 13:247. doi:10.1186/1471-2164-13-247

    Article  CAS  Google Scholar 

  • Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680. doi:10.1104/pp.102.011999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Z, Yu Y, Wang R, Yao Y, Peng H, Ni Z, Sun Q (2011) Expression divergence of TaMBD2 homoeologous genes encoding methyl CpG-binding domain proteins in wheat (Triticum aestivum L.). Gene 471:13–18. doi:10.1016/j.gene.2010.10.001

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. doi:10.1093/bioinformatics/btu817

    Article  PubMed  PubMed Central  Google Scholar 

  • Huai J, Wang M, He J, Zheng J, Dong Z, Lv H, Zhao J, Wang G (2008) Cloning and characterization of the SnRK2 gene family from Zea mays. Plant Cell Rep 27:1861–1868. doi:10.1007/s00299-008-0608-8

    Article  CAS  PubMed  Google Scholar 

  • Huang Z, Tang J, Duan W, Wang Z, Song X, Hou X (2015) Molecular evolution, characterization, and expression analysis of SnRK2 gene family in Pak-choi (Brassica rapa ssp. chinensis). Front. Plant Sci 6:879. doi:10.3389/fpls.2015.00879

    Google Scholar 

  • Julkowska MM, McLoughlin F, Galvan-Ampudia CS, Rankenberg JM, Kawa D, Klimecka M, Haring MA, Munnik T, Kooijman EE, Testerink C (2015) Identification and functional characterization of the Arabidopsis Snf1-related protein kinase SnRK2.4 phosphatidic acid-binding domain. Plant Cell Environ 38:614–624. doi:10.1111/pce.12421

    Article  CAS  PubMed  Google Scholar 

  • Kim JM, To TK, Nishioka T, Seki M (2010) Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ 33:604–611. doi:10.1111/j.1365-3040.2009.02076.x

    Article  PubMed  Google Scholar 

  • Kline KG, Barrett-Wilt GA, Sussman MR (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci USA 107:15986–15991. doi:10.1073/pnas.1007879107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004) Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16:1163–1177. doi:10.1105/tpc.019943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44:939–949. doi:10.1111/j.1365-313X.2005.02583.x

    Article  CAS  PubMed  Google Scholar 

  • Koh J, Chen G, Yoo MJ, Zhu N, Dufresne D, Erickson JE, Shao H, Chen S (2015) Comparative proteomic analysis of Brassica napus in response to drought stress. J Proteome Res 14:3068–3081. doi:10.1021/pr501323d

    Article  CAS  PubMed  Google Scholar 

  • Kulik A, Wawer I, Krzywinska E, Bucholc M, Dobrowolska G (2011) SnRK2 protein kinases-key regulators of plant response to abiotic stresses. OMICS 15:859–872. doi:10.1089/omi.2011.0091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. doi:10.1093/bioinformatics/btp324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Adams KL (2007) Expression partitioning between genes duplicated by polyploidy under abiotic stress and during organ development. Curr Biol 17:1669–1674. doi:10.1016/j.cub.2007.08.030

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IA, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang TJ, Hu Q, Wang X, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Yang L, Min J, Zhang D, Jin D, Li W, Belcram H, Tu J, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park BS, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Li J, Hu Z, Zhuang M, Huang Y, Huang J, Shi J, Mei D, Liu J, Lee TH, Wang J, Jin H, Li Z, Li X, Zhang J, Xiao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Wang X, Wang J, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930. doi:10.1038/ncomms4930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Zhang X, Zhang K, An H, Hu K, Wen J, Shen J, Ma C, Yi B, Tu J, Fu T (2015a) Comparative analysis of the Brassica napus root and leaf transcript profiling in response to drought stress. Int J Mol Sci 16:18752–18777. doi:10.3390/ijms160818752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Xin M, Qin J, Peng H, Ni Z, Yao Y, Sun Q (2015b) Temporal transcriptome profiling reveals expression partitioning of homeologous genes contributing to heat and drought acclimation in wheat (Triticum aestivum L.). BMC Plant Biol 15:152. doi:10.1186/s12870-015-0511-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Lynch M, Force AG (2000) The origin of interspecific genomic incompatibility via gene duplication. Amer Nat 156:590–605

    Article  Google Scholar 

  • Marconi G, Pace R, Traini A, Raggi L, Lutts S, Chiusano M, Guiducci M, Falcinelli M, Benincasa P, Albertini E (2013) Use of MSAP markers to analyse the effects of salt stress on DNA methylation in rapeseed (Brassica napus var. oleifera). PLoS ONE 8:e75597. doi:10.1371/journal.pone.0075597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marraccini P, Freire LP, Alves GS, Vieira NG, Vinecky F, Elbelt S, Ramos HJ, Montagnon C, Vieira LG, Leroy T, Pot D, Silva VA, Rodrigues GC, Andrade AC (2011) RBCS1 expression in coffee: Coffea orthologs, Coffea arabica homeologs, and expression variability between genotypes and under drought stress. BMC Plant Biol 11:85. doi:10.1186/1471-2229-11-85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLoughlin F, Galvan-Ampudia CS, Julkowska MM, Caarls L, van der Does D, Lauriere C, Munnik T, Haring MA, Testerink C (2012) The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J 72:436–449. doi:10.1111/j.1365-313X.2012.05089.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minkoff BB, Stecker KE, Sussman MR (2015) Rapid phosphoproteomic effects of abscisic acid (ABA) on wild-type and ABA receptor-deficient A. thaliana mutants. Mol Cell Proteomics 14:1169–1182. doi:10.1074/mcp.M114.043307

    Article  CAS  PubMed  Google Scholar 

  • Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363. doi:10.1093/pcp/pcp083

    Article  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York

    Book  Google Scholar 

  • Parker J, Koh J, Yoo MJ, Zhu N, Feole M, Yi S, Chen S (2013) Quantitative proteomics of tomato defense against Pseudomonas syringae infection. Proteomics 13:1934–1946. doi:10.1002/pmic.201200402

    Article  CAS  PubMed  Google Scholar 

  • Parkin IA, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, Denoeud F, Belcram H, Links MG, Just J, Clarke C, Bender T, Huebert T, Mason AS, Pires JC, Barker G, Moore J, Walley PG, Manoli S, Batley J, Edwards D, Nelson MN, Wang X, Paterson AH, King G, Bancroft I, Chalhoub B, Sharpe AG (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15:R77. doi:10.1186/gb-2014-15-6-r77

    Article  PubMed  PubMed Central  Google Scholar 

  • Romero P, Lafuente MT, Rodrigo MJ (2012) The Citrus ABA signalosome: identification and transcriptional regulation during sweet orange fruit ripening and leaf dehydration. J Exp Bot 63:4931–4945. doi:10.1093/jxb/ers168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saha J, Chatterjee C, Sengupta A, Gupta K, Gupta B (2014) Genome-wide analysis and evolutionary study of sucrose non-fermenting 1-related protein kinase 2 (SnRK2) gene family members in Arabidopsis and Oryza. Comput Biol Chem 49:59–70. doi:10.1016/j.compbiolchem.2013.09.005

    Article  CAS  PubMed  Google Scholar 

  • Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC’s of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11:535–542. doi:10.1016/j.tplants.2006.09.002

    Article  CAS  PubMed  Google Scholar 

  • Shao Y, Qin Y, Zou Y, Ma F (2014) Genome-wide identification and expression profiling of the SnRK2 gene family in Malus prunifolia. Gene 552:87–97. doi:10.1016/j.gene.2014.09.017

    Article  CAS  PubMed  Google Scholar 

  • Shi K, Li X, Zhang H, Zhang G, Liu Y, Zhou Y, Xia X, Chen Z, Yu J (2015) Guard cell hydrogen peroxide and nitric oxide mediate elevated CO2-induced stomatal movement in tomato. New Phytol 208:342–353. doi:10.1111/nph.13621

    Article  CAS  PubMed  Google Scholar 

  • Sirichandra C, Davanture M, Turk BE, Zivy M, Valot B, Leung J, Merlot S (2010) The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS ONE 5:e13935. doi:10.1371/journal.pone.0013935

    Article  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309. doi:10.1016/j.tplants.2007.05.001

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2: Unit 2 3 doi:10.1002/0471250953.bi0203s00

  • Tian S, Mao X, Zhang H, Chen S, Zhai C, Yang S, Jing R (2013) Cloning and characterization of TaSnRK2.3, a novel SnRK2 gene in common wheat. J Exp Bot 64:2063–2080. doi:10.1093/jxb/ert072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • U N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7:389–452

    Google Scholar 

  • Umezawa T, Sugiyama N, Takahashi F, Anderson JC, Ishihama Y, Peck SC, Shinozaki K (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Sci Signal 6: rs8 doi:10.1126/scisignal.2003509

  • Verkest A, Byzova M, Martens C, Willems P, Verwulgen T, Slabbinck B, Rombaut D, Van de Velde J, Vandepoele K, Standaert E, Peeters M, Van Lijsebettens M, Van Breusegem F, De Block M (2015) Selection for improved energy use efficiency and drought tolerance in canola results in distinct transcriptome and epigenome changes. Plant Physiol 168:1338–1350. doi:10.1104/pp.15.00155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vilela B, Moreno-Cortes A, Rabissi A, Leung J, Pages M, Lumbreras V (2013) The maize OST1 kinase homolog phosphorylates and regulates the maize SNAC1-type transcription factor. PLoS ONE 8:e58105. doi:10.1371/journal.pone.0058105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang RS, Pandey S, Li S, Gookin TE, Zhao Z, Albert R, Assmann SM (2011a) Common and unique elements of the ABA-regulated transcriptome of arabidopsis guard cells. BMC Genom 12:216. doi:10.1186/1471-2164-12-216

    Article  CAS  Google Scholar 

  • Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IA, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y et al (2011b) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039. doi:10.1038/ng.919

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Yuan F, Hao H, Zhang Y, Zhao H, Guo A, Hu J, Zhou X, Xie CG (2013a) BolOST1, an ortholog of Open Stomata 1 with alternative splicing products in Brassica oleracea, positively modulates drought responses in plants. Biochem Biophys Res Commun 442:214–220. doi:10.1016/j.bbrc.2013.11.032

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Xue L, Batelli G, Lee S, Hou YJ, Van Oosten MJ, Zhang H, Tao WA, Zhu JK (2013b) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci U S A 110:11205–11210. doi:10.1073/pnas.1308974110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Hu W, Sun J, Liang X, Yang X, Wei S, Wang X, Zhou Y, Xiao Q, Yang G, He G (2015a) Genome-wide analysis of SnRK gene family in Brachypodium distachyon and functional characterization of BdSnRK2.9. Plant Sci 237:33–45. doi:10.1016/j.plantsci.2015.05.008

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015b) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A 112:613–618. doi:10.1073/pnas.1423481112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C, Zhao L, Zhang H, Yang Z, Wang H, Wen S, Zhang C, Rustgi S, von Wettstein D, Liu B (2014) Evolution of physiological responses to salt stress in hexaploid wheat. Proc Natl Acad Sci USA 111:11882–11887. doi:10.1073/pnas.1412839111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281:5310–5318. doi:10.1074/jbc.M509820200

    Article  CAS  PubMed  Google Scholar 

  • Zhu M, Dai S, McClung S, Yan X, Chen S (2009) Functional differentiation of Brassica napus guard cells and mesophyll cells revealed by comparative proteomics. Mol Cell Proteomics 8:752–766. doi:10.1074/mcp.M800343-MCP200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu M, Simons B, Zhu N, Oppenheimer DG, Chen S (2010) Analysis of abscisic acid responsive proteins in Brassica napus guard cells by multiplexed isobaric tagging. J Proteomics 73:790–805. doi:10.1016/j.jprot.2009.11.002

    Article  CAS  PubMed  Google Scholar 

  • Zhu M, Zhu N, Song WY, Harmon AC, Assmann SM, Chen S (2014) Thiol-based redox proteins in abscisic acid and methyl jasmonate signaling in Brassica napus guard cells. Plant J 78:491–515. doi:10.1111/tpj.12490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We acknowledge Dr. Jin Koh at Interdisciplinary Center for Biotechnology Research University of Florida for reanalyzing the proteomic data of Zhu et al. (2010). This work is supported by funding from the US National Science Foundation (MCB 1412547) to S Chen and A Harmon.

Authors’ contributions

M-JY and SC conceived and designed the experiments; M-JY, NJ, and LL performed the experiments; M-JY and TM analyzed the data; M-JY, ACH, and SC wrote the manuscript; QW participated in revision of the manuscript. All authors read and approved the final submission.

Author information

Authors and Affiliations

  1. Department of Biology, Genetics Institute, University of Florida, Gainesville, FL, 32610, USA

    Mi-Jeong Yoo, Tianyi Ma, Ning Zhu, Lihong Liu, Alice C. Harmon & Sixue Chen

  2. College of Life Sciences, Northeast Forestry University, Harbin, 150040, China

    Tianyi Ma

  3. Key Laboratory of Horticultural Plant Growth, Development and Quality Improvement, Ministry of Agriculture, Department of Horticulture, Zhejiang University, Hangzhou, 310058, China

    Lihong Liu & Qiaomei Wang

  4. Plant Molecular and Cellular Biology, University of Florida, Gainesville, FL, 32611, USA

    Alice C. Harmon & Sixue Chen

  5. Proteomics and Mass Spectrometry, Interdisciplinary Center for Biotechnology Research, University of Florida, Gainesville, FL, 32610, USA

    Sixue Chen

Authors
  1. Mi-Jeong Yoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tianyi Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ning Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lihong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alice C. Harmon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qiaomei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sixue Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sixue Chen.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 831 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yoo, MJ., Ma, T., Zhu, N. et al. Genome-wide identification and homeolog-specific expression analysis of the SnRK2 genes in Brassica napus guard cells. Plant Mol Biol 91, 211–227 (2016). https://doi.org/10.1007/s11103-016-0456-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-016-0456-9

Keywords

Search

Navigation