Genome-wide investigation of SnRK2 gene family in two jute species: Corchorus olitorius and Corchorus capsularis

Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR et al (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132:666–680 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 Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147:15–27 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 Boneh U, Biton I, Schwartz A, Ben-Ari G (2012) Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant Sci 187:89–96 Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M et al (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 Wang P, Xue L, Batelli G, Lee S, Hou YJ, Van Oosten MJ, Zhang H, Tao WA, Zhu JK (2013) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci USA 110:11205–11210 Yoshida T, Fujita Y, Maruyama K, Mogami J, Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ 38:35–49 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 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 Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K et al (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 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 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 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 Boudsocq M, Droillard MJ, Barbier-Brygoo H, Lauriere C (2007) Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol Biol 63:491–503 Li L-B, Zhang Y-R, Liu K-C, Ni Z-F, Fang Z-J, Sun Q-X, Gao J-W (2010) Identification and Bioinformatics Analysis of SnRK2 and CIPK Family Genes in Sorghum. Agri Sci China 9:19–30 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 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 Liu JY, Chen NN, Cheng ZM, Xiong JS (2016) Genome-wide identification, annotation and expression profile analysis of SnRK2 gene family in grapevine. Aust J Grape Wine Res 22:478–488 Guo D, Li H-L, Zhu J-H, Wang Y, An F, Xie G-S, Peng S-Q (2017) Genome-wide identification, characterization, and expression analysis of SnRK2 family in Hevea brasiliensis. Tree Genet Genomes 13:86 Li C, Nong Q, Xie J, Wang Z, Liang Q, Solanki MK, Malviya MK, Liu X, Li Y, Htun R et al (2017) Molecular characterization and co-expression analysis of the SnRK2 gene family in sugarcane (Saccharum officinarum L.). Sci Rep 7:17659 Wu Z, Cheng J, Hu F, Qin C, Xu X, Hu K (2020) The SnRK2 family in pepper (Capsicum annuum L.): genome-wide identification and expression analyses during fruit development and under abiotic stress. Genes Genom 42:1117–1130 Wu G-Q, Liu Z-X, Xie L-L, Wang J-L (2021) Genome-wide identification and expression analysis of the BvSnRK2 genes family in sugar beet (Beta vulgaris L.) under salt conditions. J Plant Growth Regul 40:519–532 Liu Z, Ge X, Yang Z, Zhang C, Zhao G, Chen E, Liu J, Zhang X, Li F (2017) Genome-wide identification and characterization of SnRK2 gene family in cotton (Gossypium hirsutum L.). BMC Genet 18:54 Fujii H, Verslues PE, Zhu J-K (2011) Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc Natl Acad Sci USA 108:1717–1722 Diedhiou CJ, Popova OV, Dietz KJ, Golldack D (2008) The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol 8:49 Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:17306–17311 Zheng Z, Xu X, Crosley RA, Greenwalt SA, Sun Y, Blakeslee B, Wang L, Ni W, Sopko MS, Yao C et al (2010) The protein kinase SnRK2.6 mediates the regulation of sucrose metabolism and plant growth in Arabidopsis. Plant Physiol 153:99–113 Mao X, Zhang H, Tian S, Chang X, Jing R (2010) TaSnRK2.4, an SNF1-type serine/threonine protein kinase of wheat (Triticum aestivum L.), confers enhanced multistress tolerance in Arabidopsis. J Exp Bot 61:683–696 Zhang H, Mao X, Jing R, Chang X, Xie H (2011) Characterization of a common wheat (Triticum aestivum L.) TaSnRK2.7 gene involved in abiotic stress responses. J Exp Bot 62:975–988 Zhang H, Mao X, Wang C, Jing R (2010) Overexpression of a common wheat gene TaSnRK2.8 enhances tolerance to drought, salt and low temperature in Arabidopsis. PloS one 5:e16041 Phan TT, Sun B, Niu JQ, Tan QL, Li J, Yang LT, Li YR (2016) Overexpression of sugarcane gene SoSnRK2.1 confers drought tolerance in transgenic tobacco. Plant Cell Rep 35:1891–1905 Piattoni CV, Bustos DM, Guerrero SA, Iglesias AA (2011) Nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase is phosphorylated in wheat endosperm at serine-404 by an SNF1-related protein kinase allosterically inhibited by ribose-5-phosphate. Plant Physiol 156:1337–1350 Belda-Palaz贸n B, Adamo M, Valerio C, Ferreira LJ, Confraria A, Reis-Barata D, Rodrigues A, Meyer C, Rodriguez PL, Baena-Gonz谩lez E (2020) A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nature plants 6:1345–1353 Bulletin-2014, S (2014) Food and Agriculture Organization of the United Nations. SA, USA Islam MS, Saito JA, Emdad EM, Ahmed B, Islam MM, Halim A, Hossen QM, Hossain MZ, Ahmed R, Hossain MS et al (2017) Comparative genomics of two jute species and insight into fibre biogenesis. Nat Plants 3:16223 Yang Z, Dai Z, Lu R, Wu B, Tang Q, Xu Y, Cheng C, Su J (2017) Transcriptome analysis of two species of jute in response to polyethylene glycol (PEG)- induced drought stress. Sci Rep 7:16565 Yang Z, Lu R, Dai Z, Yan A, Tang Q, Cheng C, Xu Y, Yang W, Su J (2017) Salt-stress response mechanisms using de novo transcriptome sequencing of salt-tolerant and sensitive Corchorus spp. Genotypes. Genes 8:226 Yang Z, Yan A, Lu R, Dai Z, Tang Q, Cheng C, Xu Y, Su J (2017) De novo transcriptome sequencing of two cultivated jute species under salinity stress. PLoS ONE 12:e0185863 Singh AK (2017) The potential of jute crop for mitigation of greenhouse gas emission in the changing climatic scenario. J Agric Sci 13:419–423 Naik M, Barman D, Maruthi RT, Babu V, Mandal U, Kundu D (2019) Assessment of salinity tolerance based upon morpho-physiological attributes in white jute (Corchorus capsularis L.). J Environ Biol 40:377–383 Yumnam S, Sawarkar A, Mukherjee S (2018) Response to water stress on some seedling characters of tossa jute (Corchorus olitorius L.) Dhar P, Ojha D, Kar C, Mitra J (2018) Differential response of tossa jute (Corchorus olitorius) submitted to water deficit stress. Ind Crops Prod 112:141–150 Prodhan AK, Rahman ML, Haque MA (2001) Effect of water stresses on growth attributes in jute II. Plant Base Diameter. Pak J Biol Sci. 4:660–4 Prodhan AK, Rahman ML, Haque MA (2001) Effect of water stresses on growth attributes in jute I plant height. Pak J Biol Sci 4:128–35 Hamzah Saleem M, Rahman M, Ihsan M, Xiang W, Lijun L, Imran M (2020) Morphological changes and antioxidative capacity of jute (Corchorus capsularis, Malvaceae) under diferent color light? Emitting diodes. Braz J Bot 42:590 Larnyo A, Atitsogbui P (2020) Effect of temperature treatments on seed germination and seedling growth of jute mallow (Corchorus olitorius). Int J Environ Agri Biotechnol 5:1631–1640 Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410 Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279-285 Kumar M, Thammannagowda S, Bulone V, Chiang V, Han KH, Joshi CP, Mansfield SD, Mellerowicz E, Sundberg B, Teeri T et al (2009) An update on the nomenclature for the cellulose synthase genes in Populus. Trends Plant Sci 14:248–254 Delmer DP (1999) Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev Plant Physiol Plant Mol Biol 50:245–276 Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 Jin G, Nakhleh L, Snir S, Tuller T (2006) Maximum likelihood of phylogenetic networks. Bioinformatics 22:2604–2611 Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874 Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539 Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320-324 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 Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-208 Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112:531–52. https://doi.org/10.1385/1-59259-584-7:531. Chou KC, Shen HB (2010) Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE 5:e11335 Gotz S, Arnold R, Sebastian-Leon P, Martin-Rodriguez S, Tischler P, Jehl MA, Dopazo J, Rattei T, Conesa A (2011) B2G-FAR, a species-centered GO annotation repository. Bioinformatics 27:919–924 Rombauts S, Dehais P, Van Montagu M, Rouze P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27:295–296 Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300 Neupane S, Schweitzer SE, Neupane A (2019) Identification and characterization of mitogen-activated protein kinase (MAPK) genes in sunflower (Helianthus annuus L.). p 8 Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36 Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578 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 Shin R, Alvarez S, Burch AY, Jez JM, Schachtman DP (2007) Phosphoproteomic identification of targets of the Arabidopsis sucrose nonfermenting-like kinase SnRK2.8 reveals a connection to metabolic processes. Proc Natl Acad Sci USA 104:6460–6465 Zhao W, Cheng YH, Zhang C, Shen XJ, You QB, Guo W, Li X, Song XJ, Zhou XA, Jiao YQ (2017) Genome-wide identification and characterization of the GmSnRK2 family in soybean. Int J Mol Sci 18:1834 Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839 Zhu C, Schraut D, Hartung W, Schaffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981 Li W, Cui X, Meng Z, Huang X, Xie Q, Wu H, Jin H, Zhang D, Liang W (2012) Transcriptional regulation of Arabidopsis MIR168a and argonaute1 homeostasis in abscisic acid and abiotic stress responses. Plant Physiol 158:1279–1292 Creelman RA, Mullet JE (1997) BIOSYNTHESIS AND ACTION OF JASMONATES IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol 48:355–381 Pieterse CM, van Wees SC, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580 Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153-164 Browse J, Howe GA (2008) New weapons and a rapid response against insect attack. Plant Physiol 146:832–838 Wang Y, Liu G-J, Yan X-F, Wei Z-G, Xu Z-R (2011) MeJA-inducible expression of the heterologous JAZ2 promoter from Arabidopsis in Populus trichocarpa protoplasts. J Plant Dis Prot 118:69–74 Fujii H, Zhu JK (2012) Osmotic stress signaling via protein kinases. Cell Mol Life Sci 69:3165–3173 Yoo MJ, Ma T, Zhu N, Liu L, Harmon AC, Wang Q, Chen S (2016) Genome-wide identification and homeolog-specific expression analysis of the SnRK2 genes in Brassica napus guard cells. Plant Mol Biol 91:211–227 Mikolajczyk M, Awotunde OS, Muszynska G, Klessig DF, Dobrowolska G (2000) Osmotic stress induces rapid activation of a salicylic acid-induced protein kinase and a homolog of protein kinase ASK1 in tobacco cells. Plant Cell 12:165–178 Vlad F, Rubio S, Rodrigues A, Sirichandra C, Belin C, Robert N, Leung J, Rodriguez PL, Lauriere C, Merlot S (2009) Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. Plant Cell 21:3170–3184 Ng LM, Soon FF, Zhou XE, West GM, Kovach A, Suino-Powell KM, Chalmers MJ, Li J, Yong EL, Zhu JK et al (2011) Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc Natl Acad Sci USA 108:21259–21264 Mizoguchi M, Umezawa T, Nakashima K, Kidokoro S, Takasaki H, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2010) Two closely related subclass II SnRK2 protein kinases cooperatively regulate drought-inducible gene expression. Plant Cell Physiol 51:842–847 Xue T, Wang D, Zhang S, Ehlting J, Ni F, Jakab S, Zheng C, Zhong Y (2008) Genome-wide and expression analysis of protein phosphatase 2C in rice and Arabidopsis. BMC Genomics 9:550 Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353 Rieping M, Schoffl F (1992) Synergistic effect of upstream sequences, CCAAT box elements, and HSE sequences for enhanced expression of chimaeric heat shock genes in transgenic tobacco. Mol Gen Genet MGG 231:226–232 Rahman K, Ahmed N, Raihan MR, Nowroz F, Jannat F, Rahman M, Hasanuzzaman M (2021) Jute responses and tolerance to abiotic stress: mechanisms and approaches. Plants 10:1595