In silico prediction of cold responsive genes in canola by comparative genomics using Arabidopsis thaliana

Document Type : Research Paper

Authors

1 Ph.D. Candidate of Plant Biotechnology, Faculty of Agriculture, University of Guilan, Rasht, Iran.

2 Professor, Department of Plant Biotechnology, Faculty of Agriculture, University of Guilan, Rasht, Iran.

3 Assistant Professor, Department of Plant Biotechnology, Faculty of Agriculture, University of Guilan, Rasht, Iran.

4 Assistant Professor, Department of Cell and Molecular Biology, Faculty of Biological Sciences and Biotechnology, Shahid Beheshti University, Tehran, Iran.

Abstract

Low temperature is an important abiotic stress limiting the production and geographical dispersion of many crops, including rapeseed, as an important oil crop. In this study, known cis-elements regulating molecular responses of plant to cold stress were used to identify genes involved in cold tolerance. From 62,384 Unigenes from Brassica Genome Gateway, 56 cold responsive genes were identified. Promoter analysis, gene ontology enrichment, co-occurrence, protein- protein interaction and in silico gene expression analysis were performed to validate the results of gene identification. The results showed known cis-element appearance in promoter region of all identified genes which involved in different biological pathways such as Calvin cycle, respiration and signal transduction in different cell parts. Co-occurrence study of identified genes illustrated mutual connections of genes with correlations above 0.64. Promoter analysis, PPI network and investigating transcription factors involved in transcription regulation of 56 identified genes and 98 co-expressed genes indicated the molecular mechanisms and similar pathways of plant response to cold and introduce candidate genes to be used in breeding and genetic engineering programs.

Keywords

Main Subjects

References

Agarwal P, Reddy MK, Spoty, K (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant. Cell. Rep. 25: 1263-1274.
Ali Q, Ahsan M, Waseem M, Nadeem T, Muhammad H, Elahi M, Farooq J (2011) Gene expression and functional genomic approach for abiotic stress tolerance in different crop species. IJAVMS.2:221-248.
Andaya VC, Mackill DJ (2003) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J. Exp. Bot. 54: 2579-2585.
Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant. J. 36(5):652-63.
Breton G, Danyluk J, Frenette Charron J, Sarha, F (2003) Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and Arabidopsis. Plant. Physiol. 132: 64-74.
Bohnert HJ, Cushman JC (2002) Plants and environmental stress adaptation strategies in: Plant Biotechnology and Transgenic Plants. NewYork: Marcel Dekker.635-664.
Cao S, Ye M,  Jiang S (2005) Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant. Cell. Rep. 24:683-690.
Capel J, Jarillo JA, Salinas J, Maritnez- Zapater JM (1997) Two homologous low- temperature- inducible genes from Arabidopsis encode highly hydrophobic proteins. Plant. Physiol. 115: 569-576.
Chandra A, Tyagi, A (2006) Isolation of stress responsive Psb A gene from rice (Oryza sativa L.) using differential display. IJBB. 43: 244-246.
Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell. 15: 1833-1845.
Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M. Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes. Dev. 17(8): 1043-1054.
Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends. Plant. Sci. 12: 444-451.
Chow CN, Zheng HQ, Wu NY, Chien CH, Huang HD, Lee TY, Chiang-Hsieh YF, Hou PF, Yang TY, Chang WC (2015) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic. Acids. Res.1, 10-35.
Chu B, Peter Snustad D, Carter JV (1993) Alteration of P-Tubulin Gene Expression during Low-Temperature Exposure in Leaves of Arabidopsis thaliana. Plant. Physiol. 103: 371-377.
Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong, K (2007) Overexpression of a R1R2R3 MYB Gene, OsMYB3R-2, Increased tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant. Physiol. 143: 1-13.
Davuluri RV, Sun H, Palaniswamy SK, Matthews N, Molina C, Kurtz M, Grotewold E (2003) AGRIS: Arabidopsis Gene Regulatory Information Server an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC. Bioinformatic. 4:25.
Delk NA, Johnson KA, Chowdhury NI, Braam J (2005) CML24, regulated in Expression by Diverse Stimuli, Encodes a Potential Ca21 Sensor That Functions in Responses to Abscisic Acid, Daylength, and Ion Stress. Plant. Physiol. 139: 240-253.
Dong MA, Farre EM, Thomashow MF (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108:7241-7246.
Drea SC, Lao NT, Wolfe KH, Kavanagh T (2006) Gene duplication, exon gain and neofunctionalization of OEP16-related genes in land plants. Plant. J. 46: 723-735.
Du C, Hu K, Xian S, Liu C, Fan J, Tu J, Fu T (2016) Dynamic transcriptome analysis reveals AP2/ERF transcription factors responsible for cold stress in rapeseed (Brassica napus L.). Mol Genet Genomics. 291(3): 1053-67.
Engel N, Ewald R, Gupta KJ, Zrenner R, Hagemann M,  Bauwe H (2011) The pre-sequence of Arabidopsis serine hydroxymethyltransferase SHM2 selectively prevents import into mesophyll mitochondria. Plant. Physiol. 157: 1711-1720.
Furuya T, Matsuoka D, Nanmori, T (2013) Phosphorylation of Arabidopsis thaliana MEKK1 via Ca(2+) signaling as a part of the cold stress response. J. Plant.  Res. 126(6):833-40. doi: 10.1007/s10265-013-0576-0.
Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder W, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant. J.  47(5):720-34. DOI:10.1111/j.1365-313X.2006.02821.x
Gomez-Merino FC, Brearley CA, Ornatowska M, Abdel-Haliem ME, Zanor MI, Mueller-Roeber (2004) AtDGK2, a novel diacylglycerol kinase from Arabidopsis thaliana, phosphorylates 1-stearoyl-2-arachidonoyl-sn-glycerol and 1,2-dioleoyl-sn-glycerol and exhibits cold-inducible gene expression. B. J. Biol. Chem. 279:8230-8241.
Hieno A, Naznin HA, Hyakumachi M, Sakurai T, Tokizawa M, Koyama H, Sato N, Nishiyama T, Hasebe M, Zimmer AD, Lang D, Reski R, Rensing SA, Obokata J, Yamamoto YY (2014) ppdb: plant promoter database version 3.0. Nucleic. Acids. Res. 42, 1188-92.
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucl. Acids. Res. 27(1): 297-300.
Hossain MA, Chob JI, Han M, Ahn CH, Jeon JS, An G, Park PB (2010) The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J. Plant Phys.
Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann, P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv.  Bioinformatic.
Ishitani M, Xiong L, Lee H, Stevenson B, Zhu JK (1998) HOS1, a Genetic Locus Involved in Cold-Responsive Gene Expression in Arabidopsis. Plant Cell. 10: 1151-1161.
Jing M, Meng-Yao L, Wang F, Tang J, Xiong AS (2015) Genome-wide analysis of Dof family transcription factors and their responses to abiotic stresses in Chinese cabbage. BMC. Genomics. 16(1): 33. doi:10.1186/s12864-015-1242-9.
Jiang C, Iu B, Singh J (1996) Requirement of a CCGAC cis-acting element for cold induction of the BN115 gene from winter Brassica napus. J. Plant. Mol. Biol. 30: 679- 684.
Kanehisa Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic. Acids. Res. 45, D353-D361.
Karlson D. Imai, R (2003) Conservation of the Cold Shock Domain Protein Family in Plants1. Plant Physiol. 131: 12-15.
Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant. J. 36: 141-154.
Kaur G, Pati PK (2016) Analysis of cis-acting regulatory elements of Respiratory burst oxidase homolog (Rboh) gene families in Arabidopsis and rice provides clues for their diverse functions. Comput Bio and Chem. 62: 104-18.
Kim JY, Park SJ, Jang B, Jung CH, Ahn SJ, Goh CH, Cho K, Han O, Kang H (2007) Functional characterization of a glycine-rich RNA-binding protein 2 in Arabidopsis thaliana under abiotic stress conditions. Plant. J. 50: 439-451.
Kim MH, Sasaki K, Imai RJ (2009) Cold shock domain protein 3 regulates freezing tolerance in Arabidopsis thaliana .Biol. Chem. 284: 23454-23460.
Kim JS, Kim KA, Oh TR, Park CM, Kang H (2008) Functional characterization of DEAD-box RNA helicases in Arabidopsis thaliana under abiotic stress conditions. Plant. Cell. Physiol. 49(10): 1563-71. doi: 10.1093/pcp/pcn125.
Kim YO, Kim JS, Kang H (2005) Cold-inducible zinc finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis thaliana. Plant. J. 42: 890-900.
Kimura M, Yamamoto YY, Seki M, Sakurai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K, Matsui, M (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem. Photobiol. 77(2): 226-33.
Knight H, Mugford SG, Ulker B, Gao D, Thorlby G, Knight MR (2009) Identification of SFR6, a key component in cold acclimation acting post-translationally on CBF function. Plant. J. 58: 97-108.
Kurkela S, Franck M (1990) Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant. Mol.  Biol. 15(1): 137-44.
Kwak KJ, Kim YO, Kang H (2005) Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J. Exp. Bot. 56: 421. 3007-3016. doi:10.1093/jxb/eri298.
Liang C, Zong, H, Ren, F, Gue, QQ, Hu XP, Li XB (2011) A novel cold-regulated gene, COR25, of Brassica napus is involved in plant response and tolerance to cold stress. Plant. Cell. Rep. 30: 463-471.
Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondria complex I defect impairs cold-regulated nuclear gene expression. Plant. Cell. 14: 1235-1251.
Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and regulation by ICE1. Plant Cell. 17:3155-3175.
Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002) LOS2, a genetic locus rewuierd for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J. 11: 2692-2702.
Lee BH, Kapoor A, Zhu J, Zhu JK (2006) Stabilized1, a Stress-Upregulated Nuclear Protein, Is Required for Pre-mRNA Splicing, mRNA Turnover, and Stress Tolerance in Arabidopsis. Plant Cell. 18: 1736-1749.
Lee JH, Kim JJ, Kim SH, Cho HJ, Kim J, Ahn JH (2012) The E3 ubiquitin ligase HOS1 regulates low ambient temperature responsive flowering in Arabidopsis thaliana. Plant. Cell. Physiol. 53(10): 1802-14. doi: 10.1093/pcp/pcs123.
Lescot M, Dhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y (2002) PlantCARE a database of plant cis -acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic. Acids. Res. 30(1): 325-327.
Liorente F, Lopez-Cobollo RM, Catala R, Martinez-Zapater JM, Salinas J (2002) A novel cold-inducible gene from Arabidopsis, RCI3, encodes a peroxidase that constitutes a component for stress tolerance. Plant J. 32(1): 13-24. 
Malia A, Donga B, Eva M, Farréb, M, Thomashow F (2011) Circadian Clock-Associated 1 and Late Elongated Hypocotyl regulate expression of the C-REPEAT binding factor (CBF) pathway in Arabidopsis. PNAS. 7241-7246
Messing SAJ, Gabelli SB, Echeverria I, Vogel JT, Guan JC, Tan BC, Klee HJ, McCarty DR, Amzel LM (2010) Structural insights into maize Viviparous14, a key enzyme in the biosynthesis of the phytohormone abscisic acid. Plant Cell. 22: 2970-2980.
Mizoguchi T, Iriet K, Hirayama T, Hayashida N, Yamaguchi-shinozaki K, Matsumoto K, Shinozaki K (1996) A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activate protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Plant. Biol. 93: 765-769.
Mizoguchi T, Hayashida N, Yamaguchi-Shinozaki K, Kamada H, Shinozaki K (1995) Two genes that encode ribosomal-protein S6 kinase homologs are induced by cold or salinity stress in Arabidopsis thaliana. FEBS. Lett. 23: 358(2): 199-204.
Nordin K, Vahala T, Pavala ET (1993) Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant. Mol. Bio. 21: 641-653.
Obara K, Sumi K, Fukuda H (2002) The use of multiple transcription starts causes the dual targeting of Arabidopsis putative monodehydroascorbate reductase to both mitochondria and chloroplasts. Plant. Cell. Physiol. 43:697-705.
Obayashi T, Aoki Y, Tadaka S, Kagaya Y, Kinoshita K (2018) ATTED-II in 2018: A plant co-expression database based on investigation of statistical property of the mutual rank index. Plant. Cell. Physiol. 59, e3.
Okawa K, Nakayama K, Kakizaki T, Yamashita T, Inaba T (2008) Identification and characterization of Cor413im proteins as novel components of the chloroplast inner envelope. Plant. Cell. Environ. (10):1470-1483. doi: 10.1111/j.1365-3040.2008.01854.x.
Omez- erino FC, Brearly CA, Oranatowska M, Abdel-Haliem ME, Zanor MI, Mueller-Roeber B (2004) AtDGK2, a novel diacylglycerol kinase from Arabidopsis thaliana, phosphorylates 1-stearoyl-2- arachidonoyl-sn-glycerol and 1,2-dioleoyl-sn-glycerol and exhibits cold- inducible gene expression. J. Biol. Chem. 279: 8230-8241.
Orvar BL, V. Sangwan F, Omann R, Dhindsa S (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J. 23: 785-794.
Partridge M, Murphy DJ (2009) . Roles of a membrane-bound caleosin and putative peroxygenase in biotic and abiotic stress responses in Arabidopsis. Biochem. 47: 796-806.
Prasad TK, Anderson MD, Martin BA, Stewart CR (1994) Evidence for chilling-induced oxidative stress in maize seedlings and a regulatory role for hydrogen peroxide. Plant Cell. 6: 65-74.
Puhakainen T, Hess MW, Mäkelä P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant. Mol. Biol. 54(5): 743-53.
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol. 14(3): 290-295.
Raman K (2010) Construction and analysis of protein-protein interaction networks. Autom. Express. 2(1): 2.
Roy S (2016) Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant. Signal. Behav. 11(1): e1117723.
Reye JL, Campos F, Wei H, Arora R, Yang Y, Karlson DT, Covarrubias AA (2008) Functional dissection of hydrophilins during in vitro freeze protection. Plant. Cell. Environ. 31(12):1781-90. doi: 10.1111/j.1365-3040.2008.01879.x.
Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nature. 459: 1071-1078.
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowskin B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13(11): 2498-2504.
Liu S, Snowdon R, Chalhoub B. 2018. The Brassica napus Genome. Springer. ISBN 978-3-319-43694-4.
Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, Mering C (2017) The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic. Acids. Res. 45: 362-368.
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant. J. 29: 417-426.
Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell. 15: 141-152.
Ujjal J, Phukan G, Jeena S, Rakesh K, Shukla (2016) WRKY Transcription Factors: Molecular Regulation and Stress Responses in Plants. Front. Plant. Sci. 7: 7603. doi:  10.3389/fpls.2016.00760
Vergnolle C, Vaultier M, Taconnat, L, Renou JP, Kader JC, Zachowski A, Ruelland E (2005) The Cold-Induced Early Activation of Phospholipase C and D Pathways Determines the Response of Two Distinct Clusters of Genes in Arabidopsis Cell Suspensions. Plant. Physiol. 139: 1217-1233.
Wang YJ, Zhang ZG, He XJ, Zhou HL, Wen YX, Dai JX, Zhang JS, Chen SY (2003) A rice transcription factor OsbHLH1 is involved in cold stress response. Theor. Appl. Genet. 107(8): 1402-1409.
Wittkopp PJ, Kalay G (2012) cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 13: 59-69.
Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes vernalization insensetive 3. Proc. Natl. Acad. Sci. U.S.A. 103: 14631-14636.
Xin Z, Browse J (1998) eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Plant. Biol. 95: 7799-7804.
Yamaguchi-Shinozaki K, Shinozaki, K (2005) Organization of cis -acting regulatory elements in osmotic- and cold stress-responsive promoters. Trends. Plant. Sci. 10: 88-94.
Yano R, Nakamura M, Yoneyama T, Nishida I (2005) Starch-Related a-Glucan/Water Dikinase Is Involved in the Cold-Induced Development of Freezing Tolerance in Arabidopsis. Plant. Physiol. 138: 837-846.
Yang J, Wan XL, Zhang JW, Bao MZ (2016) Identification and expression analysis of nuclear factor Y families in Prunus mume under different abiotic stresses. Biologia Plantarum. 60: 419-426.
Yu SM, Chin-Fen S, Wang YC, Hsieh TH, Lu CA, Tseng TH (2010) A Novel MYBS3-Dependent pathway confers cold tolerance in Rice. Plant. Phys. 153: 145-158.
Yuan Q, Zhang C, Zhao T, Yao M, Xu X (2016) A genome-wide analysis of GATA transcription factor family in tomato and analysis of expression patterns. Int. J. Agric. Biol. 00: 000-000.
Yo K, Kim SJ, Kang H (2005) Cold-inducible zing finger-containing glycine-rich RNA-binding protein contributes to the enhancement of freezing tolerance in Arabidopsis Thaliana. Plant J. 42(6): 890-900.
Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu JK, Hasegawa PM, Bohnert HJ, Shi H, Yun DJ, Bressan RA (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc. Natl. Accad. Sci. U.S.A. 105: 4945-4950.
Zhu J, Verslues PE, Zheng X, Lee BH, Zhan X, Manabe Y, Sokolchik I, Zhu Y, Dong CH, Zhu JK, Hasegawa PM, Bressan RA (2010) Retraction for Zhu et al., HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc. Natl. Acad. Sci. U.S.A. 107: 13972-13972.
Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O (2008) Sorting Signals, N-Terminal Modifications and Abundance of the Chloroplast.  Proteome. PLoS ONE. 3(4): e1994. doi:10.1371/journal.pone.0001994.
Crop Biotechnology
Volume 8, Issue 2 - Serial Number 24
December 2018
Pages 29-46

Files

Share

How to cite

Statistics