Heterologous expression of rice RNA-binding glycine-rich (RBG) gene OsRBGD3 in transgenic Arabidopsis thaliana confers cold stress tolerance
Sangram K. Lenka A E , Amit K. Singh A , Senthilkumar K. Muthusamy A B , Shuchi Smita A C , Viswanathan Chinnusamy D and Kailash C. Bansal A E FA ICAR-National Research Centre on Plant Biotechnology, Indian Agricultural Research Institute, New Delhi, 110012, India.
B ICAR-Central Tuber Crops Research Institute, Thiruvananthapuram, 695017, India.
C Department of Immunology, School of Medicine, University of Pittsburgh, PA 15261, USA.
D ICAR-Indian Agricultural Research Institute, Division of Plant Physiology, New Delhi, 110012, India.
E TERI-Deakin NanoBiotechnology Centre, The Energy and Resources Institute, New Delhi, 110003, India.
F Corresponding author. Email: kailashbansal@hotmail.com
Functional Plant Biology 46(5) 482-491 https://doi.org/10.1071/FP18241
Submitted: 14 September 2018 Accepted: 23 January 2019 Published: 27 February 2019
Abstract
Imparting cold stress tolerance to crops is a major challenge in subtropical agriculture. New genes conferring cold tolerance needs to be identified and characterised for sustainable crop production in low-temperature stress affected areas. Here we report functional characterisation of OsRBGD3, classified previously as a class D glycine-rich RNA recognition motif (RRM) containing proteins from a drought-tolerant Indica rice cultivar N22. The gene was isolated by screening yeast one-hybrid library using the minimal promoter region of the OsMYB38 that is necessary for cold stress-responsive expression. OsRBGD3 exhibited cold, drought and salt stress inductive expression in a drought tolerant N22 rice cultivar as compared with susceptible variety IR64. OsRBGD3 was found to be localised to both nuclear and cytoplasmic subcellular destinations. Constitutive overexpression of the OsRBGD3 in transgenic Arabidopsis conferred tolerance to cold stress. ABA sensitivity was also observed in transgenic lines suggesting the regulatory role of this gene in the ABA signalling pathway. OsRBGD3 overexpression also attributed to significant root development and early flowering in transgenics. Hence, OsRBGD3 could be an important target for developing cold tolerant early flowering rice and other crops’ genotypes for increasing production in low temperature affected areas.
Additional keywords: cold tolerance, flowering, glycine-rich RRM proteins, OsRBGD3, root growth, Y1H.
References
Ben Saad R, Halima NB, Ghorbel M, Zouari N, Romdhane WB, Guiderdoni E, Al-Doss A, Hassairi A (2018) AlSRG1, a novel gene encoding an RRM-type RNA-binding protein (RBP) from Aeluropus littoralis, confers salt and drought tolerance in transgenic tobacco. Environmental and Experimental Botany 150, 25–36.| AlSRG1, a novel gene encoding an RRM-type RNA-binding protein (RBP) from Aeluropus littoralis, confers salt and drought tolerance in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar |
Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research 42, W252–W258.
| SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information.Crossref | GoogleScholarGoogle Scholar | 24782522PubMed |
Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends in Plant Science 12, 444–451.
| Cold stress regulation of gene expression in plants.Crossref | GoogleScholarGoogle Scholar | 17855156PubMed |
Chinnusamy V, Zhu J-K, Sunkar R (2010) Gene regulation during cold stress acclimation in plants In ‘Plant stress tolerance’. pp. 39–55. (Springer: Dordrecht, The Netherlands)
Ciuzan O, Hancock J, Pamfil D, Wilson I, Ladomery M (2015) The evolutionarily conserved multifunctional glycine-rich RNA-binding proteins play key roles in development and stress adaptation. Physiologia Plantarum 153, 1–11.
| The evolutionarily conserved multifunctional glycine-rich RNA-binding proteins play key roles in development and stress adaptation.Crossref | GoogleScholarGoogle Scholar | 25243592PubMed |
Cléry A, Blatter M, Allain FH (2008) RNA recognition motifs: boring? Not quite. Current Opinion in Structural Biology 18, 290–298.
| RNA recognition motifs: boring? Not quite.Crossref | GoogleScholarGoogle Scholar | 18515081PubMed |
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
| Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 10069079PubMed |
Condit CM, Meagher RB (1986) A gene encoding a novel glycine-rich structural protein of petunia. Nature 323, 178
| A gene encoding a novel glycine-rich structural protein of petunia.Crossref | GoogleScholarGoogle Scholar |
Czolpinska M, Rurek M (2018) Plant glycine-rich proteins in stress response: an emerging, still prospective story. Frontiers of Plant Science 9, 302
| Plant glycine-rich proteins in stress response: an emerging, still prospective story.Crossref | GoogleScholarGoogle Scholar |
Daubner GM, Cléry A, Allain FH (2013) RRM–RNA recognition: NMR or crystallography… and new findings. Current Opinion in Structural Biology 23, 100–108.
| RRM–RNA recognition: NMR or crystallography… and new findings.Crossref | GoogleScholarGoogle Scholar | 23253355PubMed |
Fu ZQ, Guo M, Jeong B-r, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447, 284
| A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity.Crossref | GoogleScholarGoogle Scholar | 17450127PubMed |
Fusaro A, Mangeon A, Junqueira RM, Rocha CAB, Coutinho TC, Margis R, Sachetto-Martins G (2001) Classification, expression pattern and comparative analysis of sugarcane expressed sequences tags (ESTs) encoding glycine-rich proteins (GRPs). Genetics and Molecular Biology 24, 263–273.
| Classification, expression pattern and comparative analysis of sugarcane expressed sequences tags (ESTs) encoding glycine-rich proteins (GRPs).Crossref | GoogleScholarGoogle Scholar |
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. Advances in Bioinformatics 2008, 420747
| Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes.Crossref | GoogleScholarGoogle Scholar | 19956698PubMed |
Jena K, Kim S, Suh J, Yang C, Kim Y (2012) Identification of cold-tolerant breeding lines by quantitative trait loci associated with cold tolerance in rice. Crop Science 52, 517–523.
| Identification of cold-tolerant breeding lines by quantitative trait loci associated with cold tolerance in rice.Crossref | GoogleScholarGoogle Scholar |
Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV‐B light, drought and cold stress responses. The Plant Journal 50, 347–363.
| The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV‐B light, drought and cold stress responses.Crossref | GoogleScholarGoogle Scholar | 17376166PubMed |
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. The Plant Journal 50, 439–451.
| Functional characterization of a glycine‐rich RNA‐binding protein 2 in Arabidopsis thaliana under abiotic stress conditions.Crossref | GoogleScholarGoogle Scholar | 17376161PubMed |
Kim JS, Jung HJ, Lee HJ, Kim KA, Goh CH, Woo Y, Oh SH, Han YS, Kang H (2008) Glycine‐rich RNA‐binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. The Plant Journal 55, 455–466.
| Glycine‐rich RNA‐binding protein7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 18410480PubMed |
Kim JY, Kim WY, Kwak KJ, Oh SH, Han YS, Kang H (2010) Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process. Journal of Experimental Botany 61, 2317–2325.
| Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process.Crossref | GoogleScholarGoogle Scholar | 20231330PubMed |
Koseki M, Kitazawa N, Yonebayashi S, Maehara Y, Wang Z-X, Minobe Y (2010) Identification and fine mapping of a major quantitative trait locus originating from wild rice, controlling cold tolerance at the seedling stage. Molecular Genetics and Genomics 284, 45–54.
| Identification and fine mapping of a major quantitative trait locus originating from wild rice, controlling cold tolerance at the seedling stage.Crossref | GoogleScholarGoogle Scholar | 20526617PubMed |
Kremnev D, Strand A (2014) Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis. Frontiers of Plant Science 5, 385
| Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Krishnamurthy P, Kim JA, Jeong MJ, Kang CH, Lee SI (2015) Defining the RNA-binding glycine-rich (RBG) gene superfamily: new insights into nomenclature, phylogeny, and evolutionary trends obtained by genome-wide comparative analysis of Arabidopsis, Chinese cabbage, rice and maize genomes. Molecular Genetics and Genomics 290, 2279–2295.
| Defining the RNA-binding glycine-rich (RBG) gene superfamily: new insights into nomenclature, phylogeny, and evolutionary trends obtained by genome-wide comparative analysis of Arabidopsis, Chinese cabbage, rice and maize genomes.Crossref | GoogleScholarGoogle Scholar | 26123085PubMed |
Kumar A (2007) Characterization of abiotic stress-inducible promoters. MSc Thesis. Department of Molecular Biology and Biotechnology, Indian Agricultural Research Institute, New Delhi.
Kwak KJ, Kim YO, Kang H (2005) Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. Journal of Experimental Botany 56, 3007–3016.
| Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress.Crossref | GoogleScholarGoogle Scholar | 16207746PubMed |
Kwak KJ, Park SJ, Han JH, Kim MK, Oh SH, Han YS, Kang H (2011) Structural determinants crucial to the RNA chaperone activity of glycine-rich RNA-binding proteins 4 and 7 in Arabidopsis thaliana during the cold adaptation process. Journal of Experimental Botany 62, 4003–4011.
| Structural determinants crucial to the RNA chaperone activity of glycine-rich RNA-binding proteins 4 and 7 in Arabidopsis thaliana during the cold adaptation process.Crossref | GoogleScholarGoogle Scholar | 21511907PubMed |
Lee K, Kang H (2016) Emerging roles of RNA-binding proteins in plant growth, development, and stress responses. Molecules and Cells 39, 179
| Emerging roles of RNA-binding proteins in plant growth, development, and stress responses.Crossref | GoogleScholarGoogle Scholar | 26831454PubMed |
Lenka SK, Lohia B, Kumar A, Chinnusamy V, Bansal KC (2009) Genome-wide targeted prediction of ABA responsive genes in rice based on over-represented cis-motif in co-expressed genes. Plant Molecular Biology 69, 261–271.
| Genome-wide targeted prediction of ABA responsive genes in rice based on over-represented cis-motif in co-expressed genes.Crossref | GoogleScholarGoogle Scholar | 18998058PubMed |
Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2011) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnology Journal 9, 315–327.
| Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance.Crossref | GoogleScholarGoogle Scholar | 20809928PubMed |
Lenka SK, Muthusamy SK, Chinnusamy V, Bansal KC (2018) Ectopic expression of rice PYL3 enhances cold and drought tolerance in Arabidopsis thaliana. Molecular Biotechnology 60, 350–361.
| Ectopic expression of rice PYL3 enhances cold and drought tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 29574592PubMed |
Lewinski M, Hallmann A, Staiger D (2016) Genome-wide identification and phylogenetic analysis of plant RNA binding proteins comprising both RNA recognition motifs and contiguous glycine residues. Molecular Genetics and Genomics 291, 763–773.
| Genome-wide identification and phylogenetic analysis of plant RNA binding proteins comprising both RNA recognition motifs and contiguous glycine residues.Crossref | GoogleScholarGoogle Scholar | 26589419PubMed |
Lorković ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Research 30, 623–635.
| Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 11809873PubMed |
Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T (2011) Epigenetics in alternative pre-mRNA splicing. Cell 144, 16–26.
| Epigenetics in alternative pre-mRNA splicing.Crossref | GoogleScholarGoogle Scholar | 21215366PubMed |
Mangeon A, Junqueira RM, Sachetto-Martins G (2010) Functional diversity of the plant glycine-rich proteins superfamily. Plant Signaling & Behavior 5, 99–104.
| Functional diversity of the plant glycine-rich proteins superfamily.Crossref | GoogleScholarGoogle Scholar |
Maris C, Dominguez C, Allain FHT (2005) The RNA recognition motif, a plastic RNA‐binding platform to regulate post‐transcriptional gene expression. FEBS Journal 272, 2118–2131.
| The RNA recognition motif, a plastic RNA‐binding platform to regulate post‐transcriptional gene expression.Crossref | GoogleScholarGoogle Scholar | 15853797PubMed |
Muthusamy SK, Dalal M, Chinnusamy V, Bansal KC (2016) Differential regulation of genes coding for organelle and cytosolic ClpATPases under biotic and abiotic stresses in wheat. Frontiers of Plant Science 7, 929
| Differential regulation of genes coding for organelle and cytosolic ClpATPases under biotic and abiotic stresses in wheat.Crossref | GoogleScholarGoogle Scholar |
Nicaise V, Joe A, Jeong B, Korneli C, Boutrot F, Westedt I, Staiger D, Alfano JR, Zipfel C (2013) Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. The EMBO Journal 32, 701–712.
| Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7.Crossref | GoogleScholarGoogle Scholar | 23395902PubMed |
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiology 133, 1755–1767.
| Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses.Crossref | GoogleScholarGoogle Scholar | 14645724PubMed |
Raghuvanshi S, Gour P, Joseph SV (2016) Manually Curated Database of Rice Proteins (MCDRP), a database of digitized experimental data on rice. Current Plant Biology 7–8, 26–30.
| Manually Curated Database of Rice Proteins (MCDRP), a database of digitized experimental data on rice.Crossref | GoogleScholarGoogle Scholar |
Sachetto-Martins G, Franco LO, de Oliveira DE (2000) Plant glycine-rich proteins: a family or just proteins with a common motif? Biochimica et Biophysica Acta (BBA) – Gene Structure and Expression 1492, 1–14.
| Plant glycine-rich proteins: a family or just proteins with a common motif?Crossref | GoogleScholarGoogle Scholar |
Sato Y, Antonio BA, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Research 39, D1141–D1148.
| RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions.Crossref | GoogleScholarGoogle Scholar | 21045061PubMed |
Shaik R, Ramakrishna W (2012) Bioinformatic analysis of epigenetic and microRNA mediated regulation of drought responsive genes in rice. PLoS One 7, e49331
| Bioinformatic analysis of epigenetic and microRNA mediated regulation of drought responsive genes in rice.Crossref | GoogleScholarGoogle Scholar | 23145152PubMed |
Smita S, Katiyar A, Chinnusamy V, Pandey DM, Bansal KC (2015) Transcriptional regulatory network analysis of MYB transcription factor family genes in rice. Frontiers of Plant Science 6, 1157
| Transcriptional regulatory network analysis of MYB transcription factor family genes in rice.Crossref | GoogleScholarGoogle Scholar |
Wang B, Wang G, Shen F, Zhu S (2018) A glycine-rich RNA-binding protein, CsGR-RBP3, is involved in defense responses against cold stress in harvested cucumber (Cucumis sativus L.) fruit. Frontiers of Plant Science 9, 540
| A glycine-rich RNA-binding protein, CsGR-RBP3, is involved in defense responses against cold stress in harvested cucumber (Cucumis sativus L.) fruit.Crossref | GoogleScholarGoogle Scholar |
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets. PLoS One 2, e718
| An ‘electronic fluorescent pictograph’ browser for exploring and analyzing large-scale biological data sets.Crossref | GoogleScholarGoogle Scholar | 17684564PubMed |
Zhang Q, Chen Q, Wang S, Hong Y, Wang Z (2014) Rice and cold stress: methods for its evaluation and summary of cold tolerance-related quantitative trait loci. Rice 7, 24
| Rice and cold stress: methods for its evaluation and summary of cold tolerance-related quantitative trait loci.Crossref | GoogleScholarGoogle Scholar | 25279026PubMed |
Zhang Y, Gu L, Hou Y, Wang L, Deng X, Hang R, Chen D, Zhang X, Zhang Y, Liu C, Cao X (2015) Integrative genome-wide analysis reveals HLP1, a novel RNA-binding protein, regulates plant flowering by targeting alternative polyadenylation. Cell Research 25, 864
| Integrative genome-wide analysis reveals HLP1, a novel RNA-binding protein, regulates plant flowering by targeting alternative polyadenylation.Crossref | GoogleScholarGoogle Scholar | 26099751PubMed |
Zhu J, Dong C-H, Zhu J-K (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Current Opinion in Plant Biology 10, 290–295.
| Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation.Crossref | GoogleScholarGoogle Scholar | 17468037PubMed |