Abstract
RCD1 protein confers multiple stress tolerance to plant, while playing in it developmental roles as well. After an extensive characterization of its gene in A. thaliana, role of its orthologues under varying stresses have also been characterized in rice, wheat and tomato plants. RCD1 of A. thaliana with its rice homologue has been found consensually involved in providing plant tolerance against oxidative and osmotic stresses; however, its stress-tolerance roles under other environmental stresses seem rather contrasting. This is also the case with the expression profile, primary protein structure and binding affinities of these two homologues. Such differences in behaviours of the RCD1 homologues raises need to study their evolutionary status, in an effort to infer relative conservation of their functions. To elucidate this pattern, available RCD1 homologues have been subjected to Maximum Parsimony and Bayesian Inference-based analysis in this research. Conservation status of the SRO1/RCD1 type-specific WWE domain has also been explored using the available sequences in online databases along with the WWE-encoding sequences obtained in sugarcane, wheat and rice using single set of primers designed on conserved flanking regions. Results suggest a high conservation of these homologues within plant families, suggesting family-specific conservation of their functionalities in demonstrating stress responses.
*Electronic supplementary material. The online version of this article (DOI: 10.1515/biolog-2016-0081) contains supplementary material, which is available to authorized users.
Acknowledgements
Authors are thankful to National Agricultural Research Centre (NARC), Islamabad and INCOM Rockwool (PVT.) for providing seeds and rockwool to aid in this research.
References
Ahlfors R., Lang S., Overmyer K., Jaspers P., Brosche M., Tauriainen A., Kollist H., Tuominen H., Belles-Boix E., Piippo M., Inze D., Palva E.T. & Kangasjarvi J. 2004. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell. 16: 1925–1937.10.1105/tpc.021832Search in Google Scholar
Anjum S., Raza S., Azhar A. & Qamarunnisa S. 2015. Bnsro1: A new homologue of Arabidopsis thaliana rcd1 from Brassica napus. Biologia 70: 588–598.10.1515/biolog-2015-0073Search in Google Scholar
Aravind L. 2001. The WWE domain: a common interaction module in protein ubiquitination and ADP ribosylation. Trends Biochem. Sci. 26: 273–275.10.1016/S0968-0004(01)01787-XSearch in Google Scholar
Babajani G., Effendy J. & Plant A.L. 2009. Sl-SROl increases salt tolerance and is a member of the radical-induced cell death 1-similar to RCD1 gene family of tomato. Plant Sci. 176: 214–222.10.1016/j.plantsci.2008.10.012Search in Google Scholar
Bloomster T., Salojärvi J., Sipari N., Brosché M., Ahlfors R., Keinänen M., Overmeyer K. & Kangasjärvi J. 2011. Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol. 157: 1866–1883.10.1104/pp.111.181883Search in Google Scholar PubMed PubMed Central
Boscaiu M., Donat P., Linares J. & Vicente O. 2012. Stress-tolerant wild plants: a source of knowledge and biotechnological tools for the genetic improvement of stress tolerance in crop plants. Not. Bot. Horti. Agrobo. 40: 323–327.10.15835/nbha4028199Search in Google Scholar
Boyer J.S. 1982. Plant productivity and environment. Science 218: 443–448.10.1126/science.218.4571.443Search in Google Scholar PubMed
Corpet F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16: 10881–10890.10.1093/nar/16.22.10881Search in Google Scholar PubMed PubMed Central
Citarelli M., Teotia S. & Lamb R.S. 2010. Evolutionary history of the poly(ADP-ribose) polymerase gene family in eukaryotes. BMC Evol. Biol. 10: 308.10.1186/1471-2148-10-308Search in Google Scholar PubMed PubMed Central
D’Amours D., Desnoyers S., DaSilva I. & Poirier G. 1999. Poly (ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J. 342: 249–268.10.1042/bj3420249Search in Google Scholar
Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. ”jModel-Test 2: more models, new heuristics and parallel computing”. Nat. Methods 9: 772.10.1038/nmeth.2109Search in Google Scholar
deCastro E., Sigrist C.J., Gattiker A., Bulliard V., Langendijk-Genevaux P.S., Gasteiger E., Bairoch A. & Hulo N. 2006. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Res. 34: 362–365.10.1093/nar/gkl124Search in Google Scholar
Doyle J.J. & Doyle J.L. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11–15.Search in Google Scholar
Drummond A.J. & Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7: 214.10.1186/1471-2148-7-214Search in Google Scholar
Fujibe T., Saji H., Arakawa K., Yabe N., Takeuchi Y. & Yamamoto K.T. 2004. A methyl viologen resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol. 134: 275–285.10.1104/pp.103.033480Search in Google Scholar
Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D. & Bairoch A. 2003. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31: 3784-3788.10.1093/nar/gkg563Search in Google Scholar
Goodstein D.M., Shu S., Howson R., Neupane R., Hayes R.D., Fazo J., Mitros T., Dirks W., Hellsten U. & Putnam N. 2012. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40: 1178–1186.10.1093/nar/gkr944Search in Google Scholar
Hofmann K. & Bucher P. 1996. The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends Biochem. Sci. 21: 172–173.10.1016/S0968-0004(96)30015-7Search in Google Scholar
Jaspers P., Blomster T., Brosche M., Saloja J., Ahlfors R., Vainonen J.P., Reddy A.R., Immink R., Angenent G., Turck F., Overmyer K. & Kangasjärvi J. 2009. Unequally redundant RCD1 and SRO1 mediate stress and developmental responses and interact with transcription factors. Plant J. 60: 268–279.10.1111/j.1365-313X.2009.03951.xSearch in Google Scholar PubMed
Jaspers P., Brosché M., Overmyer K. & Kangasjärvi J. 2010a. The transcription factor interacting protein RCD1 contains a novel conserved domain. Plant Signal. Behav. 5: 78–80.10.4161/psb.5.1.10293Search in Google Scholar PubMed PubMed Central
Jaspers P., Overmyer K., Wrzaczek M., Vainonen J.P., Blomster T., Salojärvi J., Ramesha A.R. & Kangasjärvi J. 2010b. The RST and PARP-like domain containing SRO protein family: analysis of protein structure, function and conservation in land plants. BMC Genomics 11: 170.10.1186/1471-2164-11-170Search in Google Scholar PubMed PubMed Central
Julia P.V., Pinja J., Michael W., Airi L., Ramesha A.R., Vaahtera L., Brosché M. & Kangasjärvi J. 2012. RCD1-DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. Biochem. J. 442: 573–581.10.1042/BJ20111739Search in Google Scholar
Katiyar-Agarwal S., Zhu J., Kim K., Agarwal M., Fu X., Huang A. & Zhu J.K. 2006. The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl. Acad. Sci. USA 103: 18816–18821.10.1073/pnas.0604711103Search in Google Scholar
Liu S., Wang M., Wei T., Meng C., Wang M. & Xia G. 2014. A wheat SIMILAR TO RCD-ONE gene enhances seedling growth and abiotic stress resistance by modulating redox homeostasis and maintaining genomic integrity. Plant Cell. 26: 164–180.10.1105/tpc.113.118687Search in Google Scholar
Marchler-Bauer A., Anderson J.B., Cherukuri P.F., DeWeese-Scott C., Geer L.Y., Gwadz M., He S., Hurwitz D.I., Jackson J.D., Ke Z. & et al. 2005. CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res. 33: 192–196.10.1093/nar/gki069Search in Google Scholar
Overmyer K., Tuominen H., Kettunen R., Betz C., Langebartels C., Sandermann H., Kangasjärvi J. 2000. Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell. 12: 1849–1862.10.1105/tpc.12.10.1849Search in Google Scholar
Posada D. & Buckley T. 2004. Model selection and model averaging in phylognetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53: 793–808.10.1080/10635150490522304Search in Google Scholar
Pruitt K.D., Tatusova T. & Maglott D.R. 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35: 61–65.Search in Google Scholar
Punta M., Coggill P.C., Eberhardt R.Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G., Clements J., Ceric G. & Clements J. 2012. The Pfam protein families database. Nucleic Acids Res. 40: 290–301.10.1093/nar/gkr1065Search in Google Scholar
Rhee S.Y., Beavis W., Berardini T.Z., Chen G., Dixon D., Doyle A., Margarita Garcia-Hernandez M., Huala E., Lander G., Montoa M. & et al. 2003. The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res. 31: 224–228.10.1093/nar/gkg076Search in Google Scholar
Rombel I.T., Sykes K.F., Rayner S. & Johnston S.A. 2002. ORF-FINDER: a vector for high-throughput gene identification. Gene 282: 33–41.10.1016/S0378-1119(01)00819-8Search in Google Scholar
Rouard M., Guignon V., Aluome C., Laporte M.A., Droc G., Walde C., Zmasek C.M., Perin C. & Conte M.G. 2011. Green-PhylDB v2.0: comparative and functional genomics in plants. Nucleic Acids Res. 39: 1095–1102.10.1093/nar/gkq811Search in Google Scholar PubMed PubMed Central
Sievers F., Wilm A., Dineen D., Gibson T.J., Karplus K., Li W., McWilliam H., Remmert M., Söding J., Thompson J.D. & Higgins D.G. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7: 539.10.1038/msb.2011.75Search in Google Scholar PubMed PubMed Central
Sigrist C.J., de Castro E., Cerutti L., Cuche B.A., Hulo N., Bridge A., Bougueleret L. & Xenarios I. 2013. New and continuing developments at PROSITE. Nucleic Acids Res. 41: 344–347.10.1093/nar/gks1067Search in Google Scholar PubMed PubMed Central
Solcitis P.S. & Solcitis D.E. 2013. Angiosperm phylogeny: A framework for studies of genome evolution. Plant Genome Diversity Volume 2. Springer Vienna, pp. 1-11.Search in Google Scholar
Swofford D.L. 2002. PAUP*: Phylogenetic analysis using parsimony (* and other methods). Version, 4.Search in Google Scholar
Teotia S. & Lamb R.S. 2009. The paralogous genes RADICAL-INDUCED CELL DEATH1 and SIMILAR TO RCD ONE1 have partially redundant functions during Arabidopsis development. Plant Physiol. 151: 180–198.10.1104/pp.109.142786Search in Google Scholar PubMed PubMed Central
Thompson J.D., Higgins D.G. & Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.10.1093/nar/22.22.4673Search in Google Scholar PubMed PubMed Central
Untergrasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B. C., Remm M. & Rozen S.G. 2012. Primer3 – new capabilities and interfaces. Nucleic Acids Res. 40: 115.10.1093/nar/gks596Search in Google Scholar PubMed PubMed Central
You J., Zong W., Li X., Ning J., Hu H., Li X., Xiao J. & Xiong L. 2013a. The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J. Exp. Bot. 64: 569–583.10.1093/jxb/ers349Search in Google Scholar PubMed PubMed Central
You J., Zong W., Du H., Hu H. & Xiong L. 2013b. A special member of the rice SRO family, OsSRO1c, mediates responses to multiple abiotic stresses through interaction with various transcription factors. Plant Mol. Biol. 4: 693–705.10.1007/s11103-013-0163-8Search in Google Scholar PubMed
Zhu Y., Du B., Qian J., Zou B. & Hua J. 2013. Disease resistance gene-induced growth inhibition is enhanced by rcd1 independent of defense activation in Arabidopsis. Plant Physiol. 161: 2005–2013.10.1104/pp.112.213363Search in Google Scholar PubMed PubMed Central
©2016 Institute of Botany, Slovak Academy of Sciences
Articles in the same Issue
- Cellular and Molecular Biology
- Molecular detection of Mycobacterium tuberculosis complex in the 8th century skeletal remains from the territory of Slovakia
- Cellular and Molecular Biology
- First report of microorganisms of Caucasus glaciers (Georgia)
- Cellular and Molecular Biology
- Codon optimization of Aspergillus niger feruloyl esterase and its expression in Pichia pastoris
- Botany
- Response of lichens Cladonia arbuscula subsp. mitis and Cladonia furcata to nitrogen excess
- Botany
- No confirmation for previously suggested presence of diploid cytotypes of Sesleria (Poaceae) on the Balkan Peninsula
- Botany
- RCD1 homologues and their constituent WWE domain in plants: analysis of conservation through phylogeny methods
- Botany
- Nucleoli migration coupled with cytomixis
- Cellular and Molecular Biology
- Evaluation of appropriate reference gene for normalization of microRNA expression by real-time PCR in Lablab purpureus under abiotic stress conditions
- Zoology
- The fractal nature of the latitudinal biodiversity gradient
- Zoology
- A new species of Neoribates (Neoribates) (Acari: Oribatida: Parakalummidae) with key to the Neotropical species of the subgenus
- Zoology
- Diversity patterns of aquatic specialists and generalists: contrasts among two spring-fen mesohabitats and nearby streams
- Zoology
- Heteroptera (Insecta: Hemiptera) of the peat bogs of Belarusian Lakeland
- Cellular and Molecular Biology
- Cloning of monoacylglycerol o-acyltransferase 2 cDNA from a silkworm, Bombyx mori
- Zoology
- Biological aspect of the surface structure of the tongue in the adult red kangaroo (Macropus rufus) — light and scanning electron microscopy
- Zoology
- Status of the rose-ringed parakeet Psittacula krameri in Lisbon, Portugal
- Zoology
- Considerations on the vulnerability of the Eurasian water shrew Neomys fodiens to the presence of introduced brown trout Salmo trutta
Articles in the same Issue
- Cellular and Molecular Biology
- Molecular detection of Mycobacterium tuberculosis complex in the 8th century skeletal remains from the territory of Slovakia
- Cellular and Molecular Biology
- First report of microorganisms of Caucasus glaciers (Georgia)
- Cellular and Molecular Biology
- Codon optimization of Aspergillus niger feruloyl esterase and its expression in Pichia pastoris
- Botany
- Response of lichens Cladonia arbuscula subsp. mitis and Cladonia furcata to nitrogen excess
- Botany
- No confirmation for previously suggested presence of diploid cytotypes of Sesleria (Poaceae) on the Balkan Peninsula
- Botany
- RCD1 homologues and their constituent WWE domain in plants: analysis of conservation through phylogeny methods
- Botany
- Nucleoli migration coupled with cytomixis
- Cellular and Molecular Biology
- Evaluation of appropriate reference gene for normalization of microRNA expression by real-time PCR in Lablab purpureus under abiotic stress conditions
- Zoology
- The fractal nature of the latitudinal biodiversity gradient
- Zoology
- A new species of Neoribates (Neoribates) (Acari: Oribatida: Parakalummidae) with key to the Neotropical species of the subgenus
- Zoology
- Diversity patterns of aquatic specialists and generalists: contrasts among two spring-fen mesohabitats and nearby streams
- Zoology
- Heteroptera (Insecta: Hemiptera) of the peat bogs of Belarusian Lakeland
- Cellular and Molecular Biology
- Cloning of monoacylglycerol o-acyltransferase 2 cDNA from a silkworm, Bombyx mori
- Zoology
- Biological aspect of the surface structure of the tongue in the adult red kangaroo (Macropus rufus) — light and scanning electron microscopy
- Zoology
- Status of the rose-ringed parakeet Psittacula krameri in Lisbon, Portugal
- Zoology
- Considerations on the vulnerability of the Eurasian water shrew Neomys fodiens to the presence of introduced brown trout Salmo trutta