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Candidate gene markers associated with cold tolerance in vegetative stage of rice (Oryza sativa L.)

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Abstract

Low temperature inhibits seedling emergence and early vegetative growth of rice (Oryza sativa L.), especially in cultivars of the subspecies indica, which are the most productive in the temperate region of South America. To improve breeding efficiency, we identified molecular markers associated with cold response related phenotypes, such as membrane integrity, photoinhibition and visual assessment of damage. A candidate gene approach was used to select genomic simple sequence repeat (gSSR) markers. For marker-trait association two strategies were used, candidate gene association mapping (CGAM) and single marker analysis (SMA) in a segregating F2:3 population. Thirty-six gSSR were identified but only 14 were polymorphic in the CGAM population. Using this approach, we found marker RM22034 associated with membrane integrity, RM6547 and RM14978 with photoinhibition, and RM144 with visual assessment of damage. The SMA strategy identified markers RM6651, RM14978, RM22034 and RM4 associated with membrane integrity and RM22034 with photoinhibition. All markers are currently available for marker assisted selection in rice breeding programs located in temperate regions.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Andaya VC, Mackill DJ (2003) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J Exp Bot 54:2579–2585

    Article  CAS  PubMed  Google Scholar 

  • Andaya VC, Tai TH (2006) Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. Theor Appl Genet 113:467–475

    Article  CAS  PubMed  Google Scholar 

  • Andaya VC, Tai TH (2007) Fine mapping of the qCTS4 locus associated with seedling cold tolerance in rice (Oryza sativa L.). Mol Breeding 20:349–358

    Article  CAS  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet 25:25–29

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ayres NM, McClung AM, Larkin PD, Bligh HFJ, Jones CA, Park WD (1997) Microsatellites and a single-nucleotide polymorphism differentiate apparent amylose classes in an extended pedigree of US rice germplasm. Theor Appl Genet 94:773–781

    Article  CAS  Google Scholar 

  • Balzarini M, Di Rienzo J (2004) Info-Gen: software para análisis estadístico de datos genéticos. Facultad de Ciencias Agropecuarias. Universidad Nacional de Córdoba. Argentina

  • Bates D, Maechler M, Bolker B (2011) lme4: Linear Mixed-E_ects Models Using S4 Classes. R package version 0.999375-38, URL http://CRAN.R-project.org/package=lme4

  • Benjamin Y, Hochberg Y (1995) Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. J. R. Statist. Soc. B. 57:289–300 ISSN 0035–9246/95/57289

    Google Scholar 

  • Boguski MS, Lowe TM, Tolstoshev CM (1993) dbEST–database for “expressed sequence tags”. Nat Genet 4:332–333

    Article  CAS  PubMed  Google Scholar 

  • Bonnecarrere V, Borsani O, Diaz P, Capdevielle F, Blanco P, Monza J (2011) Response to photoxidative stress induced by cold in japonica rice is genotype dependent. Plant Sci 180:726–732

    Article  CAS  PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Broman KW, Wu H, Sen S, Churchill G (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890

    Article  CAS  PubMed  Google Scholar 

  • Catanho M, Mascarenhas D, Degrave W, de Miranda AB (2006) BioParser: a tool for processing of sequence similarity analysis reports. Appl Bioinformatics 5(1):49–53

    Article  PubMed  Google Scholar 

  • Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant Japónica rice. BMC Genom 8:175–193

    Article  Google Scholar 

  • Counce PA, Keisling TC, Mitchell J (2000) A uniform, objective and adaptive system for expressing rice development. Crop Sci 40:436–443

    Article  Google Scholar 

  • Cruz M (2010). Tolerancia del arroz a la temperatura baja. In: Degiovanni Beltramo, Víctor M.; Martínez Racines, César P.; Motta O., Francisco (Eds). Producción eco-eficiente del arroz en América Latina. Centro Internacional de Agricultura Tropical (CIAT), Cali. pp. 180–190. (Publicación CIAT No. 365)

  • D’hoop BB, Paulo MJ, Mank RA, van Eck HJ, Van Eeuwijk FA (2008) Association mapping of quality traits in potato (Solanum tuberosum L.). Euphytica 161:47–60

    Article  Google Scholar 

  • De los Reyes B, Morsy M, Gibbons J, Varma TSN, Antoine W, McGrath JM, Halgren R, Redus M (2003) A snapshot of the low temperature stress transcriptome of developing rice seedlings (Oryza sativa L.) via ESTs from subtracted cDNA library. Theor Appl Genet 107:1071–1082

    Article  CAS  PubMed  Google Scholar 

  • Ehrenreich IM, Hanzawa Y, Chou L, Roe JL, Kover PX, Purugganan MD (2009) Candidate gene association mapping of arabidopsis flowering time. Genetics 183:325–335

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • García AA, Kido EA, Meza AN, Souza HM, Pinto LR, Pastina MM, Leite CS, Silva JA, Ulian EC, Figueira A, Souza AP (2006) Development of an integrated genetic map of a sugarcane (Saccharum spp.) commercial cross, based on a maximum-likelihood approach for estimation of linkage and linkage phases. Theor Appl Gen 112:298–314

    Article  Google Scholar 

  • Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9:868–877

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162

    Article  CAS  PubMed  Google Scholar 

  • Jannink JL, Walsh B (2002) Association mapping in plant populations. In: Kang MS (ed) Quantitative genetics, genomics and plant breeding. CAB International, Wallingford, pp 59–68

    Google Scholar 

  • Kashi Y, King D, Soller M (1997) Simple sequence repeats as a source of quantitative genetic variation. Trends Gen 13:74–78

    Article  CAS  Google Scholar 

  • Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34

    Article  CAS  PubMed  Google Scholar 

  • Kim SI, Tai TH (2011) Evaluation of seedling cold tolerance in rice cultivars: a comparison of visual ratings and quantitative indicators of physiological changes. Euphytica 178:437–447

    Article  Google Scholar 

  • Kocsy G, Galiba G, Brunold C (2001) Role of glutathione in adaptation and signalling during chilling and cold acclimation in plants. Physiol Plantarum 113:158–164

    Article  CAS  Google Scholar 

  • Li CC, Rutger N (1980) Inheritance of cool-temperature vigor in rice and its relationship with other agronomic characters. Corp Sci 20:295–298

    Article  Google Scholar 

  • Li YC, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465

    Article  CAS  PubMed  Google Scholar 

  • Li YC, Korol AB, Fahima T, Nevo E (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21:991–1007

    Article  CAS  PubMed  Google Scholar 

  • Matthies IE, Weise S, Förster J, Röder MS (2009) Association mapping and marker development of the candidate genes (1 → 3), (1 → 4)-β-d-Glucan-4-glucanohydrolase and (1 → 4)-β-Xylan endohydrolase 1 for malting quality in barley. Euphytica 170:109–122

    Article  CAS  Google Scholar 

  • Morsy MR, Almutairia AM, Gibbonsa J, Yunb SJ, de los Reyes BG (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature. Gene 344:171–180

    Article  CAS  PubMed  Google Scholar 

  • Morsy MR, Jouve L, Hausman JF, Hoffman V, Stewart JM (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164:157–167

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Lam-Son PT, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

    Article  CAS  PubMed  Google Scholar 

  • Narasimhamoorthy B, Bouton JH, Olsen KM, Sledge MK (2007) Quantitative trait loci and candidate gene mapping of aluminum tolerance in diploid alfalfa. Theor Appl Genet 114:901–913

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pachecoy MA, Ramirez IA, Marin A, Pontaroli AC (2014) Assessment of cold tolerance at early developmental stages and allelic variation at candidate genes in South American rice germplasm. Euphytica 197:423–434

    Article  CAS  Google Scholar 

  • Pereira da Cruz R, Kothe SC (2000) Melhoramento genético para tolerância ao frio em arroz irrigado. Ciência rural 30:909–917

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotec 18:233–234

    Article  CAS  Google Scholar 

  • Shahi BB, Khush GS (1986) Genetic analysis of cold tolerance in rice. In: Proceedings International rice genetics symposium, 1., Los Baños: International Rice Research Institute, 931p, pp. 429–435

  • Sthapit BR, Witcombe JR (1998) Inheritance of tolerance to chilling stress in rice during germination and plumule greening. Crop Sci 38:660–665

    Article  Google Scholar 

  • Szalma SJ, Buckler ES IV, Snook ME, McMullen MD (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theor Appl Genet 110:1324–1333

    Article  CAS  PubMed  Google Scholar 

  • Temnykh S, Lukashova A, Cartinhour S, DeClerck G, Lipovich L, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S (1981) Fundamentals of rice crop science. International Rice Research Institute, Los Baños 269p

    Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Yun KY, Park MR, Mohanty B, Herath V, Xu F, Mauleon R, Wijaya E, Bajic VB, Bruskiewich R, de los Reyes BG (2010) Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of Japonica rice to chilling stress. BMC Plant Biol 10:16

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang P, Li J, Li X, Liu X, Zhao X, Lu Y (2011) Population structure and genetic diversity in a rice core collection (Oryza sativa L.) investigated with SSR markers. PLoS One 6:e27565

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank Dr. Ariel Castro for useful comments and suggestions for improving the manuscript; and Maribel Ceppa, Sara Murchio, Belén Bonilla, Marlene Bentancor and Daniela Deppa for their assistance with electrolyte leakage determinations. This work was supported by INIA (Instituto Nacional de Investigación Agropecuaria). The research was conducted at the Uruguayan National Agriculture Research Institute (INIA) and Latin American Fund for Irrigated Rice (FLAR).

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Authors and Affiliations

  1. Unidad de Biotecnología, Estación Experimental Wilson Ferreira Aldunate, Instituto Nacional de Investigación Agropecuaria, Ruta 48, Km 10, Rincón del Colorado, 90200, Canelones, Uruguay

    Victoria Bonnecarrère & Silvia Garaycochea

  2. Departamento de Biología Vegetal, Facultad de Agronomía, Laboratorio de Bioquímica, Av. Garzón 780, 12900, Montevideo, Uruguay

    Gastón Quero, Jorge Monza & Omar Borsani

  3. Departamento de Biología Vegetal, Facultad de Agronomía, Laboratorio de Genética, Av. Garzón 780, 12900, Montevideo, Uruguay

    Eliana Monteverde

  4. Programa de Arroz, Estación Experimental Treinta y Tres, Instituto Nacional de Investigación Agropecuaria, Ruta 8, Km 282, 33000, Treinta y Tres, Uruguay

    Juan Rosas & Fernando Pérez de Vida

  5. Fondo Latinoamericano de Arroz de Riego (FLAR), Km 7 Recta Cali, Palmira, AA6713, Cali, Valle del Cauca, Colombia

    Maribel Cruz & Edgar Corredor

Authors
  1. Victoria Bonnecarrère
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  2. Gastón Quero
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  3. Eliana Monteverde
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  4. Juan Rosas
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  5. Fernando Pérez de Vida
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  6. Maribel Cruz
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  7. Edgar Corredor
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  8. Silvia Garaycochea
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  9. Jorge Monza
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  10. Omar Borsani
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Corresponding author

Correspondence to Victoria Bonnecarrère.

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Victoria Bonnecarrère, Gastón Quero have contributed equally to this work

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Bonnecarrère, V., Quero, G., Monteverde, E. et al. Candidate gene markers associated with cold tolerance in vegetative stage of rice (Oryza sativa L.). Euphytica 203, 385–398 (2015). https://doi.org/10.1007/s10681-014-1290-2

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