Cold stress causes various injuries to rice seedlings in low-temperature and high-altitude areas and is therefore an important factor affecting rice production in such areas. In this study, root conductivity (RC) was used as an indicator to map quantitative trait loci (QTLs) of cold tolerance in Oryza rufipogon Griff., Dongxiang wild rice (DX), at its two-leaf stage. The correlation coefficients between RC and the plant survival rate (PSR) at the seedling and maturity stages were –0.85 and –0.9 (P = 0.01), respectively, indicating that RC is a reliable index for evaluating cold tolerance of rice. A preliminary mapping group was constructed from 151 BC2F1 plants using DX as a cold-tolerant donor and the indica variety Nanjing 11 (NJ) as a recurrent parent. A total of 113 codominant simple-sequence repeat (SSR) markers were developed, with a parental polymorphism of 17.3%. Two cold-tolerant QTLs, named qRC10-1 and qRC10-2 were detected on chromosome 10 by composite interval mapping. qRC10-1 (LOD = 3.1, RM171-RM1108) was mapped at 148.3 cM, and qRC10-2 (LOD = 6.1, RM25570-RM304) was mapped at 163.3 cM, which accounted for 9.4% and 32.1% of phenotypic variances, respectively. To fine map the major locus qRC10-2, NJ was crossed with a BC4F2 plant (L188-3), which only carried the QTL qRC10-2, to construct a large BC5F2 fine-mapping population with 13,324 progenies. Forty-five molecular markers were designed to evenly cover qRC10-2, and 10 markers showed polymorphisms between DX and NJ. As a result, qRC10-2 was delimited to a 48.5-kb region between markers qc45 and qc48. In this region, Os10g0489500 and Os10g0490100 exhibited different expression patterns between DX and NJ. Our results provide a basis for identifying the gene(s) underlying qRC10-2, and the markers developed here may be used to improve low-temperature tolerance of rice seedling and maturity stages via marker-assisted selection (MAS). Key Message With root electrical conductivity used as a cold-tolerance index, the quantitative trait locus qRC10-2 was fine mapped to a 48.5-kb candidate region, and Os10g0489500 and Os10g0490100 were identified as differently expressed genes for qRC10-2.
References
[1]
Maclean JL, Dawe DC, Hardy B, Hettel GP (2002) Rice Almanac: source book for the most important economic activity on earth. In. 3rd edn. Int. Rice Res. Inst., pp6–8.
[2]
Nakagahra M, Okuno K, Vaughan D (1997) Rice genetic resources: history, conservation, investigative characterization and use in Japan. Plant Mol Biol 35 (1–2): 69–77 doi:10.1023/A:1005784431759.
[3]
Kuroki M, Saito K, Matsuba S, Yokogami N, Shimizu H, et al. (2007) A quantitative trait locus for cold tolerance at the booting stage on rice chromosome 8. Theor Appl Genet 115 (5): 593–600 doi:10.1007/s00122-007-0589-y.
[4]
Jiang L, Xun M, Wang J, Wan J (2008) QTL analysis of cold tolerance at seedling stage in rice (Oryza sativa L.) using recombination inbred lines. Journal of Cereal Science 48 (1): 173–179 doi:10.1016/j.jcs.2007.08.013.
[5]
Suh JP, Jeung JU, Lee JI, Choi YH, Yea JD, et al. (2010) Identification and analysis of QTLs controlling cold tolerance at the reproductive stage and validation of effective QTLs in cold-tolerant genotypes of rice (Oryza sativa L.). Theor Appl Genet 120 (5): 985–995 doi:10.1007/s00122-009-1226-8.
[6]
Saito K, Miura K, Nagano K, Hayano-Saito Y, Araki H, et al. (2001) Identification of two closely linked quantitative trait loci for cold tolerance on chromosome 4 of rice and their association with anther length. Theor Appl Genet 103 (6–7): 862–868 doi:10.1007/s001220100661.
[7]
Saito K, Hayano-Saito Y, Maruyama-Funatsuki W, Sato Y, et al. (2004) Physical mapping and putative candidate gene identification of a quantitative trait locus Ctb1 for cold tolerance at the booting stage of rice. Theor Appl Genet 109 (3): 515–522 doi:10.1007/s00122-004-1667-z.
[8]
Saito K, Hayano-Saito Y, Kuroki M, Sato Y (2010) Map-based cloning of the rice cold tolerance gene Ctb1. Plant science 179 (1): 97–102 doi:10.1016/j.plantsci.2010.04.004.
[9]
Zhou L, Zeng Y, Zheng W, Tang B, Yang S, et al. (2010) Fine mapping a QTL qCTB7 for cold tolerance at the booting stage on rice chromosome 7 using a near-isogenic line. Theor Appl Genet 121 (5): 895–905 doi:10.1007/s00122-010-1358-x.
[10]
Shirasawa S, Endo T, Nakagomi K, Yamaguchi M, Nishio T (2012) Delimitation of a QTL region controlling cold tolerance at booting stage of a cultivar, ‘Lijiangxintuanheigu’, in rice, Oryza sativa L. Theor Appl Genet 124. (5): 937–946 doi:10.1007/s00122-011-1758-6.
[11]
Dai L, Lin X, Ye C, Ise K, Saito K, et al. (2004) Identification of quantitative trait loci controlling cold tolerance at the reproductive stage in Yunnan landrace of rice, Kunmingxiaobaigu. Breeding Science 54 (3): 253–258 doi:10.1270/jsbbs.54.253.
[12]
Qian Q, Zeng D, He P, Zheng X, Chen Y, et al. (2000) QTL analysis of the rice seedling cold tolerance in a double haploid population derived from anther culture of a hybrid between indica and japonica rice. Chin Sci Bull 45 (5): 448–453 doi:10.1007/bf02884949.
[13]
Miura K, Lin SY, Yano M, Nagamine T (2001) Mapping quantitative trait loci controlling low temperature germinability in rice (Oryza sativa L.). Breeding Science 51 (4): 293–299 doi:10.1270/jsbbs.51.293.
[14]
Teng S, Zeng D, Qian Q, Kunihifo Y, Huang D, et al. (2001) QTL analysis of rice low temperature germinability. Chin Sci Bull 46 (21): 1800–1803 doi:10.1007/bf02900554.
[15]
Andaya VC, Thomas HT (2007) Fine mapping of the qCTS4 locus associated with seedling cold tolerance in rice (Oryza sativa L.). Mol Breeding 20 (4): 349–358 doi:10.1007/s11032-007-9096-8.
[16]
Ji SL, Jiang L, Wang YH, Zhang WW, Liu X, et al. (2009) Quantitative trait loci mapping and stability for low temperature germination ability of rice. Plant Breeding 128 (4): 387–392 doi:10.1111/j.1439-0523.2008.01533.x.
[17]
Koseki M, Kitazawa N, Yonebayashi S, Maehara Y, Wang ZX, et al. (2010) Identification and fine mapping of a major quantitative trait locus originating from wild rice, controlling cold tolerance at the seedling stage. Mol Genet Genomics 284 (1): 45–54 doi:10.1007/s00438-010-0548-1.
[18]
Suh JP, Lee CK, Lee JH, Kim JJ, Kim SM, et al. (2012) Identification of quantitative trait loci for seedling cold tolerance using RILs derived from a cross between japonica and tropical japonica rice cultivars. Euphytica 184 (1): 101–108 doi:10.1007/s10681-011-0575-y.
[19]
Andaya VC, Tai TH (2006) Fine mapping of the qCTS12 locus, a major QTL for seedling cold tolerance in rice. Theor Appl Genet 113 (3): 467–475 doi:10.1007/s00122-006-0311-5.
[20]
Cai W, Morishima H (2002) QTL clusters reflect character associations in wild and cultivated rice. Theor Appl Genet 104 (8): 1217–1228 doi:10.1007/s00122-001-0819-7.
[21]
Zhang ZH, Su L, Li W, Chen W, Zhu YG (2005) A major QTL conferring cold tolerance at the early seedling stage using recombinant inbred lines of rice (Oryza sativa L.). Plant Science 168 (2): 527–534 doi:10.1016/j.plantsci.2004.09.021.
[22]
Lou Q, Chen L, Sun Z, Xing Y, Li J, et al. (2007) A major QTL associated with cold tolerance at seedling stage in rice (Oryza sativa L.). Euphytica 158 (1–2): 87–94 doi:10.1007/s10681-007-9431-5.
[23]
Jiang L, Liu SJ, Hou MY, Tang JY, Chen LM, et al. (2006) Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.). Field Crops Research 98(1): 68–75 doi:10.1016/j.fcr.2005.12.015.
[24]
Wang ZF, Wang FH, Zhou R, Wang JF, Zhang HS (2011) Identification of quantitative trait loci for cold tolerance during the germination and seedling stages in rice (Oryza sativa L.). Euphytica 183 (3): 405–413 doi:10.1007/s10681-011-0469-z.
[25]
Saruyama H, Tanida M (1995) Effect of chilling on activated oxygen-scavenging enzymes in low temperature-sensitive and -tolerant cultivars of rice (Oryza sativa L.). Plant Science 109 (2): 105–113 doi:10.1016/0168-9452(95)04156-O.
[26]
Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi S, Tasaka Y, et al. (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356 (6371): 710–713 doi:10.1038/356710a0.
[27]
Murata N, Wada H (1995) Acyl-lipid desaturases and their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308 (Pt 1): 1–8.
[28]
Saltveit ME (2001) Chilling injury is reduced in cucumber and rice seedlings and in tomato pericarp discs by heat-shocks applied after chilling. Postharvest Biology and Technology 21 (2): 169–177 doi:10.1016/S0925-5214(00)00132-0.
[29]
Yu J, Zhang L, Cui H, Zhang YX, Cang J, et al. (2008) Physiological and biochemical characteristics of Dongnongdongmai 1 before wintering in high-cold area. Acta Agronomica Sinica 34 (11): 2019–2025 doi:10.3724/SP.J.1006.2008.02019.
[30]
Tian F, Zhu ZF, Fu YC, Wang XK, Sun CQ (2006) Construction of introgression lines carrying wild rice (Oryza rufipogon Griff.) segments in cultivated rice (Oryza sativa L.) background and characterization of introgressed segments associated with yield-related traits. Theor Appl Genet 112 (3): 570–580. doi: 10.1007/s00122-005-0165-2
[31]
Li F, Guo S, Zhao Y, Chen D, Chong K, et al. (2010) Overexpression of a homopeptide repeat-containing bHLH protein gene (OrbHLH001) from Dongxiang Wild Rice confers freezing and salt tolerance in transgenic Arabidopsis. Plant Cell Rep 29 (9): 977–986 doi:10.1007/s00299-010-0883-z.
[32]
Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, et al. (2003) Mapping quantitative trait loci for yield, yield components, and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107: 479–493. doi: 10.1007/s00122-003-1270-8
[33]
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, et al. (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1: 174–181. doi: 10.1016/j.ygeno.2008.12.003
[34]
Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121: 185–199.
[35]
Lincoln S, Daly M, Lander ES (1992) Mapping genes controlling quantitative traits with MAPMAKER/QTL 1.1. Whitehead Institute technical report, 2nd edn. Massachusetts.
[36]
Wang S, Basten CJ, Zeng ZB (2007) Windows QTL Cartographer 2.5. Department of Statistics. North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart？.htm.
[37]
Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5 (2): 69–76 doi:10.1007/BF00020088.
[38]
Panaud O, Chen X, McCouch SR (1996) Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice (Oryza sativa L.). Mol Gen Genet 252 (5): 597–607 doi:10.1007/BF02172406.
[39]
Xiao N, Sun GL, Hong Y, Xia RX, Zhang C, et al. (2011) Cloning of genome-specific repetitive DNA sequences in wild rice (O. rufipogon Griff.), and the development of Ty3-gypsy retrotransposon-based SSAP marker for distinguishing rice (O. sativa L.) indica and japonica subspecies. Genet Resour Crop Evol 58 (8): 1177–1186 doi:10.1007/s10722-010-9651-8.
[40]
Oka HI (1988) Origin of cultivated rice. Developments in crop science, vol 14. Elsevier, Amsterdam.
[41]
Wang ZY, Second G, Tanksley SD (1992) Polymorphism and phylogenetic relationships among species in the genus Oryza as determined by analysis of nuclear RFLPs. Theor Appl Genet 83: 565–581. doi: 10.1007/bf00226900
[42]
Second G (1982) Origin of the genetic diversity of cultivated rice (Oryza spp.), study of the polymorphism scored at 40 isozyme loci. Jpn J Genet 57: 25–57. doi: 10.1266/jjg.57.25
[43]
Mao DH, Chen CY (2012) Colinearity and Similar Expression Pattern of Rice DREB1s Reveal Their Functional Conservation in the Cold-Responsive Pathway. Plos one 7(10): e47275. doi: 10.1371/journal.pone.0047275
[44]
Zhang F, Huang LY, Wang WS, Zhao XQ, Zhu LH, et al. (2012) Genome-wide gene expression profiling of introgressed indica rice alleles associated with seedling cold tolerance improvement in a japonica rice background. BMC Genomics 13 (1): 461 doi:10.1186/1471-2164-13-461.
[45]
Dai LY, Lin XH, Ye CR, Ise K, Saito K, et al. (2004) Identification of quantitative trait loci controlling cold tolerance at the reproductive stage in Yunnan landrace of rice. Breed Sci 54: 253–258. doi: 10.1270/jsbbs.54.253
[46]
Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24: 445–451. doi: 10.1146/annurev.pp.24.060173.002305
[47]
Yoshida H, Kato A (1994) Cold–induced accumulation of RNAs and cloning of cDNAs related to chilling injury in rice. Breed Sci 44, 361–365.
[48]
Lee TM, Lur HS, Chu C (1995) Abscisic acid and putrescine accumulation in chilling–tolerant rice cultivars. Crop Science 35: 502–508. doi: 10.2135/cropsci1995.0011183x003500020037x
[49]
Orvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: The role of actin cytoskeleton and membrane fluidity. Plant J. 23(6): 785–794. doi: 10.1046/j.1365-313x.2000.00845.x
[50]
Andaya VC, Mackill DJ (2003a) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. J Exp Bot 54 (392): 2579–2585 doi:10.1093/jxb/erg243.
[51]
Andaya VC, Mackill DJ (2003b) QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica x indica cross. Theor Appl Genet 106 (6): 1084–1090 doi:10.1007/s00122-002-1126-7.
[52]
Yang ZM, Huang DQ, Tang WQ, Zheng Y, Liang KJ, et al. (2013) Mapping of Quantitative Trait Loci Underlying Cold Tolerance in rice seedlings via high-throughput sequencing of pooled extremes. Plos one 8(7): e68433. doi: 10.1371/journal.pone.0068433
[53]
Liu F, Xu W, Song Q, Tan L, Liu J, et al. (2013) Microarray-assisted fine-mapping of quantitative trait loci for cold tolerance in rice. Mol Plant, 6 (3): 757–67 doi:10.1093/mp/sss161.
[54]
Barras F, Van GF, Chatterjee AK (1994) Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu Rev Phytopathol 32 (1): 201–234 doi:10.1146/annurev.py.32.090194.001221.
[55]
De LG, Cervone F, Hahn MG, Darvill A, Albersheim P (1991) Bacterial endopectate lyase: evidence that plant cell wall pH prevents tissue maceration and increases the half-life of elicitor-active oligogalacturonides. Physiol Mol Plant Pathol 39 (5): 335–344 doi:10.1016/0885-5765(91)90015-A.
[56]
Cao J (2012) The pectin lyases in Arabidopsis thaliana: evolution, selection and expression profiles. PLoS ONE 7 (10): e46944 doi:10.1371/journal.pone.0046944.
[57]
Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, et al. (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21 (11): 2692–2702 doi:10.1093/emboj/21.11.2692.
[58]
Bouton S, Leboeuf E, Mouille G, Leydecker M, Talbotec J, et al. (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. The Plant Cell 14, 2577–2590. doi: 10.1105/tpc.004259
[59]
Solecka D, Zebrowski J, Kacperska A (2008) Are pectins involved in cold acclimation and de-acclimation of winter oil-seed rape plants. Ann Bot 101 (4): 521–530.
[60]
Liu HH, Ma Y, Chen N, Guo SY, Liu HL, et al. (2013) Overexpression of stress-inducible OsBURP16, the β subunit of polygalacturonase 1, decreases pectin content and cell adhesion and increases abiotic stress sensitivity in rice. Plant Cell Environ, doi:10.1111/pce.12223.
