Abstract
Wide adoption of direct-seeded rice practices has been hindered by poorly leveled fields, heavy rainfall and poor drainage, which cause accumulation of water in the fields shortly after sowing, leading to poor crop establishment. This is due to the inability of most rice varieties to germinate and reach the water surface under complete submergence. Hence, tolerance of anaerobic conditions during germination is an essential trait for direct-seeded rice cultivation in both rainfed and irrigated ecosystems. A QTL study was conducted to unravel the genetic basis of tolerance of anaerobic conditions during germination using a population derived from a cross between IR42, a susceptible variety, and Ma-Zhan Red, a tolerant landrace from China. Phenotypic data was collected based on the survival rates of the seedlings at 21 days after sowing of dry seeds under 10 cm of water. QTL analysis of the mapping population consisting of 175 F2:3 families genotyped with 118 SSR markers identified six significant QTLs on chromosomes 2, 5, 6, and 7, and in all cases the tolerant alleles were contributed by Ma-Zhan Red. The largest QTL on chromosome 7, having a LOD score of 14.5 and an R 2 of 31.7 %, was confirmed using a BC2F3 population. The QTLs detected in this study provide promising targets for further genetic characterization and for use in marker-assisted selection to rapidly develop varieties with improved tolerance to anaerobic condition during germination. Ultimately, this trait can be combined with other abiotic stress tolerance QTLs to provide resilient varieties for direct-seeded systems.
Similar content being viewed by others
References
Angaji SA, Septiningsih EM, Mackill DJ, Ismail AM (2010) QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.). Euphytica 172:159–168
Bailey-Serres J, Chang R (2005) Sensing and signaling in response to oxygen deprivation in plants and other organisms. Ann Bot 96:507–518
Biswas JK, Yamauchi M (1997) Mechanism of seedling establishment of direct-seeded rice (Oryza sativa L.) under lowland conditions. Bot Bull Acad Sin 38:29–32
Cai HW, Morishima H (2002) QTL clusters reflect character associations in wild and cultivated rice. Theor Appl Genet 100:840–846
Chang TT (1991) Findings from a 28-year seed viability experiment. Int Rice Res Newsl 16:5–6
Chauhan BS (2012) Weed ecology and weed management strategies for dry-seeded rice in Asia. Weed Technol 26:1–13
Dong Y, Kamiuten H, Yang Z, Lin D, Ogawa T, Luo L, Matsuo H (2006) Mapping of quantitative trait loci for gibberelic acid response at rice (Oryza sativa L.) seedling stage. Plant Sci 170:12–17
Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia Ann Rev Plant Physiol. Mol Biol 48:223–250
Ella ES, Dionisio-Sese ML, Ismail AM (2010) Proper management improves seedling survival and growth during early flooding in contrasting rice genotypes. Crop Sci 50:1997–2008
Ella ES, Dionisio-Sese ML, Ismail AM (2011) Seed pretreatment in rice reduces damage, enhances carbohydrate mobilization and improves emergence and seedling establishment under flooded conditions. AoB-PLANTS 2011 plr007 doi:10.1093/aobpla/plr007
Ellis RHT, Hong TD, Roberts EH (1992) The low moisture-content limit to the negative logarithmic relation between seed longevity and moisture content in three subspecies of rice. Ann Bot 69:53–58
Gu X-Y, Kianian SF, Foley ME (2004) Multiple loci and epistases control genetic variation for seed dormancy in weedy rice (Oryza sativa). Genetics 166:1503–1516
Gu X-Y, Kianian SF, Hareland GA, Hoffer BL, Foley ME (2005) Genetic analysis of adaptive syndromes interrelated with seed dormancy in weedy rice (Oryza sativa). Theor Appl Genet 110:1108–1118
Gu X-Y, Liu T, Feng J, Suttle JC, Gibbons J (2010) The qSD12 underlying gene promotes abscisic acid accumulation in early developing seeds to induce primary dormancy in rice. Plant Mol Biol 73:97–104
Han L, Qiao Y, Zhang S, Zhang Y, Cao G, Kim J, Lee K, Koh H (2007) Identification of quantitative trait loci for cold response of seedling vigor traits in rice. J Genet Genomics 34:239–246
Hoffmann-Benning S, Kende H (1992) On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol 99:1156–1161
Horton RF (1991) The effect of ethylene and other regulators on coleoptile growth of rice under anoxia. Plant Sci 79:57–62
Hwang YS, Thomas BR, Rodriguez RL (1999) Differential expression of rice α-amylase genes during seedling development under anoxia. Plant Mol Bio 40:911–920
Ikehashi H (1973) Studies on the environmental and varietal differences of germination habits in rice seeds with special reference to plant breeding (in Japanese with English summary). Kordan 744J Cent Agric Exp Stan 19:1–60
Ismail AM, Ella ES, Vergara GV, Mackill DJ (2009) Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann Bot 103:197–209
Ismail AM, Johnson DE, Ella ES, Vergara GV, Baltazar AM (2012) Adaptation to flooding during emergence and seedling growth in rice and weeds, and implications for crop establishment. AoB-PLANTS 2012: pls019 doi:10.1093/aobpla/pls019
Iwata N, Shinada H, Kiuchi H, Sato T, Fujino K (2010) Mapping of QTLs controlling seedling establishment using a direct seeding method in rice. Breed Sci 60:353–360
Jiang L, Hou M, Wang C, Wan J (2004) Quantitative trait loci and epistatic analysis of seed anoxia germinability in rice (Oryza sativa L.). Rice Sci 11:238–244
Jiang L, Liu S, Hou M, Tang J, Chen L, Zhai H, Wan J (2006) Analysis of QTLs for seed low temperature germinability and anoxia germinability in rice (Oryza sativa L.). Field Crops Res 98:68–75
Konchan S, Kono Y (1996) Spread of direct seeded lowland rice in Northeast Thailand: farmers’ adaptation to economic growth. Southeast Asian Stud 33:523–546
Kordan HA (1974) Patterns of shoot and root growth in rice seedlings germinating under water. J Appl Ecol 11:685–690
Lin SY, Sasaki T, Yano M (1998) Mapping quantitative trait loci controlling seed dormancy and heading date in rice, Oryza sativa L., using backcross inbred lines. Theor Appl Genet 96:997–1003
Loreti E, Yamaguchi J, Alpi A, Perata P (2003) Sugar modulation of α-amylase genes under anoxia. Ann Bot 91:143–148
Lu X-L, Niu A-L, Cai H-Y, Zhao Y, Liu J-W, Zhu Y-G, Zhang Z-H (2007) Genetics dissection of seedling and early vigor in a recombinant inbred line population of rice. Plant Sci 172:212–220
Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932
Matsumura H, Takano T, Takeda G, Uchimiya H (1998) Adh1 is transcriptionally active but its translational product is reduced in a rad mutant of rice (Oryza sativa L.), which is vulnerable to submergence stress. Theor Appl Genet 97:1197–1203
McCouch SR (2008) Gene nomenclature system for rice. Rice 1:72–84
McCouch SR, Sweeney M, Li J, Jiang H, Thomson M, Septiningsih E, Edwards J, Moncada P, Xiao J, Garris A, Tai T, Martinez C, Tohme J, Sugiono M, McClung A, Yuan LP, Ahn SN (2007) Through the genetic bottleneck: O. rufipogon as a source of trait-enhancing alleles for O. sativa. Euphytica 154:317–339
McDonald MB (1999) Seed deterioration: physiology, repair and assessment. Seed Sci Technol 27:177–237
Miura K, Lin SY, Yano M, Nagamine T (2002) Mapping quantitative trait loci controlling seed longevity in rice (Oryza sativa L.). Theor Appl Genet 104:981–986
Nelson JC (1997) QGene software for marker-based genomic analysis and breeding. Mol Breed 3:239–245
Pandey S, Velasco L (2002) Economics of direct seeding in Asia: patterns of adoption and research priorities. In: Pandey S, Mortimer M, Wade L, Lopez K, Hardy B (eds) Direct seeding: research strategies and opportunities, pp 3-8
Perata P, Guglielminetti L, Alpi A (1997) Mobilization of endosperm reserves in cereal seeds under anoxia. Ann Bot 79:49–56
Ram PC, Singh BB, Singh AK, Ram P, Singh PN, Singh HP, Boamfa I, Harren F, Reuss J, Jackson MB, Settler TL, Wade LJ, Singh VP (2002) Physiological basis of submergence tolerance in rainfed lowland rice: prospects of germplasm improvement through marker aided breeding. Field Crops Res 76:131–152
Ricard B, Mocquot B, Fournier A, Delseny M, Pradet A (1986) Expression of alcohol dehydrogenase in rice embryos under anoxia. Plant Mo1 Biol 7:321–329
Saika H, Matsumura H, Takano T, Tsutsumi N, Nakazono M (2006) A point mutation of Adh1 gene is involved in the repression of coleoptiles elongation under submergence in rice. Breed Sci 56:69–74
Sasahara T, Ikarashi H, Kambayashi M (1986) Genetic variations in embryo and endosperm weights, seedling growth parameters and α-amylase activity of the germinated grains in rice (Oryza sativa L.). Jpn J Breed 36:248–261
Sasaki K, Fukuta Y, Sato T (2005) Mapping of quantitative trait loci controlling seed longevity of rice (Oryza sativa L.) after various periods of seed storage. Pl Breed 124:361–366
Septiningsih EM, Prasetiyono J, Lubis E, Tai TH, Tjubaryat T, Moeljopawiro S, McCouch SR (2003) Identification of quantitative trait loci for yield and yield components in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon. Theor Appl Genet 107:1419–1432
Septiningsih EM, Pamplona AM, Sanchez DL, Neeraja CN, Vergara GV, Heuer S, Ismail AM, Mackill DJ (2009) Development of Submergence Tolerant Rice Cultivars: the Sub1 Locus and Beyond. Annals Bot 103:151–160
Septiningsih EM, Collard BCY, Heuer S, Bailey-Serres J, Ismail AM, Mackill DJ (2012a) Applying genomics tools for breeding submergence tolerance in rice. In: Varshney RK, Tuberosa R (eds) Genomics applications in plant breeding: Improvement for abiotic stresses. Wiley-Blackwell, USA, In press
Septiningsih EM, Sanchez DL, Singh N, Sendon PMD, Pamplona AM, Heuer S, Mackill DJ (2012b) Identifying novel QTLs for submergence tolerance in rice cultivars IR72 and Madabaru. Theor Appl Genet 124:867–874
Shingaki-Wells RN, Huang S, Taylor NL, Carroll AJ, Zhou W, Millar AH (2011) Differential molecular responses of rice and wheat coleoptiles to anoxia reveal novel metabolic adaptations in amino acid metabolism for tissue tolerance. Plant Physiol 156:1706–1724
Siddique SB, Seshu DV, Pardee WD (1988) Rice cultivar variability for accelerated aging of seed. In: IRRI research paper series 131, International Rice Research Institute, Manila, Philippines, p 1-7
Thomson MJ, Tai TH, McClung AM, Hinga ME, Lobos KB, Xu Y, Martinez C, McCouch SR (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
Thomson MJ, Edwards JD, Septiningsih EM, Harrington SE, McCouch SR (2006) Substitution mapping of dth1.1, a flowering time quantitative trait locus (QTL) associated with transgressive variation in rice, reveals multiple sub-QTL. Genetics 172:2501–2514
Tuong TP, Pablico PP, Yamauchi M, Confensor R, Moody K (2000) Increasing water productivity and weed suppression of wet-seeded rice: effect of water management and rice genotypes. Exp Agric 36:71–89
Wang S, Basten CJ, and Zeng Z-B (2010) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
Williams JF, Peterson ML (1973) Relation between alpha-amylase activity and growth of rice seedlings. Crop Sci 13:612–614
Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708
Yamauchi M, Winn T (1996) Rice seed vigor and seedling establishment in anaerobic soil. Crop Sci 36:680–686
Yamauchi M, Aguilar AM, Vaughan DA, Seshu DV (1993) Rice (Oryza sativa L.) germplasm suitable for direct sowing under soil surface. Euphytica 67:177–184
Yang J, Zhu J (2005) Methods for predicting superior genotypes under multiple environments based on QTL effects. Theor Appl Genet 110:1268–1274
Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536
Yang J, Hu CC, Hu H, Yu RD, Xia Z, Ye XZ, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24:721–723
Zhang Z-H, Qu X-S, Wan S, Chen L-H, Zhu Y-G (2005a) Comparison of QTL controlling seedling vigor under different temperature conditions using recombinant inbred lines in Rice (Oryza sativa). Ann Bot 95:423–429
Zhang Z-H, Yu S-B, Yu T, Huang Z, Zhu Y-G (2005b) Mapping quantitative trait loci (QTLs) for seedling vigor using recombinant inbred lines of rice (Oryza sativa). Field Crop Res 91:161–170
Zheng K, Subudhi PK, Domingo J, Magpantay G, Huang N (1995) Rapid DNA isolation for marker assisted selection in rice breeding. Rice Genet Newsl 12:255–258
Acknowledgments
The technical assistance of R. Garcia, J. Mendoza., E. Suiton, and A. M. Pamplona is gratefully acknowledged. The work reported here was supported in part by a grant from the Bill and Melinda Gates Foundation (BMGF) through the project “Stress-Tolerant Rice for Africa and South Asia (STRASA)”, by the German Federal Ministry for Economic Cooperation and Development (BMZ), and by the Global Rice Science Partnership (GRiSP).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Y. Xu.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Septiningsih, E.M., Ignacio, J.C.I., Sendon, P.M.D. et al. QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theor Appl Genet 126, 1357–1366 (2013). https://doi.org/10.1007/s00122-013-2057-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-013-2057-1