Abstract
Rice (Oryza sativa L.) head-rice yield (HR) is a key export and domestic quality trait whose genetic control is poorly understood. With the goal of identifying genomic regions influencing HR, quantitative-trait-locus (QTL) mapping was carried out for quality-related traits in recombinant inbred lines (RILs) derived from crosses of common parent Cypress, a high-HR US japonica cultivar, with RT0034, a low-HR indica line (129 RILs) and LaGrue, a low-HR japonica cultivar (298 RILs), grown in two US locations in 2005–2007. Early heading increased HR in the Louisiana (LA) but not the Arkansas (AR) location. Fitting QTL-mapping models to separate QTL main and QTL × environment interaction (QEI) effects and identify epistatic interactions revealed six main-effect HR QTLs in the two crosses, at four of which Cypress contributed the increasing allele. Multi-QTL models accounted for 0.36 of genetic and 0.21 of genetic × environment interaction of HR in MY1, and corresponding proportions of 0.25 and 0.37 in MY2. The greater HR advantage of Cypress in LA than in AR corresponded to a genomewide pattern of opposition of HR-increasing QTL effects by AR-specific effects, suggesting a selection strategy for improving this cultivar for AR. Treating year–location combinations as independent environments resulted in underestimation of QEI effects, evidently owing to lower variation among years within location than between location. Identification of robust HR QTLs in elite long-grain germplasm is suggested to require more detailed attention to the interaction of plant and grain development parameters with environmental conditions than has been given to date.
Similar content being viewed by others
Abbreviations
- QTL:
-
Quantitative-trait locus
- GEI:
-
Genetic × environment interaction
- QEI:
-
QTL × environment interaction
- QQI:
-
QTL × QTL interaction
- QQEI:
-
QQI × environment interaction
- HR:
-
Head-rice yield
- RIL:
-
Recombinant inbred line
- MET:
-
Multi-environment trial
- MIM:
-
Multiple-interval mapping
References
Aluko G, Martinez C, Tohme J, Castano C, Bergman C, Oard JH (2004) QTL mapping of grain quality traits from the interspecific cross Oryza sativa x O. glaberrima. Theor Appl Genet 109:630–639
Bauer A, Hoti F, von Korff M, Pillen K, Léon J, Sillanpää M (2009) Advanced backcross-QTL analysis in spring barley (H. vulgare ssp. spontaneum) comparing a REML versus a Bayesian model in multi-environmental field trials. Theor Appl Genet 119:105–123
Boer MP, Wright D, Feng L, Podlich DW, Luo L, Cooper M, van Eeuwijk FA (2007) A mixed-model quantitative trait loci (QTL) analysis for multiple-environment trial data using environmental covariables for QTL-by-environment interactions, with an example in maize. Genetics 177:1801–1813
Carlborg Ö, Kerje S, Schütz K, Jacobsson L, Jensen P, Andersson L (2003) A global search reveals epistatic interaction between QTL for early growth in the chicken. Genome Res 13:413–421
Childs N (2006) Rice situation and outlook yearbook. United States Department of Agriculture, Economic Research Service
Cooper NTW, Siebenmorgen TJ, Counce PA (2008) Effects of nighttime temperature during kernel development on rice physicochemical properties. Cereal Chem 85:276–282
Counce PA, Bryant RJ, Bergman CJ, Bautista RC, Wang YJ, Siebenmorgen TJ, Moldenhauer KAK, Meullenet JFC (2005) Rice milling quality, grain dimensions, and starch branching as affected by high night temperatures. Cereal Chem 82:645–648
de Givry S, Bouchez M, Chabrier P, Milan D, Schiex T (2005) CarthaGene: multipopulation integrated genetic and radiation hybrid mapping. Bioinformatics 21:1703–1704
Dong YJ, Tsuzuki E, Lin DZ, Kamiunten H, Terao H, Matsuo M, Cheng SH (2004) Molecular genetic mapping of quantitative trait loci for milling quality in rice (Oryza sativa L.). J Cereal Sci 40:109–114
Dudley JW, Johnson GR (2009) Epistatic models improve prediction of performance in corn. Crop Sci 49:763–770
Fan CH, Xing YZ, Mao HL, Lu TT, Han B, Xu CG, Li XH, Zhang QF (2006) GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor Appl Genet 112:1164–1171
Fjellstrom RG, Chen M, Bergman CJ, McClung AM (2004) Single nucleotide polymorphism markers at the rice alk locus controlling alkali spreading value. In: Rice Technical Working Group Meeting. Rice Technical Working Group, New Orleans, LA, p 66
Fukuta Y, Sasahara H, Tamura K, Fukuyama T (2000) RFLP linkage map included the information of segregation distortion in a wide-cross population between indica and japonica rice (Oryza sativa L.). Breed Sci 50:65–72
Hao W, Zhu M-Z, Gao J-P, Sun S-Y, Lin H-X (2009) Identification of quantitative trait loci for rice quality in a population of chromosome segment substitution lines. J Integr Plant Biol 51:500–512
Harushima Y, Yano M, Shomura A, Sato M, Shimano T, Kuboki Y, Yamamoto T, Lin SY, Antonio BA, Parco A, Kajiya H, Huang N, Yamamoto K, Nagamura Y, Kurata N, Khush GS, Sasaki T (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148:479–494
Jiang C, Zeng Z-B (1997) Mapping quantitative trait loci with dominant and missing markers in various crosses from two inbred lines. Genetica 101:47–58
Jiang GH, Hong XY, Xu CG, Li XH, He YQ (2005) Identification of quantitative trait loci for grain appearance and milling quality using a doubled-haploid rice population. J Integr Plant Biol 47:1391–1403
Joehanes R, Nelson JC (2008) QGene 4.0, an extensible Java QTL-analysis platform. Bioinformatics 24:2788–2789
Juliano BO, Bechtel DB (1985) The rice grain and its gross composition. In: Juliano BO (ed) Rice: chemistry and technology, 2nd edn. The American Association of Cereal Chemists, St. Paul, pp 17–58
Kao C-H, Zeng Z-B, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152:1203–1216
Kepiro JL, McClung AM, Chen MH, Yeater KM, Fjellstrom RG (2007) Mapping QTLs for milling yield and grain characteristics in a tropical japonica long grain cross. J Cereal Sci 48:477–485
Kunze OR, Calderwood DL (1985) Rough rice drying. In: Juliano BO (ed) Rice: Chemistry and Technology, 2nd edn. The American Association of Cereal Chemists, St. Paul, pp 233–264
Li ZF, Wan JM, Xia JF, Zhai HQ (2003a) Mapping quantitative trait loci underlying appearance quality of rice grains (Oryza sativa L.). Acta Genet Sin 30:251–259
Li ZK, Yu SB, Lafitte HR, Huang N, Courtois B, Hittalmani S, Vijayakumar CHM, Liu GF, Wang GC, Shashidhar HE, Zhuang JY, Zheng KL, Singh VP, Sidhu JS, Srivantaneeyakul S, Khush GS (2003b) QTL × environment interactions in rice. I. Heading date and plant height. Theor Appl Genet 108:141–153
Li JM, Xiao JH, Grandillo S, Jiang LY, Wan YZ, Deng QY, Yuan LP, McCouch SR (2004) QTL detection for rice grain quality traits using an interspecific backcross population derived from cultivated Asian (O. sativa L.) and African (O. glaberrima S.) rice. Genome 47:697–704
Lin SY, Ikehashi H, Yanagihara S, Kawashima A (1992) Segregation distortion via male gametes in hybrids between indica and japonica or wide-compatibility varieties of rice (Oryza sativa L). Theor Appl Genet 84:812–818
Lin HX, Yamamoto T, Sasaki T, Yano M (2000) Characterization and detection of epistatic interactions of 3 QTLs, Hd1, Hd2, and Hd3, controlling heading date in rice using nearly isogenic lines. Theor Appl Genet 101:1021–1028
Lou J, Chen L, Yue G, Lou Q, Mei H, Xiong L, Luo L (2009) QTL mapping of grain quality traits in rice. J Cereal Sci 50:145–151
Maccaferri M, Sanguineti MC, Corneti S, Ortega JLA, Salem MB, Bort J, DeAmbrogio E, del Moral LFG, Demontis A, El-Ahmed A, Maalouf F, Machlab H, Martos V, Moragues M, Motawaj J, Nachit M, Nserallah N, Ouabbou H, Royo C, Slama A, Tuberosa R (2008) Quantitative trait loci for grain yield and adaptation of durum wheat (Triticum durum Desf.) across a wide range of water availability. Genetics 178:489–511
Malosetti M, Voltas J, Romagosa I, Ullrich SE, van Eeuwijk FA (2004) Mixed models including environmental covariables for studying QTL by environment interaction. Euphytica 137:139–145
McCouch SR, Teytelman L, Xu YB, Lobos KB, Clare K, Walton M, Fu BY, Maghirang R, Li ZK, Xing YZ, Zhang QF, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199–207
Mei H, Luo L, Guo L, Wang Y, Yu X, Ying C, Li Z (2002) Molecular mapping of QTLs for rice milling yield traits. Acta Genet Sin 29:791–797
Moldenhauer KAK, Gibbons JH, McKenzie KS (2004) Rice varieties. In: Champagne ET (ed) Rice: chemistry and technology, 3rd edn. The American Association of Cereal Chemists, St. Paul, pp 49–75
Pérez CM, Juliano BO (1978) Modification of the simplified amylose test for milled rice. Starch 30:424–426
Piepho H-P (2000) A mixed-model approach to mapping quantitative trait loci in barley on the basis of multiple environment data. Genetics 156:2043–2050
SAS Institute (2004) SAS 9.1.3 help and documentation. SAS Institute, Inc, Cary
Septiningsih EM, Trijatmiko KR, Moeljopawiro S, McCouch SR (2003) Identification of quantitative trait loci for grain quality in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O. rufipogon. Theor Appl Genet 107:1433–1441
Shimomura K, Low-Zeddies SS, King DP, Steeves TDL, Whiteley A, Kushla J, Zemenides PD, Lin A, Vitaterna MH, Churchill GA, Takahashi JS (2001) Genome-wide epistatic interaction analysis reveals complex genetic determinants of circadian behavior in mice. Genome Res 11:959–980
Siebenmorgen TJ, Meullenet JF (2004) Impact of drying, storage, and milling of rice quality and functionality. In: Champagne ET (ed) Rice: chemistry and technology, 3rd edn. The American Association of Cereal Chemists, St. Paul, pp 301–328
Stylianou I, Korstanje R, Li R, Sheehan S, Paigen B, Churchill G (2006) Quantitative trait locus analysis for obesity reveals multiple networks of interacting loci. Mamm Genome 17:22–36
Tan YF, Xing YZ, Li JX, Yu SB, Xu CG, Zhang QF (2000) Genetic bases of appearance quality of rice grains in Shanyou 63, an elite rice hybrid. Theor Appl Genet 101:823–829
Tan YF, Sun M, Xing YZ, Hua JP, Sun XL, Zhang QF, Corke H (2001) Mapping quantitative trait loci for milling quality, protein content and color characteristics of rice using a recombinant inbred line population derived from an elite rice hybrid. Theor Appl Genet 103:1037–1045
van Ruiten HTL (1985) Rice milling: an overview. In: Juliano BO (ed) Rice: chemistry and technology, 2nd edn. The American Association of Cereal Chemists, St. Paul, pp 349–388
von Korff M, Grando S, Del Greco A, This D, Baum M, Ceccarelli S (2008) Quantitative trait loci associated with adaptation to Mediterranean dryland conditions in barley. Theor Appl Genet 117:653–669
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wan XY, Wan JM, Weng JF, Jiang L, Bi JC, Wang CM, Zhai HQ (2005) Stability of QTLs for rice grain dimension and endosperm chalkiness characteristics across eight environments. Theor Appl Genet 110:1334–1346
Wang GL, Mackill DJ, Bonman JM, McCouch SR, Champoux MC, Nelson RJ (1994) RFLP mapping of genes conferring complete and partial resistance to blast in a durably resistant rice cultivar. Genetics 136:1421–1434
Wang CM, Yasui H, Yoshimura A, Wan JM, Zhai HQ (2002) Identification of quantitative trait loci controlling F2 sterility and heading date in rice. Acta Genet Sin 29:339–342
Ware DH, Jaiswal PJ, Ni JJ, Yap I, Pan XK, Clark KY, Teytelman L, Schmidt SC, Zhao W, Chang K, Cartinhour S, Stein LD, McCouch SR (2002) Gramene, a tool for grass genomics. Plant Physiol 130:1606–1613
Webb BD (1985) Criteria of rice quality in the United States. In: Juliano BO (ed) Rice: Chemistry and Technology, 2nd edn. The American Association of Cereal Chemists, St. Paul, pp 403–442
Wei WH, Knott S, Haley CS, de Koning DJ (2010) Controlling false positives in the mapping of epistatic QTL. Heredity 104:401–409
Xing YZ, Xu CG, Hua JP, Tan YF, Sun XL (2001) Mapping and isolation of quantitative trait loci controlling plant height and heading date in rice. Acta Bot Sin 43:721–726
Xing YZ, Tan YF, Hua JP, Sun XL, Xu CG, Zhang Q (2002) Characterization of the main effects, epistatic effects and their environmental interactions of QTLs on the genetic basis of yield traits in rice. Theor Appl Genet 105:248–257
Xu S, Jia Z (2007) Genomewide analysis of epistatic effects for quantitative traits in barley. Genetics 175:1955–1963
Yamamoto T, Taguchi-Shiobara F, Ukai Y, Sasaki T, Yano M (2001) Mapping quantitative trait loci for days-to-heading, and culm, panicle and internode lengths in a BC1F3 population using an elite rice variety, Koshihikari, as the recurrent parent. Breed Sci 51:63–71
Yamamoto T, Yonemaru J, Yano M (2009) Towards the understanding of complex traits in rice: substantially or superficially? DNA Res 16:141–154
Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23:1527–1536
Yano M, Harushima Y, Nagamura Y, Kurata N, Minobe Y, Sasaki T (1997) Identification of quantitative trait loci controlling heading date in rice using a high-density linkage map. Theor Appl Genet 95:1025–1032
Yoshida S, Ikegami M, Kuze J, Sawada K, Hashimoto Z, Ishii T, Nakamura C, Kamijima O (2002) QTL analysis for plant and grain characters of sake-brewing rice using a doubled haploid population. Breed Sci 52:309–317
Zhang Y-M, Gai J (2009) Methodologies for segregation analysis and QTL mapping in plants. Genetica 136:311–318
Zhao K, Wright M, Kimball J, Eizenga G, McClung A, Kovach M, Tyagi W, Ali ML, Tung CW, Reynolds A, Bustamante CD, McCouch SRP (2010) Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS One (in press)
Zheng TQ, Xu JL, Li ZK, Zhai HQ, Wan JM (2007) Genomic regions associated with milling quality and grain shape identified in a set of random introgression lines of rice (Oryza sativa L.). Plant Breed 126:158–163
Zhou L, Chen L, Jiang L, Zhang W, Liu L, Liu X, Zhao Z, Liu S, Zhang L, Wang J, Wan J (2009) Fine mapping of the grain chalkiness QTL qPGWC-7 in rice (Oryza sativa L.). Theor Appl Genet 118:581–590
Acknowledgments
We thank J. Delgado for all image analysis measurements; J. Cammack, K. Landry, C. Henry, P. Roberts, J. Bonnette, H. Hoffpauir, C. Conner, and J. Vawter for all milling determinations; N. Gipson for amylose content determinations; L. Murray for consultation on linear models; E. Christensen and S. Simpson for genotypic analysis; I. Roughton for fissuring determinations; and F.-M. Xie for providing the MY1 mapping population. Support for this work has been provided in part by US Department of Agriculture Cooperative State Research, Education and Extension Service—National Research Initiative—Applied Plant Genomics Program grant 2004-35317-14867 entitled “RiceCAP: A coordinated research, education, and extension project for the application of genomic discoveries to improve rice in the United States.” This is contribution 09-002-J from the Kansas Agriculture Experiment Station.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Q. Zhang.
Rights and permissions
About this article
Cite this article
Nelson, J.C., McClung, A.M., Fjellstrom, R.G. et al. Mapping QTL main and interaction influences on milling quality in elite US rice germplasm. Theor Appl Genet 122, 291–309 (2011). https://doi.org/10.1007/s00122-010-1445-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-010-1445-z