Genetics, Vol. 158, 1737-1753, August 2001, Copyright © 2001

Overdominant Epistatic Loci Are the Primary Genetic Basis of Inbreeding Depression and Heterosis in Rice. I. Biomass and Grain Yield

Zhi-Kang Lib,a, L. J. Luoc, H. W. Meic, D. L. Wangd, Q. Y. Shud, R. Tabienb, D. B. Zhongc, C. S. Yingc, J. W. Stanselb, G. S. Khusha, and A. H. Patersonb,e
a Plant Breeding, Genetics, and Biochemistry Division, International Rice Research Institute, Metro Manila, The Philippines,
b Department of Soil and Crop Sciences, Texas A&M University, College Station, Texas 77843,
c China National Rice Research Institute, 310006 Hangzhou, China,
d Department of Agronomy, Zhejiang Agricultural University, 310029 Hangzhou, China
e Department of Crop and Soil Sciences, University of Georgia, Athens, Georgia 30602

Corresponding author: Zhi-Kang Li, Plant Breeding, Genetics, and Biochemistry Division, International Rice Research Institute, DAPO Box 7777, Metro Manila, The Philippines., z.li{at}cgiar.org (E-mail)

Communicating editor: A. G. CLARK

To understand the genetic basis of inbreeding depression and heterosis in rice, main-effect and epistatic QTL associated with inbreeding depression and heterosis for grain yield and biomass in five related rice mapping populations were investigated using a complete RFLP linkage map of 182 markers, replicated phenotyping experiments, and the mixed model approach. The mapping populations included 254 F10 recombinant inbred lines derived from a cross between Lemont (japonica) and Teqing (indica) and two BC and two testcross hybrid populations derived from crosses between the RILs and their parents plus two testers (Zhong 413 and IR64). For both BY and GY, there was significant inbreeding depression detected in the RI population and a high level of heterosis in each of the BC and testcross hybrid populations. The mean performance of the BC or testcross hybrids was largely determined by their heterosis measurements. The hybrid breakdown (part of inbreeding depression) values of individual RILs were negatively associated with the heterosis measurements of their BC or testcross hybrids, indicating the partial genetic overlap of genes causing hybrid breakdown and heterosis in rice. A large number of epistatic QTL pairs and a few main-effect QTL were identified, which were responsible for >65% of the phenotypic variation of BY and GY in each of the populations with the former explaining a much greater portion of the variation. Two conclusions concerning the loci associated with inbreeding depression and heterosis in rice were reached from our results. First, most QTL associated with inbreeding depression and heterosis in rice appeared to be involved in epistasis. Second, most (~90%) QTL contributing to heterosis appeared to be overdominant. These observations tend to implicate epistasis and overdominance, rather than dominance, as the major genetic basis of heterosis in rice. The implications of our results in rice evolution and improvement are discussed.





This article has been cited by other articles:


Home page
GeneticsHome page
L. Li, K. Lu, Z. Chen, T. Mu, Z. Hu, and X. Li
Dominance, Overdominance and Epistasis Condition the Heterosis in Two Heterotic Rice Hybrids
Genetics, November 1, 2008; 180(3): 1725 - 1742.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. S. Escobar, A. Nicot, and P. David
The Different Sources of Variation in Inbreeding Depression, Heterosis and Outbreeding Depression in a Metapopulation of Physa acuta
Genetics, November 1, 2008; 180(3): 1593 - 1608.
[Abstract] [Full Text] [PDF]


Home page
J HeredHome page
I. Fernandez-Silva, E. Moreno, I. Eduardo, P. Arus, J. M. Alvarez, and A. J. Monforte
On the Genetic Control of Heterosis for Fruit Shape in Melon (Cucumis Melo L.)
J. Hered., September 23, 2008; (2008) esn075v1.
[Abstract] [Full Text] [PDF]


Home page
Mol PlantHome page
H.-Y. Zhang, H. He, L.-B. Chen, L. Li, M.-Z. Liang, X.-F. Wang, X.-G. Liu, G.-M. He, R.-S. Chen, L.-G. Ma, et al.
A Genome-Wide Transcription Analysis Reveals a Close Correlation of Promoter INDEL Polymorphism and Heterotic Gene Expression in Rice Hybrids
Mol Plant, September 1, 2008; 1(5): 720 - 731.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. Radoev, H. C. Becker, and W. Ecke
Genetic Analysis of Heterosis for Yield and Yield Components in Rapeseed (Brassica napus L.) by Quantitative Trait Locus Mapping
Genetics, July 1, 2008; 179(3): 1547 - 1558.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. E. Melchinger, H. F. Utz, and C. C. Schon
Genetic Expectations of Quantitative Trait Loci Main and Interaction Effects Obtained With the Triple Testcross Design and Their Relevance for the Analysis of Heterosis
Genetics, April 1, 2008; 178(4): 2265 - 2274.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. Maccaferri, M. C. Sanguineti, S. Corneti, J. L. A. Ortega, M. B. Salem, J. Bort, E. DeAmbrogio, L. F. G. del Moral, A. Demontis, A. El-Ahmed, et al.
Quantitative Trait Loci for Grain Yield and Adaptation of Durum Wheat (Triticum durum Desf.) Across a Wide Range of Water Availability
Genetics, January 1, 2008; 178(1): 489 - 511.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. E. Melchinger, H. F. Utz, H.-P. Piepho, Z.-B. Zeng, and C. C. Schon
The Role of Epistasis in the Manifestation of Heterosis: A Systems-Oriented Approach
Genetics, November 1, 2007; 177(3): 1815 - 1825.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
B. Kusterer, H.-P. Piepho, H. F. Utz, C. C. Schon, J. Muminovic, R. C. Meyer, T. Altmann, and A. E. Melchinger
Heterosis for Biomass-Related Traits in Arabidopsis Investigated by Quantitative Trait Loci Analysis of the Triple Testcross Design With Recombinant Inbred Lines
Genetics, November 1, 2007; 177(3): 1839 - 1850.
[Abstract] [Full Text] [PDF]


Home page
ANN BOT (LOND)Home page
S.-H. Cheng, J.-Y. Zhuang, Y.-Y. Fan, J.-H. Du, and L.-Y. Cao
Progress in Research and Development on Hybrid Rice: A Super-domesticate in China
Ann. Bot., October 1, 2007; 100(5): 959 - 966.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
Z. Tang, X. Wang, Z. Hu, Z. Yang, and C. Xu
Genetic Dissection of Cytonuclear Epistasis in Line Crosses
Genetics, September 1, 2007; 177(1): 669 - 672.
[Abstract] [Full Text] [PDF]


Home page
Crop Sci.Home page
B. Wang, Y. Wu, W. Guo, X. Zhu, N. Huang, and T. Zhang
QTL Analysis and Epistasis Effects Dissection of Fiber Qualities in an Elite Cotton Hybrid Grown in Second Generation
Crop Sci., July 30, 2007; 47(4): 1384 - 1392.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
E. Frascaroli, M. A. Cane, P. Landi, G. Pea, L. Gianfranceschi, M. Villa, M. Morgante, and M. E. Pe
Classical Genetic and Quantitative Trait Loci Analyses of Heterosis in a Maize Hybrid Between Two Elite Inbred Lines
Genetics, May 1, 2007; 176(1): 625 - 644.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
B. Kusterer, J. Muminovic, H. F. Utz, H.-P. Piepho, S. Barth, M. Heckenberger, R. C. Meyer, T. Altmann, and A. E. Melchinger
Analysis of a Triple Testcross Design With Recombinant Inbred Lines Reveals a Significant Role of Epistasis in Heterosis for Biomass-Related Traits in Arabidopsis
Genetics, April 1, 2007; 175(4): 2009 - 2017.
[Abstract] [Full Text] [PDF]


Home page
Genome ResHome page
N. M. Springer and R. M. Stupar
Allelic variation and heterosis in maize: How do two halves make more than a whole?
Genome Res., March 1, 2007; 17(3): 264 - 275.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
D. Hedgecock, J.-Z. Lin, S. DeCola, C. D. Haudenschild, E. Meyer, D. T. Manahan, and B. Bowen
Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas)
PNAS, February 13, 2007; 104(7): 2313 - 2318.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
Y. Semel, J. Nissenbaum, N. Menda, M. Zinder, U. Krieger, N. Issman, T. Pleban, Z. Lippman, A. Gur, and D. Zamir
From the Cover: Overdominant quantitative trait loci for yield and fitness in tomato
PNAS, August 29, 2006; 103(35): 12981 - 12986.
[Abstract] [Full Text] [PDF]


Home page
J Exp BotHome page
S. Quarrie, S Pekic Quarrie, R Radosevic, D Rancic, A Kaminska, J. Barnes, M Leverington, C Ceoloni, and D Dodig
Dissecting a wheat QTL for yield present in a range of environments: from the QTL to candidate genes
J. Exp. Bot., August 1, 2006; 57(11): 2627 - 2637.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
B. van Swinderen and R. J. Greenspan
Flexibility in a Gene Network Affecting a Simple Behavior in Drosophila melanogaster
Genetics, April 1, 2005; 169(4): 2151 - 2163.
[Abstract] [Full Text] [PDF]


Home page
Crop Sci.Home page
J. Zhao, H. C. Becker, D. Zhang, Y. Zhang, and W. Ecke
Oil Content in a European x Chinese Rapeseed Population: QTL with Additive and Epistatic Effects and Their Genotype-Environment Interactions
Crop Sci., January 1, 2005; 45(1): 51 - 59.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. Peccoud, K. V. Velden, D. Podlich, C. Winkler, L. Arthur, and M. Cooper
The Selective Values of Alleles in a Molecular Network Model Are Context Dependent
Genetics, April 1, 2004; 166(4): 1715 - 1725.
[Abstract] [Full Text] [PDF]


Home page
Plant Physiol.Home page
R. C. Meyer, O. Torjek, M. Becher, and T. Altmann
Heterosis of Biomass Production in Arabidopsis. Establishment during Early Development
Plant Physiology, April 1, 2004; 134(4): 1813 - 1823.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
D. Zhong, A. Pai, and G. Yan
Quantitative Trait Loci for Susceptibility to Tapeworm Infection in the Red Flour Beetle
Genetics, November 1, 2003; 165(3): 1307 - 1315.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
J. Hua, Y. Xing, W. Wu, C. Xu, X. Sun, S. Yu, and Q. Zhang
Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid
PNAS, March 4, 2003; 100(5): 2574 - 2579.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. P. Hua, Y. Z. Xing, C. G. Xu, X. L. Sun, S. B. Yu, and Q. Zhang
Genetic Dissection of an Elite Rice Hybrid Revealed That Heterozygotes Are Not Always Advantageous for Performance
Genetics, December 1, 2002; 162(4): 1885 - 1895.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. J. Luo, Z.-K. Li, H. W. Mei, Q. Y. Shu, R. Tabien, D. B. Zhong, C. S. Ying, J. W. Stansel, G. S. Khush, and A. H. Paterson
Overdominant Epistatic Loci Are the Primary Genetic Basis of Inbreeding Depression and Heterosis in Rice. II. Grain Yield Components
Genetics, August 1, 2001; 158(4): 1755 - 1771.
[Abstract] [Full Text] [PDF]