Hierarchical additive effects on heterosis in rice (Oryza sativa L.)

Exploitation of heterosis in crops has contributed greatly to improvement in global food and energy production. In spite of the pervasive importance of heterosis, a complete understanding of its mechanisms has remained elusive. In this study, a small test-crossed rice population was constructed to investigate the formation mechanism of heterosis for 13 traits. The results of the relative mid-parent heterosis and modes of inheritance of all investigated traits demonstrated that additive effects were the foundation of heterosis for complex traits in a hierarchical structure, and multiplicative interactions among the component traits were the framework of heterosis in complex traits. Furthermore, new balances between unit traits and related component traits provided hybrids with the opportunity to achieve an optimal degree of heterosis for complex traits. This study dissected heterosis of both reproductive and vegetative traits from the perspective of hierarchical structure for the first time. Additive multiplicative interactions of component traits were proven to be the origin of heterosis in complex traits. Meanwhile, more attention should be paid to component traits, rather than complex traits, in the process of revealing the mechanism of heterosis.

[1]  G. Jander,et al.  Additive effects of two quantitative trait loci that confer Rhopalosiphum maidis (corn leaf aphid) resistance in maize inbred line Mo17 , 2014, Journal of experimental botany.

[2]  Tai Wang,et al.  Differential analysis of proteomes and metabolomes reveals additively balanced networking for metabolism in maize heterosis. , 2014, Journal of proteome research.

[3]  Jianbing Yan,et al.  Genetic basis of grain yield heterosis in an “immortalized F2” maize population , 2014, Theoretical and Applied Genetics.

[4]  H. Pospisil,et al.  Genome-wide meta-analysis of maize heterosis reveals the potential role of additive gene expression at pericentromeric loci , 2014, BMC Plant Biology.

[5]  D. Lobell,et al.  A meta-analysis of crop yield under climate change and adaptation , 2014 .

[6]  W. Zhou,et al.  Balance between a Higher Degree of Heterosis and Increased Reproductive Isolation: A Strategic Design for Breeding Inter-Subspecific Hybrid Rice , 2014, PloS one.

[7]  A. Capriotti,et al.  Heterosis profile of sunflower leaves: a label free proteomics approach. , 2014, Journal of proteomics.

[8]  Waqas Ahmed Malik,et al.  Heterosis-associated proteome analyses of maize (Zea mays L.) seminal roots by quantitative label-free LC-MS. , 2013, Journal of proteomics.

[9]  John Clifton-Brown,et al.  Accelerating the domestication of a bioenergy crop: identifying and modelling morphological targets for sustainable yield increase in Miscanthus , 2013, Journal of experimental botany.

[10]  Zhaohu Li,et al.  Construction of a linkage map and QTL mapping for fiber quality traits in upland cotton (Gossypium hirsutum L.) , 2013 .

[11]  Zhongxu Lin,et al.  Intraspecific linkage map construction and QTL mapping of yield and fiber quality of Gossypium babardense. , 2013 .

[12]  Z. Chen,et al.  Genomic and epigenetic insights into the molecular bases of heterosis , 2013, Nature Reviews Genetics.

[13]  Nathan M. Springer,et al.  Progress toward understanding heterosis in crop plants. , 2013, Annual review of plant biology.

[14]  J. Birchler,et al.  Genomic dosage effects on heterosis in triploid maize , 2013, Proceedings of the National Academy of Sciences.

[15]  Matthias Scholz,et al.  Heterosis manifestation during early Arabidopsis seedling development is characterized by intermediate gene expression and enhanced metabolic activity in the hybrids. , 2012, The Plant journal : for cell and molecular biology.

[16]  B. Mangin,et al.  The Genetic Basis of Heterosis: Multiparental Quantitative Trait Loci Mapping Reveals Contrasted Levels of Apparent Overdominance Among Traits of Agronomical Interest in Maize (Zea mays L.) , 2012, Genetics.

[17]  Lanzhi Li,et al.  QTL Mapping of Combining Ability and Heterosis of Agronomic Traits in Rice Backcross Recombinant Inbred Lines and Hybrid Crosses , 2012, PloS one.

[18]  J. Zou,et al.  A Dynamic and Complex Network Regulates the Heterosis of Yield-Correlated Traits in Rapeseed (Brassica napus L.) , 2011, PloS one.

[19]  S. Kaeppler Heterosis: one boat at a time, or a rising tide? , 2011, The New phytologist.

[20]  H. Piepho,et al.  Nonadditive protein accumulation patterns in Maize (Zea mays L.) hybrids during embryo development. , 2010, Journal of proteome research.

[21]  R. Veitia,et al.  Heterosis , 2010, Plant Cell.

[22]  Qifa Zhang,et al.  Genetic and molecular bases of rice yield. , 2010, Annual review of plant biology.

[23]  Dani Zamir,et al.  The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato , 2010, Nature Genetics.

[24]  Y. Qi,et al.  Global Epigenetic and Transcriptional Trends among Two Rice Subspecies and Their Reciprocal Hybrids[W] , 2010, Plant Cell.

[25]  B. Lu,et al.  Efficient indica and japonica rice identification based on the InDel molecular method: Its implication in rice breeding and evolutionary research , 2009 .

[26]  Zhike Lu,et al.  Inaugural Article: A transcriptomic analysis of superhybrid rice LYP9 and its parents , 2009 .

[27]  Shuang Wu,et al.  Additive and over-dominant effects resulting from epistatic loci are the primary genetic basis of heterosis in rice. , 2009, Journal of integrative plant biology.

[28]  Lanzhi Li,et al.  Dominance, Overdominance and Epistasis Condition the Heterosis in Two Heterotic Rice Hybrids , 2008, Genetics.

[29]  J. Qiu Is China ready for GM rice? , 2008, Nature.

[30]  H. Piepho,et al.  Comparison of Maize (Zea mays L.) F1-Hybrid and Parental Inbred Line Primary Root Transcriptomes Suggests Organ-Specific Patterns of Nonadditive Gene Expression and Conserved Expression Trends , 2008, Genetics.

[31]  Nathan M. Springer,et al.  Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis , 2008, BMC Plant Biology.

[32]  F. Hochholdinger,et al.  Towards the molecular basis of heterosis. , 2007, Trends in plant science.

[33]  Nathan M. Springer,et al.  Allelic variation and heterosis in maize: how do two halves make more than a whole? , 2007, Genome research.

[34]  Jianbing Yan,et al.  Detection of quantitative trait loci and heterotic loci for plant height using an immortalized F2 population in maize , 2007 .

[35]  Z. Lippman,et al.  Heterosis: revisiting the magic. , 2007, Trends in genetics : TIG.

[36]  X. Cui,et al.  Inheritance Patterns of Transcript Levels in F1 Hybrid Mice , 2006, Genetics.

[37]  H. Piepho,et al.  Comparative expression profiling in meristems of inbred-hybrid triplets of maize based on morphological investigations of heterosis for plant height , 2006, Plant Molecular Biology.

[38]  J. Birchler,et al.  Unraveling the genetic basis of hybrid vigor , 2006, Proceedings of the National Academy of Sciences.

[39]  Naama Menda,et al.  Overdominant quantitative trait loci for yield and fitness in tomato , 2006, Proceedings of the National Academy of Sciences.

[40]  Nathan M. Springer,et al.  Cis-transcriptional Variation in Maize Inbred Lines B73 and Mo17 Leads to Additive Expression Patterns in the F1 Hybrid , 2006, Genetics.

[41]  O. Crasta,et al.  Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis , 2006, Theoretical and Applied Genetics.

[42]  Dan Nettleton,et al.  All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[43]  U. Roessner,et al.  Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement , 2006, Nature Biotechnology.

[44]  Eric E Schadt,et al.  Cis-acting expression quantitative trait loci in mice. , 2005, Genome research.

[45]  Zihua Hu,et al.  Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. , 2003, The Plant journal : for cell and molecular biology.

[46]  R. Bernardo,et al.  Genetic basis of heterosis explored by simple sequence repeat markers in a random-mated maize population , 2003, Theoretical and Applied Genetics.

[47]  Z. Li,et al.  Gene actions of QTLs affecting several agronomic traits resolved in a recombinant inbred rice population and two backcross populations , 2003, Theoretical and Applied Genetics.

[48]  Jinping Hua,et al.  Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  V. Lefebvre,et al.  Comparative mapping of Phytophthora resistance loci in pepper germplasm: evidence for conserved resistance loci across Solanaceae and for a large genetic diversity , 2003, Theoretical and Applied Genetics.

[50]  A. Paterson,et al.  Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. , 2001, Genetics.

[51]  A. Paterson,et al.  Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. , 2001, Genetics.

[52]  Cai-guo Xu,et al.  Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[53]  A. Paterson,et al.  Genetics of Hybrid Sterility and Hybrid Breakdown in an Intersubspecific Rice ( O y a sativa L.) Population , 2022 .

[54]  A. Paterson,et al.  Epistasis for three grain yield components in rice (Oryza sativa L.). , 1997, Genetics.

[55]  H. F. Utz,et al.  Heterosis and gene effects of multiplicative characters: theoretical relationships and experimental results from Vicia faba L. , 1994, Theoretical and Applied Genetics.

[56]  C. Cockerham,et al.  Multiplicative vs. arbitrary gene action in heterosis. , 1992, Genetics.

[57]  T. Helentjaris,et al.  Molecular marker-facilitated investigations of quantitative trait loci in maize. II. Factors influencing yield and its component traits , 1987 .

[58]  J. Wendel,et al.  Molecular-marker-facilitated investigations of quantitative-trait loci in maize. I. Numbers, genomic distribution and types of gene action. , 1987, Genetics.

[59]  W. Hill The genetic basis of heterosis , 1982, Annales de génétique et de sélection animale.

[60]  G. Hobson,et al.  The possible use of mitochondrial complementation as an indicator of yield heterosis in breeding hybrid wheat , 1973, Euphytica.

[61]  Charles Darwin,et al.  The Effects of Cross and Self Fertilisation in the Vegetable Kingdom , 1972 .

[62]  W. Williams Heterosis and the genetics of complex characters , 1960, Heredity.

[63]  A. Melchinger,et al.  Correlation between parental transcriptome and field data for the characterization of heterosis in Zea mays L. , 2009, Theoretical and Applied Genetics.

[64]  H. Piepho,et al.  Heterosis in early seed development: a comparative study of F1 embryo and endosperm tissues 6 days after fertilization , 2009, Theoretical and Applied Genetics.

[65]  R. Jorgensen,et al.  Genetic and developmental control of anthocyanin biosynthesis. , 1991, Annual review of genetics.