TY - JOUR
AU - Kapoor, Sanjay
AB - Abstract Perceived by Charles Darwin in many vegetable plants and rediscovered by George H Shull and Edward M East in maize, heterosis or hybrid vigour is one of the most widely utilized phenomena, not only in agriculture but also in animal breeding. Although, numerous studies have been carried out to understand its genetic and/or molecular basis in the past 100 years, our knowledge of the underlying molecular processes that results in hybrid vigour can best be defined as superficial. Even after century long deliberations, there is no consensus on the relative/individual contribution of the genetic/epigenetic factors in the manifestation of heterosis. However, with the recent advancements in functional genomics, transcriptomics, proteomics, and metabolomics-related technologies, the riddle of heterosis is being reinvestigated by adopting systems-level approaches to understand the underlying molecular mechanisms. A number of intriguing hypotheses are converging towards the idea of a cumulative positive effect of the differential expression of a variety of genes, on one or several yield-affecting metabolic pathways or overall energy-use efficiency, as the underlying mechanism for the manifestation of heterosis. Presented here is a brief account of clues gathered from various investigative approaches targeted towards better scientific understanding of this process. Circadian clock, dominance, energy use efficiency, growth and development, over-dominance, yield Introduction Heterosis or hybrid vigour is a phenomenon that describes the survival and performance superiority of a hybrid offspring over the average of both its genetically distinct parents. In plants, heterosis is known to be a multigenic complex trait and can be extrapolated as the sum total of many physiological and phenotypic traits including magnitude and rate of vegetative growth, flowering time, yield (in terms of inflorescence number, flowers per inflorescence, fruit or grain set and weight), and resistance to biotic and abiotic environmental rigours; each of them contributing to heterosis to a certain extent (Lippman and Zamir, 2007). Clues from genetic studies Conventionally, the manifestation of heterosis has been attributed to ‘Dominance’ as well ‘Over-dominance’ as the major underlying genetic factors. Later ‘Epistatic interactions’ and ‘Epigenetics factors’ were also found to contribute to heterosis. Emerging views now suggest that the combination of the parental pair has a major bearing on the extent of heterosis manifested by the hybrid for different traits and thereby affecting the overall performance of the hybrid (Chen, 2010). Hybrid formation could also be defined as an event where two adequately distinct genomes come together and undergo a phase of genomic turbulence before entering a state of homeostasis. This phase of genomic turbulence or ‘Genomic Shock’, as proposed by Barbara McClintock (McClintock, 1984), may cause the genome-wide relaxation of gene expression including transposon activation, ultimately leading to differential/novel expression patterns (Ha et al., 2009). Clues from transcriptomic studies A number of whole-genome transcriptome analyses have been carried out in successful inbred parental lines and the hybrid combinations to classify differential gene expression patterns into modes of gene action in a hybrid vis-à-vis its inbred parental lines and to correlate those changes to gains in biomass and yield (Kollipara et al., 2002; Guo et al., 2003, 2004, 2006; Auger et al., 2005; Bao et al., 2005; Huang et al., 2006a, b; Swanson-Wagner et al., 2006; Hochholdinger and Hoecker, 2007; Meyer et al., 2007; Song et al., 2007; Springer and Stupar, 2007; Uzarowska et al., 2007; Hoecker et al., 2008a, b; Stupar et al., 2008; Zhang et al., 2008; Gang Wei et al., 2009; Birchler et al., 2010; Frisch et al., 2010; Jahnke et al., 2010; Riddle et al., 2010). In another strategy, transcriptomes of large parental populations have been analysed to establish correlations between differential expression patterns in a number of parental inbreds to yield-related parameters in the hybrids resulting from their factorial crosses (Hoecker et al., 2008a; Stupar et al., 2008). As a universal code for heterosis related transcriptomic studies, the modes of gene action (for differentially expressed genes) have mainly been classified into additive, dominance, and over-dominance categories. The additive mode of gene action represents mid-parental expression values in the hybrid, while the dominance mode signifies both low and high parent-like expression. In the case of over-dominance or under-dominance, the expression value of a particular differentially expressed gene in the hybrid is either higher than the high parent or lower than the low parent value, respectively. The initial transcriptome based studies (Comings and MacMurray, 2000) explained heterosis as the establishment of more favourable gene expression levels in the hybrids compared with the parents. Several studies in maize and rice reported the prevalence of non-additive gene expression (Auger et al., 2005; Uzarowska et al., 2007; Hoecker et al., 2008a; Zhang et al., 2008; Fujimoto et al., 2012; Meyer et al., 2012),while others detected mainly additive gene expression levels (Swanson-Wagner et al., 2006; Meyer et al., 2007; Zhang et al., 2008). In contrast to the observation in maize (Swanson-Wagner et al., 2006), work on growth heterosis in larval pacific oysters revealed non-additive gene action to be the predominant mode of gene action during the active growth phase in the hybrids (Hedgecock et al., 2007). Of the two heterotic hybrids resulting from PA64s X93-11 and the Nipponbare X93-11 crosses, the first predominantly exhibited additivity (Zhang et al., 2008), while non-additivity was the major mode of gene action in the second hybrid, at the younger stages of development (Zhang et al., 2008; He et al., 2010). In two recent reports, the manifestation of biomass heterosis in Arabidopsis Col-0 and C24 hybrids during the early stages of vegetative development has been attributed to the predominance of either dominant [high parent-like; intermediate; (Meyer et al., 2012) or over-dominant; higher than the high parent; (Fujimoto et al., 2012)] non-additive gene expression modes. The moderate non-additivity was suggested to lead to higher metabolic activity due to a better resource efficiency, and therefore enhanced performance in the hybrids (Meyer et al., 2012). Fujimoto and coworkers, however, have correlated extreme non-additivity, exhibited by a major proportion of differentially expressed genes, to increased photosynthesis and determination of cell size and number, which could play a central role in the manifestation of biomass heterosis (Fujimoto et al., 2012). Transcriptomic analyses have been further refined to reveal allele-specific expression in reciprocal hybrids but the significance of maternal or paternal effects on gene expression could not be established (Guo et al., 2004; Stupar and Springer, 2006). Recently, in maize and Arabidopsis, epigenetic modifications in circadian clock genes and altered gene expression resulting from differentially expressed small RNAs have been linked to increased biomass and, eventually, to heterosis (Ni et al., 2009; Groszmann et al., 2011). Surprisingly, over-dominant mode of gene action of a single flowering gene has been found to drive yield heterosis (Krieger et al., 2010). Data from transcriptomic studies has enhanced our understanding of the extent of genome-wide transcriptome fluctuations, while highlighting the importance of certain key biochemical pathways that may prove to be quintessential for the manifestation of heterosis. These studies have also revealed the common occurrence of genes from basic metabolisms like carbohydrate, protein, lipid, and hormone in many hybrids suggesting a possibility of higher-level regulatory mechanism(s), which is able to influence these pathways in most heterotic combinations. Clues from epigenomic studies When two genetically distant parental lines are combined to obtain hybrids, besides obvious interactions in cis and trans genetic factors, DNA methylation machinery and its components that maintain and regulate epigenomic status would also interact. To gain insights into the extent of the role played by the epigenetic machinery and its dynamics in the manifestation of heterosis, genome-wide methylation, miRNA expression, and siRNA distribution patterns have been analysed in the past three to four years (Ha et al., 2009; Groszmann et al., 2011; Shen et al., 2012). Rapid changes in siRNA population and non-additive expression of more than 50% miRNA was observed in Arabidopsis allotetraploids lines, suggesting the involvement of the small RNA machinery in growth, vigour, and adaptation (Ha et al., 2009). In a study involving the mapping of genomic regions contributing to 24-nt small RNA population in Arabidopsis thaliana C24 and Ler accessions and their intraspecific hybrids, positive correlation between genomic regions with reduced 24-nt small RNA levels, differential gene expression, and the respective changes in DNA methylation levels were revealed (Groszmann et al., 2011). Using genome-wide methylome profiling of the same parent–hybrid combination, Shen and co-workers found that both hybrids had increased cytosine methylation compared with the parents (Shen et al., 2012). The higher methylation levels were correlated with transcriptional down-regulation of more genes in the hybrids than the parental lines. These genes included central clock genes, CCA1 and LHY, which have previously been shown to have profound effects on biomass heterosis (Shen et al., 2012). This study further showed that increased DNA methylation in hybrids predominantly occurred in regions that were differentially methylated in the parents and covered by small RNAs, implying that RNA-dependent DNA methylation may be responsible for increased DNA methylation in reciprocal hybrids. Using the same parental combination Greaves et al. (2012) showed that methylome dynamics in the hybrid were frequently associated with regions where parental methylation levels were different. This means that the methylation levels of alleles from one parent were altered to resemble that of the other parent by a process that also involved changes in corresponding si-RNA levels. A recent study involving small RNA profiling in a maize hybrid–parent combination revealed the non-additive differential accumulation of ~90% of miRNA species, along with the specific accumulation of three miRNA species in the hybrid compared with the parental lines (Ding et al., 2012). In this investigation, about two-thirds of the differentially expressed miRNA families exhibited down-regulation. These miRNA families included, miR168, miR164, miR169, miR156, and miR396 that are known to regulate ARGONAUTE 1 (AGO1), NAC Domain containing proteins (NAC1), Nuclear Factor Y (NFY), Spindle Pole Body (SBP domain proteins), and Zinc finger GRFs (GRFs) which are, in turn, known for their involvement in various development-associated pathways and those involved in energy and protein metabolism. The emerging model If plants are biological engines, which take light energy as input to assimilate basic elements into biomass, the net energy converted to biomass could be expressed as:  EnergyBiomass = Energyinput - Energyconsumed Hence, either an increase in the input energy or a decrease in the energy consumed in basic metabolic processes could result in increased growth and biomass. A recent model by Goff emphasizes the role of energy-use efficiency in the manifestation of multigenic heterosis (Goff, 2011). According to this model, hybrids have more efficient growth than the inbreds because of the significant reduction in the energy-consuming processes of protein metabolism. Because of this fine-tuning, hybrids are able to conserve energy from basic metabolism, and translate it into higher growth rates and biomass (Hauben et al., 2009). The importance of increased energy input, on the other hand, has been highlighted by Ni and coworkers (Ni et al., 2009), who proposed that resetting of the circadian clock to a higher amplitude during the day leads to increased photosynthetic efficiency and, thereby, to growth vigour and increased biomass. Taken together it is becoming evident that, in a biological system, a positive modulation of energy can translate into vigour and biomass. In different heterotic combinations, this modulation might be achieved by different means and at different phases of growth and development. This might explain the observed differences in the modes of gene action at various stages of development. In different heterotic combinations, both additive and non-additive modes of differential gene actions have been shown to be involved in the manifestation of heterosis. Correlations between the positive modulation of the circadian clock and the non-additive mode of gene action have mainly been found during the early developmental stages of heterotic hybrids (Fujimoto et al., 2012) and there is mounting evidence of the involvement of the epigenetic machinery in regulating this multigenic trait (Groszmann et al., 2011; Greaves et al., 2012). Delineation and functional characterization of major yield-related QTLs have resulted in identification of genes associated with specific traits like panicle branching, grain number, grain size, grain weight etc, which might have been contributing to heterosis. Introgression of naturally occurring (or synthetic) superior alleles of these genes could be used for directed heterosis (Fig. 1: Ashikari et al., 2005; Tamaki et al., 2007; Krieger et al., 2010; Mao et al., 2010; Miura et al., 2010; Li et al., 2011). Fig. 1. View largeDownload slide A diagrammatic representation of the current status of our understanding of the molecular basis of heterosis based on studies carried out in Arabidopsis, maize, and rice during vegetative (young and mature) or reproductive stages of development. Most of these studies reveal a major proportion of differential expression profiles (DEPs) in younger vegetative and reproductive stages to be non-additive, although additive DEPs do exist. During mature stages of vegetative development the differential expression activity has been reported to be significantly reduced and a major proportion consists of additive DEPs. The non-additive DEPs have been shown to affect components of the clock and a significant number of the downstream CCA1 Binding Site (CBS)-/evening element containing genes involved in photosynthesis and starch biosynthesis, which have been implicated in biomass heterosis. The additive DEPs may also contribute to biomass heterosis albeit in a less significant manner. The increase in biomass during vegetative development may contribute to the yield. On the other hand, mutations/silencing or overexpression of single genes identified by in-depth characterization of yield-related QTLs (representing non-additive DEPs) have also been found to have profound effects on yield during stages of reproductive development. Recent studies also show linkages between epigenetic determinants, non-additive DEPs, and the circadian clock contributing to biomass gains. The colour and thickness of the numbered arrows are representative of their linkages to the stages of development and literature support as following: (1) Zhang et al., 2008; He et al., 2010; Fujimoto et al., 2012; Meyer et al., 2012; (2) Stupar and Springer, 2006; Swanson-Wagner et al., 2006; Zhang et al., 2008; (3) Wei et al., 2009; (4) Ha et al., 2009; Groszmann et al., 2011; Greaves et al., 2012; Shen et al., 2012; (5) Xiong et al., 1999; Ha et al., 2009; (6) Hauben et al., 2009; (7) He et al., 2010; Shen et al., 2012; (8) Ni et al., 2009; Shen et al., 2012; (9) Auger et al., 2005; (10) Ashikari et al., 2005; Tamaki et al., 2007; Krieger et al., 2010; Mao et al., 2010; Miura et al., 2010; Li et al., 2011; (11) Miura et al., 2010; (12) Stupar and Springer, 2006; (13) Gibson et al., 2004; Huang et al., 2006b; Ge et al., 2008; Wei et al., 2009. Fig. 1. View largeDownload slide A diagrammatic representation of the current status of our understanding of the molecular basis of heterosis based on studies carried out in Arabidopsis, maize, and rice during vegetative (young and mature) or reproductive stages of development. Most of these studies reveal a major proportion of differential expression profiles (DEPs) in younger vegetative and reproductive stages to be non-additive, although additive DEPs do exist. During mature stages of vegetative development the differential expression activity has been reported to be significantly reduced and a major proportion consists of additive DEPs. The non-additive DEPs have been shown to affect components of the clock and a significant number of the downstream CCA1 Binding Site (CBS)-/evening element containing genes involved in photosynthesis and starch biosynthesis, which have been implicated in biomass heterosis. The additive DEPs may also contribute to biomass heterosis albeit in a less significant manner. The increase in biomass during vegetative development may contribute to the yield. On the other hand, mutations/silencing or overexpression of single genes identified by in-depth characterization of yield-related QTLs (representing non-additive DEPs) have also been found to have profound effects on yield during stages of reproductive development. Recent studies also show linkages between epigenetic determinants, non-additive DEPs, and the circadian clock contributing to biomass gains. The colour and thickness of the numbered arrows are representative of their linkages to the stages of development and literature support as following: (1) Zhang et al., 2008; He et al., 2010; Fujimoto et al., 2012; Meyer et al., 2012; (2) Stupar and Springer, 2006; Swanson-Wagner et al., 2006; Zhang et al., 2008; (3) Wei et al., 2009; (4) Ha et al., 2009; Groszmann et al., 2011; Greaves et al., 2012; Shen et al., 2012; (5) Xiong et al., 1999; Ha et al., 2009; (6) Hauben et al., 2009; (7) He et al., 2010; Shen et al., 2012; (8) Ni et al., 2009; Shen et al., 2012; (9) Auger et al., 2005; (10) Ashikari et al., 2005; Tamaki et al., 2007; Krieger et al., 2010; Mao et al., 2010; Miura et al., 2010; Li et al., 2011; (11) Miura et al., 2010; (12) Stupar and Springer, 2006; (13) Gibson et al., 2004; Huang et al., 2006b; Ge et al., 2008; Wei et al., 2009. The next set of questions would be: how is the modulation of energy achieved to yield positive heterosis; mechanistically, what are its components and how does mixing of two genomes affect their equilibrium? Certainly, when two adequately different genomes come together in a hybrid, the genome dynamics (depending on cis, trans, and chromatin/epigenomic interactions) translates into the differential expression of a large number of genes. The changes in gene expression patterns, whether additive or non-additive, would affect both regulatory and metabolic pathways depending on their affiliations and in a manner that would have a net positive or negative effect on the cumulative output of any individual pathway. It seems logical that, if an individual or a combination of differential gene expression patterns translates into positive modulation of any major regulatory pathway, it could have a major influence on the manifestation of heterosis (Fig. 2). But could we identify key pathways whose net positive modulation is obligatory for the manifestation of heterosis? The circadian clock and down-regulation of protein metabolism certainly seem two of those, but are these two sufficient? In another scenario, heterosis could still manifest if, instead of a major regulatory pathway, a group of downstream biochemical pathways are individually affected by the transcriptome dynamics and are able to bring net positivity to the system in terms of growth and development. However, to gauge the net positivity or negativity in the system for growth and development, a manageable number of standard markers (either biochemical or mode of gene actions) will have to be identified or developed. These markers would help define the currency of energy in all its denominations, and the net balance of this currency in the system would define the state and extent of heterosis. The development of such a currency system and understanding of its dynamics would bring us closer to the ultimate goal of predicting the heterotic potential of any unknown parental combination. Fig. 2. View largeDownload slide A model outlining the mechanistic aspects of manifestation of heterosis. Mixing of two adequately distant genomes brings about cis, trans, and chromatin level changes in the hybrid, which results in differential expression of a number of genes. These expression patterns, which might represent additive or non-additive modes of gene action, may primarily affect a few major regulatory pathways which, in turn, send out regulatory cues that either individually or cumulatively affect a number of downstream metabolic pathways (including photosynthesis, starch and protein metabolism, etc) in either a positive or a negative manner. These individual pathways, whether placed on the input side or the consumption side of the energy equation, affect various aspects of growth and development. The net positivity or negativity in the system, therefore, would define the state and extent of heterosis. Fig. 2. View largeDownload slide A model outlining the mechanistic aspects of manifestation of heterosis. Mixing of two adequately distant genomes brings about cis, trans, and chromatin level changes in the hybrid, which results in differential expression of a number of genes. These expression patterns, which might represent additive or non-additive modes of gene action, may primarily affect a few major regulatory pathways which, in turn, send out regulatory cues that either individually or cumulatively affect a number of downstream metabolic pathways (including photosynthesis, starch and protein metabolism, etc) in either a positive or a negative manner. These individual pathways, whether placed on the input side or the consumption side of the energy equation, affect various aspects of growth and development. The net positivity or negativity in the system, therefore, would define the state and extent of heterosis. References Ashikari M Sakakibara H Lin S Yamamoto T Takashi T Nishimura A Angeles ER Qian Q Kitano H Matsuoka M. 2005 Cytokinin oxidase regulates rice grain production Science  309 741– 745 Google Scholar CrossRef Search ADS   Auger DL Gray AD Ream TS Kato A Coe EH Jr Birchler JA. 2005 Nonadditive gene expression in diploid and triploid hybrids of maize Genetics  169 389– 397 Google Scholar CrossRef Search ADS   Bao J Lee S Chen C et al.   2005 Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars Plant Physiology  138 1216– 1231 Google Scholar CrossRef Search ADS   Birchler JA Yao H Chudalayandi S Vaiman D Veitia RA. 2010 Heterosis The Plant Cell  22 2105– 2112 Google Scholar CrossRef Search ADS   Chen ZJ. 2010 Molecular mechanisms of polyploidy and hybrid vigor Trends in Plant Science  15 57– 71 Google Scholar CrossRef Search ADS   Comings D MacMurray JP. 2000 Molecular heterosis: a review Molecular Genetics and Metabolism  71 19– 31 Google Scholar CrossRef Search ADS   Ding D Wang Y Han M Fu Z Li W Liu Z Hu Y Tang J. 2012 MicroRNA transcriptomic analysis of heterosis during maize seed germination PloS One  7 e39578 Google Scholar CrossRef Search ADS   Frisch M Thiemann A Fu J Schrag TA Scholten S Melchinger AE. 2010 Transcriptome-based distance measures for grouping of germplasm and prediction of hybrid performance in maize Theoretical and Applied Genetics  120 441– 450 Google Scholar CrossRef Search ADS   Fujimoto R Taylor JM Shirasawa S Peacock WJ Dennis ES. 2012 Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity Proceedings of the National Academy of Sciences, USA  109 7109– 7114 Google Scholar CrossRef Search ADS   Gang Wei Yong Taoa Guozhen Liuc et al.   2009 A transcriptomic analysis of superhybrid rice LYP9 and its parents Proceedings of the National Academy of Sciences, USA  106 7695– 7701 Google Scholar CrossRef Search ADS   Google Scholar Ge X Chen W Song S Wang W Hu S Yu J. 2008 Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9 and its parental lines BMC Plant Biology  8– 114 Gibson G Riley-Berger R Harshman L Kopp A Vacha S Nuzhdin S Wayne M. 2004 Extensive sex-specific nonadditivity of gene expression in Drosophila melanogaster Genetics  167 1791– 1799 Google Scholar CrossRef Search ADS   Goff SA. 2011 A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding New Phytologist  189 923– 937 Google Scholar CrossRef Search ADS   Greaves IK Groszmann M Ying H Taylor JM Peacock WJ Dennis ES. 2012 Trans chromosomal methylation in Arabidopsis hybrids Proceedings of the National Academy of Sciences, USA  109 3570– 3575 Google Scholar CrossRef Search ADS   Groszmann M Greaves IK Albertyn ZI Scofield GN Peacock WJ Dennis ES. 2011 Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor Proceedings of the National Academy of Sciences, USA  108 2617– 2622 Google Scholar CrossRef Search ADS   Guo M Rupe MA Danilevskaya ON Yang X Hu Z. 2003 Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm The Plant Journal  36 30– 44 Google Scholar CrossRef Search ADS   Guo M Rupe MA Yang X Crasta O Zinselmeier C Smith OS Bowen B. 2006 Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis Theoretical and Applied Genetics  113 831– 845 Google Scholar CrossRef Search ADS   Guo M Rupe MA Zinselmeier C Habben J Bowen BA Smith OS. 2004 Allelic variation of gene expression in maize hybrids The Plant Cell  16 1707– 1716 Google Scholar CrossRef Search ADS   Ha M Lu J Tian L Ramachandran V Kasschau KD Chapman EJ Carrington JC Chen X Wang X-J Chen ZJ. 2009 Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids Proceedings of the National Academy of Sciences, USA  106 17835– 17840 Google Scholar CrossRef Search ADS   Hauben M Haesendonckx B Standaert E et al.   2009 Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield Proceedings of the National Academy of Sciences, USA  106 20109– 20114 Google Scholar CrossRef Search ADS   He G Zhu X Elling AA et al.   2010 Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids The Plant Cell  22 17– 33 Google Scholar CrossRef Search ADS   Hedgecock D Lin JZ DeCola S Haudenschild CD Meyer E Manahan DT Bowen B. 2007 Transcriptomic analysis of growth heterosis in larval Pacific oysters (Crassostrea gigas) Proceedings of the National Academy of Sciences, USA  104 2313– 2318 Google Scholar CrossRef Search ADS   Hochholdinger F Hoecker N. 2007 Towards the molecular basis of heterosis Trends in Plant Science  12 427– 432 Google Scholar CrossRef Search ADS   Hoecker N Keller B Muthreich N Chollet D Descombes P Piepho HP Hochholdinger F. 2008 a Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of non-additive gene expression and conserved expression trends Genetics  179 1275– 1283 Google Scholar CrossRef Search ADS   Hoecker N Lamkemeyer T Sarholz B et al.   2008 b Analysis of non-additive protein accumulation in young primary roots of a maize (Zea mays L.) F1-hybrid compared to its parental inbred lines Proteomics  8 3882– 3894 Google Scholar CrossRef Search ADS   Huang Y Li L Chen Y Li X Xu C Wang S Zhang Q. 2006 a Comparative analysis of gene expression at early seedling stage between a rice hybrid and its parents using a cDNA microarray of 9198 uni-sequences Science in China Series C: Life Sciences  49 519– 529 Google Scholar CrossRef Search ADS   Huang Y Zhang L Zhang J Yuan D Xu C Li X Zhou D Wang S Zhang Q. 2006 b Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs Plant Molecular Biology  62 579– 591 Google Scholar CrossRef Search ADS   Jahnke S Sarholz B Thiemann A Kuhr V Gutierrez-Marcos JF Geiger HH Piepho HP Scholten S. 2010 Heterosis in early seed development: a comparative study of F1 embryo and endosperm tissues 6 days after fertilization . Theoretical and Applied Genetics  120 389– 400 Google Scholar CrossRef Search ADS   Kollipara KP Saab IN Wych RD Lauer MJ Singletary GW. 2002 Expression profiling of reciprocal maize hybrids divergent for cold germination and desiccation tolerance Plant Pphysiology  129 974– 992 Google Scholar CrossRef Search ADS   Krieger U Lippman ZB Zamir D. 2010 The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato Nature Genetics  42 459– 463 Google Scholar CrossRef Search ADS   Li M Tang D Wang K Wu X Lu L Yu H Gu M Yan C Cheng Z. 2011 Mutations in the F-box gene LARGER PANICLE improve the panicle architecture and enhance the grain yield in rice Plant Biotechnology Journal  9 1002– 1013 Google Scholar CrossRef Search ADS   Lippman Z Zamir D. 2007 Heterosis: revisiting the magic Trends in Genetics  23 60– 66 Google Scholar CrossRef Search ADS   Mao H Sun S Yao J Wang C Yu S Xu C Li X Zhang Q. 2010 Linking differential domain functions of the GS3 protein to natural variation of grain size in rice Proceedings of the National Academy of Sciences, USA  107 19579– 19584 Google Scholar CrossRef Search ADS   McClintock B. 1984 The significance of responses of the genome to challenge Science  226 792– 801 Google Scholar CrossRef Search ADS   Meyer RC Witucka-Wall H Becher M et al.   2012 Heterosis manifestation during early Arabidopsis seedling development is characterized by intermediate gene expression and enhanced metabolic activity in the hybrids The Plant Journal  71 669– 683 Google Scholar CrossRef Search ADS   Meyer S Pospisil H Scholten S. 2007 Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern Plant Molecular Biology  63 381– 391 Google Scholar CrossRef Search ADS   Miura K Ikeda M Matsubara A Song XJ Ito M Asano K Matsuoka M Kitano H Ashikari M. 2010 OsSPL14 promotes panicle branching and higher grain productivity in rice Nature Genetics  42 545– 549 Google Scholar CrossRef Search ADS   Ni Z Kim E-D Ha M Lackey E Liu J Zhang Y Sun Q Chen ZJ. 2009 Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids Nature  457 327– 331 Google Scholar CrossRef Search ADS   Riddle NC Jiang H An L Doerge RW Birchler JA. 2010 Gene expression analysis at the intersection of ploidy and hybridity in maize Theoretical and Applied Genetics  120 341– 353 Google Scholar CrossRef Search ADS   Shen H He H Li J et al.   2012 Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids The Plant Cell  24 875– 892 Google Scholar CrossRef Search ADS   Song X Ni Z Yao Y Xie C Li Z Wu H Zhang Y Sun Q. 2007 Wheat (Triticum aestivum L.) root proteome and differentially expressed root proteins between hybrid and parents Proteomics  7 3538– 3557 Google Scholar CrossRef Search ADS   Springer NM Stupar RM. 2007 Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Research  17 264– 275 Google Scholar CrossRef Search ADS   Stupar RM Gardiner JM Oldre AG Haun WJ Chandler VL Springer NM. 2008 Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis BMC Plant Biology  8 33 Google Scholar CrossRef Search ADS   Stupar RM Springer NM. 2006 Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid Genetics  173 2199– 2210 Google Scholar CrossRef Search ADS   Swanson-Wagner RA Jia Y DeCook R Borsuk LA Nettleton D Schnable PS. 2006 All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents Proceedings of the National Academy of Sciences, USA  103 6805– 6810 Google Scholar CrossRef Search ADS   Tamaki S Matsuo S Wong HL Yokoi S Shimamoto K. 2007 Hd3a protein is a mobile flowering signal in rice Science  316 1033– 1036 Google Scholar CrossRef Search ADS   Uzarowska A Keller B Piepho HP Schwarz G Ingvardsen C Wenzel G Lubberstedt T. 2007 Comparative expression profiling in meristems of inbred-hybrid triplets of maize based on morphological investigations of heterosis for plant height Plant Molecular Biology  63 21– 34 Google Scholar CrossRef Search ADS   Wei G Tao Y Liu G et al.   2009 A transcriptomic analysis of superhybrid rice LYP9 and its parents Proceedings of the National Academy of Sciences, USA  106 7695– 7701 Google Scholar CrossRef Search ADS   Xiong LZ Xu CG Saghai Maroof MA Zhang Q. 1999 Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique Molecular and General Genetics  261 439– 446 Google Scholar CrossRef Search ADS   Zhang HY Hang H Liang-Bi C et al.   2008 A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids Molecular Plant  1 720– 731 Google Scholar CrossRef Search ADS   © The Author [2012]. 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TI - Heterosis: emerging ideas about hybrid vigour
JF - Journal of Experimental Botany
DO - 10.1093/jxb/ers291
DA - 2012-10-23
UR - https://www.deepdyve.com/lp/oxford-university-press/heterosis-emerging-ideas-about-hybrid-vigour-kpUKUin2C0
SP - 6309
EP - 6314
VL - 63
IS - 18
DP - DeepDyve
ER -