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Genomic architecture of biomass heterosis in Arabidopsis

ABSTRACT: Heterosis is most frequently manifested by the substantially increased vigorous growth of hybrids compared with their parents. Investigating genomic variations in natural populations is essential to understand the initial molecular mechanisms underlying heterosis in plants. Here, we characterized the genomic architecture associated with biomass heterosis in 200 Arabidopsis hybrids. The genome-wide heterozygosity of hybrids makes a limited contribution to biomass heterosis, and no locus shows an obvious overdominance effect in hybrids. However, the accumulation of significant genetic loci identified in genome wide association studies (GWAS) in hybrids strongly correlates with better-parent heterosis (BPH). Candidate genes for biomass BPH fall into diverse biological functions, including cellular, metabolic, and developmental processes and stimulus-responsive pathways. Important heterosis candidates include WUSCHEL, ARGOS, and some genes that encode key factors involved in cell cycle regulation. Interestingly, transcriptomic analyses in representative Arabidopsis hybrid combinations reveal that heterosis candidate genes are functionally enriched in stimulus-responsive pathways, including responses to biotic and abiotic stimuli and immune responses. In addition, stimulus-responsive genes are repressed to low-parent levels in hybrids with high BPH, whereas middle-parent expression patterns are exhibited in hybrids with no BPH. Our study reveals a genomic architecture for understanding the molecular mechanisms of biomass heterosis in Arabidopsis, in which the accumulation of the superior alleles of genes involved in metabolic and cellular processes improve the development and growth of hybrids, whereas the overall repressed expression of stimulus responsive genes prioritizes growth over responding to environmental stimuli in hybrids under normal conditions.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE85759 | GEO | 2017/08/03

SECONDARY ACCESSION(S): PRJNA339285

REPOSITORIES: GEO

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Project description:Hybrid plants and animals grow larger and more vigorously than the parents, a common phenomenon known as hybrid vigor or heterosis. Heterosis often correlates with the genetic distance between hybridizing parents, but the mechanism for this is largely unknown. We found that genetic distance was correlated with natural variation of stress responses under the control of the circadian clock. CIRCADIAN-CLOCK-ASSOCIATED1 (CCA1) and LATE-ELONGATED-HYPOCOTYL (LHY) or CCA1 alone mediate expression amplitudes and periods of these stress-responsive genes in stress and non-stress conditions. In Arabidopsis thaliana intraspecific hybrids, genome-wide expression of many biotic and abiotic stress-responsive genes was diurnally repressed to promote biomass heterosis, which is associated with several biomass quantitative trait loci (QTLs). Expression differences in four selected stress-responsive genes among ten ecotypes could be used to predict heterosis in their hybrids. Parent plants with larger expression differences between stress-responsive genes produced higher-vigor hybrids, while those with smaller differences produced lower-vigor hybrids. Stress-responsive genes were epigenetically repressed in the hybrids under normal conditions but induced during times of stress at certain times of the day, balancing the tradeoff between stress responses and growth. Consistently, repressing the stress genes in diploids increased growth vigor. We demonstrate how hybrids manipulate diurnal stress-responsive gene expression to enhance growth vigor. Both circadian and epigenetic regulation play key roles in the altered expression of stress-responsive genes in hybrids. Our findings provide a conceptual advance and mechanistic understanding of heterosis, as well as selection criteria for parents to be effectively used for producing high-yield hybrids. Examination of gene expression in Arabidopsis thaliana F1 hybrids between Col and C24 and 3 time points using mRNA-seq

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Genomic architecture of biomass heterosis in Arabidopsis

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