Comparative Transcriptional Profiling and Preliminary Study on Heterosis Mechanism of Super-Hybrid Rice

Song, Gui Sheng; Zhai, Hong; Peng, Yong; Zhang, Lei; Wei, Gang; Chen, Xiao Ying; Xiao, Yu; Wang, Lili; Chen, Yue Jun; Wu, Bin; Chen, Bin; Zhang, Yu; Chen, Hua; Feng, Xiu; Gong, Wan; Liu, Yao; Yin, Zhi; Wang, Zhen; Liu, Guo Zhen; Xu, Hong; Xiao, Wei; Zhao, Xiao Ling; Ouwerkerk, Pieter B.F.; Hankemeier, Thomas; Reijmers, Theo H.; Heijden, Rob van der; Lu, Cong; Wang, Mei; Greef, J. van der; Zhu, Zhen

doi:10.1093/mp/ssq046

Cited by 113 publications

(114 citation statements)

References 69 publications

(98 reference statements)

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“…Previous studies of heterosis have revealed possible mechanisms to account for the increased vigor, but the mechanisms that underlie this complex phenotype are still poorly understood, and the role of DNA methylation in heterosis is unclear (26)(27)(28)(29). Our results suggest that the majority of gene-expression changes in hybrids are not associated with cis-acting DNA methylation changes, and instead indicate that trans effects may mediate the majority of the transcriptional differences in hybrid offspring.…”

Section: Resultsmentioning

confidence: 58%

Transcriptome and methylome interactions in rice hybrids

Chodavarapu

Feng

Ding

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

196

180

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DNA methylation is a heritable epigenetic mark that controls gene expression, is responsive to environmental stresses, and, in plants, may also play a role in heterosis. To determine the degree to which DNA methylation is inherited in rice, and how it both influences and is affected by transcription, we performed genome-wide measurements of these patterns through an integrative analysis of bisulfite-sequencing, RNA-sequencing, and siRNA-sequencing data in two inbred parents of the Nipponbare (NPB) and indica (93-11) varieties of rice and their hybrid offspring. We show that SNPs occur at a rate of about 1∕253 bp between the two parents and that these are faithfully transmitted into the hybrids. We use the presence of these SNPs to reconstruct the two chromosomes in the hybrids according to their parental origin. We found that, unlike genetic inheritance, epigenetic heritability is quite variable. Cytosines were found to be differentially methylated (epimutated) at a rate of 7.48% (1∕15 cytosines) between the NPB and 93-11 parental strains. We also observed that 0.79% of cytosines were epimutated between the parent and corresponding hybrid chromosome. We found that these epimutations are often clustered on the chromosomes, with clusters representing 20% of all epimutations between parental ecotypes, and 2-5% in F1 plants. Epimutation clusters are also strongly associated with regions where the production of siRNA differs between parents. Finally, we identified genes with both allele-specific expression patterns that were strongly inherited as well as those differentially expressed between hybrids and the corresponding parental chromosome. We conclude that much of the misinheritance of expression levels is likely caused by epimutations and trans effects.bioinformatics | plant biology D NA methylation is an epigenetic mark that can often lead to the repression of gene expression (1, 2). It is enriched in heterochromatin and, when present at regulatory sites, usually acts as a repressor of expression, most notably in transposons (3). However, it is also found over coding regions, where it likely does not directly affect transcription and is associated with moderately expressed genes (2, 4-6). In plants, DNA methylation occurs in three different contexts: CG, CHG, and CHH (where H is any nucleotide but G). In Arabidopsis, each context is maintained by different enzymes: MET1 for CG sites, CMT3 for CHG sites and DRM2 for CHH sites. CG and CHG sites are symmetric across the two DNA strands, which is thought to be important for the maintenance of methylation at these sites following DNA replication. In contrast, CHH sites are not symmetric, and their methylation is mediated by RNA-directed DNA methylation pathways (RdDM), which use siRNAs to initiate de novo methylation (3). Cellular methylation states tend to persist during cell division, and recent studies in Arabidopsis have also shown that DNA methylation is faithfully inherited across generations (7,8). Nonetheless, we are only beginning to understand how different...

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Section: Resultsmentioning

confidence: 58%

Transcriptome and methylome interactions in rice hybrids

Chodavarapu

Feng

Ding

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

196

180

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“…Notably, the association of increased biomass with CCA1 repression during the day has been independently demonstrated in Arabidopsis intraspecific hybrids (Miller et al, 2012;Shen et al, 2012). In superhybrid rice (Oryza sativa), yield-related quantitative trait loci are also associated with gene expression changes in the circadian clock and light signaling pathways (Song et al, 2010). Moreover, downregulation of CCA1 expression during the day in Arabidopsis diploids leads to more starch at dusk and increased biomass, a phenotype similar to that seen in the hybrids (Ni et al, 2009).…”

Section: Introductionmentioning

confidence: 83%

A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis inArabidopsisIntraspecific Hybrids

Miller

et al. 2014

The Plant Cell

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Hybrid plants and animals often show increased levels of growth and fitness, a phenomenon known as hybrid vigor or heterosis. Circadian rhythms optimize physiology and metabolism in plants and animals. In plant hybrids and polyploids, expression changes of the genes within the circadian regulatory network, such as CIRCADIAN CLOCK ASSOCIATED1 (CCA1), lead to heterosis. However, the relationship between allelic CCA1 expression and heterosis has remained elusive. Here, we show a parent-of-origin effect on altered circadian rhythms and heterosis in Arabidopsis thaliana F1 hybrids. This parent-of-origin effect on biomass heterosis correlates with altered CCA1 expression amplitudes, which are associated with methylation levels of CHH (where H = A, T, or C) sites in the promoter region. The direction of rhythmic expression and hybrid vigor is reversed in reciprocal F1 crosses involving mutants that are defective in the RNA-directed DNA methylation pathway (argonaute4 and nuclear RNA polymerase D1a) but not in the maintenance methylation pathway (methyltransferase1 and decrease in DNA methylation1). This parent-of-origin effect on circadian regulation and heterosis is established during early embryogenesis and maintained throughout growth and development.

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“…The difference in expression of genes encoding PHYA and PHYB (Si033984, Si033968) between the hybrid and female was not significant. However, no DEG encoding any phytochromes was found in a study by Song et al (2010), although circadian clock genes were also downregulated in hybrid rice. This indicates that the causes of differential expression of circadian clock genes are complex.…”

Section: Discussionmentioning

confidence: 84%

“…Wei et al (2009) investigated transcriptome profiles of superhybrid rice LYP9 and its parental cultivars 93-11and PA64s in 7 tissues and identified 3926 DEGs as a potential group of heterosis-related genes. Song et al (2010) found 1183 DEGs to be significantly enriched in pathways such as photosynthesis and carbon-fixation, and most key genes involved in the carbon-fixation pathway exhibited up-regulated expression in F 1 hybrid rice. Qin et al (2013), provided a repertoire of genes useful for identifying genes involved in maize ear trait heterosis.…”

Section: Introductionmentioning

confidence: 99%

An expression profiling analysis of hybrid millet and its parents at grain filling stage

Liu¹,

Zhang²,

Li³

et al. 2015

Genet. Mol. Res.

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ABSTRACT. Heterosis has been widely used in crop breeding and production. However, a shortage of genes known to function in heterosis significantly limits our understanding of the molecular basis underlying heterosis. Here, we report 740 differentially expressed genes (DEGs) in the leaves of the hybrid millet Zhang No.5 and its parents at the grain filling stage determined using Solexa Illumina digital gene expression. Of the 740 DEGs, 546 were from the hybrid and its parents and most were up-regulated in the hybrid. Particularly, a large number of DEGs related to starch and carbohydrate metabolism and 2 DEGs encoding chlorophyll a/b binding proteins were up-regulated in hybrid millet. Moreover, all DEGs were enriched in the biological process and molecular function, and no DEGs were found to be enriched in the cellular component of GO terms. Pathway enrichment using KEGG showed that several DEGs were enriched in the circadian rhythm pathway. Further analysis revealed that the altered circadian rhythm, which mediates photosynthesis and carbohydrate accumulation, may play an important role in heterosis of the hybrid millet.

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Comparative Transcriptional Profiling and Preliminary Study on Heterosis Mechanism of Super-Hybrid Rice

Cited by 113 publications

References 69 publications

Transcriptome and methylome interactions in rice hybrids

Transcriptome and methylome interactions in rice hybrids

A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis inArabidopsisIntraspecific Hybrids

An expression profiling analysis of hybrid millet and its parents at grain filling stage

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