Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth

Virdi, Kamaldeep S.; Laurie, John D.; Xu, Ying; Yu, Jinxin; Shao, Mon Ray; Sanchez, Robersy; Kundariya, Hardik; Wang, Dong; Riethoven, Jean-Jack M.; Wamboldt, Yashitola; Arrieta-Montiel, Maria P.; Shedge, Vikas; Mackenzie, Sally A.

doi:10.1038/ncomms7386

Cited by 91 publications

(134 citation statements)

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“…New mitochondrial genes may provide unique sources of genetic variation that have phenotypic consequences. These consequences can benefit natural adaptation and prove useful for crop breeding [10,42,[49][50][51]. In addition, the new CMS genes identified in this study could greatly expand the germplasm for hybrid rice breeding.…”

Section: Discussionmentioning

confidence: 96%

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Tang

Zheng

et al. 2016

Cell Res

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New gene origination is a major source of genomic innovations that confer phenotypic changes and biological diversity. Generation of new mitochondrial genes in plants may cause cytoplasmic male sterility (CMS), which can promote outcrossing and increase fitness. However, how mitochondrial genes originate and evolve in structure and function remains unclear. The rice Wild Abortive type of CMS is conferred by the mitochondrial gene WA352c (previously named WA352) and has been widely exploited in hybrid rice breeding. Here, we reconstruct the evolutionary trajectory of WA352c by the identification and analyses of 11 mitochondrial genomic recombinant structures related to WA352c in wild and cultivated rice. We deduce that these structures arose through multiple rearrangements among conserved mitochondrial sequences in the mitochondrial genome of the wild rice Oryza rufipogon, coupled with substoichiometric shifting and sequence variation. We identify two expressed but nonfunctional protogenes among these structures, and show that they could evolve into functional CMS genes via sequence variations that could relieve the self-inhibitory potential of the proteins. These sequence changes would endow the proteins the ability to interact with the nucleus-encoded mitochondrial protein COX11, resulting in premature programmed cell death in the anther tapetum and male sterility. Furthermore, we show that the sequences that encode the COX11-interaction domains in these WA352c-related genes have experienced purifying selection during evolution. We propose a model for the formation and evolution of new CMS genes via a "multi-recombination/protogene formation/functionalization" mechanism involving gradual variations in the structure, sequence, copy number, and function.

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Section: Discussionmentioning

confidence: 96%

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Tang

Zheng

et al. 2016

Cell Res

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“…A total of 50% of (40). Selection of F4 lines derived from this cross show enhanced growth, suggesting that altered epigenetic states can influence the potential for growth to produce vigor-like characteristics (40,41).…”

Section: Discussionmentioning

confidence: 99%

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

Greaves

Eichten

Groszmann

et al. 2016

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

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Hybrid Arabidopsis plants undergo epigenetic reprogramming producing decreased levels of 24-nt siRNAs and altered patterns of DNA methylation that can affect gene expression. Driving the changes in methylation are the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM). In TCM/TCdM the methylation state of one allele is altered to resemble the other allele. We show that Pol IV-dependent sRNAs are required to establish TCM events. The changes in DNA methylation and the associated changes in sRNA levels in the F1 hybrid can be maintained in subsequent generations and affect hundreds of regions in the F2 epigenome. The inheritance of these altered epigenetic states varies in F2 individuals, resulting in individuals with genetically identical loci displaying different epigenetic states and gene expression profiles. The change in methylation at these regions is associated with the presence of sRNAs. Loci without any sRNA activity can have altered methylation states, suggesting that a sRNA-independent mechanism may also contribute to the altered methylation state of the F1 and F2 generations.H ybrid vigor, heterosis, is important in agriculture due to the increased performance of hybrid plants over parental lines. The increase in performance is attributable to changes in gene expression (1, 2) but how these changes result in the increased performance of the hybrid is still not known. The level of hybrid vigor is believed to correlate with the genetic distance between parental lines; however, hybrid vigor can occur in progeny derived from crosses of genetically similar parents. An example is found in intraspecific crosses between Arabidopsis thaliana accessions. In crosses between C24 and Landsberg erecta (Ler), up to a 100% increase in plant biomass and seed yield is observed (3). The different epigenomes of the two parental accessions could provide the diversity required to initiate gene expression changes and vigor-related characteristics. A number of laboratories have investigated whether there are epigenetic changes in Arabidopsis hybrids, whether they affect gene expression, and whether they contribute to the hybrid vigor phenotype (1, 3-6).We have previously established that F1 hybrids between Arabidopsis accessions undergo some epigenetic reprogramming. We found that the abundance of 24-nt siRNAs is reduced in F1 hybrids and that a second epigenetic system, DNA methylation ( m C), is also altered in the hybrid genome (1, 3, 5). The altered m C patterns in the hybrids involve the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM), where the m C state of one parental allele is altered to resemble the other allele (reviewed in ref. 7). Due to the presence of siRNAs at regions that undergo TCM/TCdM, we have suggested that siRNAs are the initiating molecules that establish these TCM/TCdM events (reviewed in ref. 8). In the hybrid nucleus, the complement of 24-nt siRNAs can interact with homologous sequences from either parent.The TCM and TCdM...

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“…The msh1 mutant is markedly altered in growth rate, branching behavior, flowering time, juvenility-maturity growth transition, perennial growth behavior, and abiotic stress response (Xu et al, 2012). This developmental reprogramming (DR) is accompanied by altered genome methylation, with the intensity of the altered phenotype showing an apparent association with an enhanced non-CG hypermethylation of pericentromeric genomic intervals (Virdi et al, 2015). This complex DR phenotype has been recapitulated in several crop species, both monocot and dicot, by RNA interference (RNAi) suppression of MSH1, prompting changes in growth rate, tillering, flowering time, leaf morphology, and abiotic stress tolerance (Xu et al, 2012).…”

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confidence: 99%

MutS HOMOLOG1-Derived Epigenetic Breeding Potential in Tomato

Yang

Kundariya

et al. 2015

Plant Physiol.

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Evidence is compelling in support of a naturally occurring epigenetic influence on phenotype expression in land plants, although discerning the epigenetic contribution is difficult. Agriculturally important attributes like heterosis, inbreeding depression, phenotypic plasticity, and environmental stress response are thought to have significant epigenetic components, but unequivocal demonstration of this is often infeasible. Here, we investigate gene silencing of a single nuclear gene, MutS HOMOLOG1 (MSH1), in the tomato (Solanum lycopersicum) 'Rutgers' to effect developmental reprogramming of the plant. The condition is heritable in subsequent generations independent of the MSH1-RNA interference transgene. Crossing these transgene-null, developmentally altered plants to the isogenic cv Rutgers wild type results in progeny lines that show enhanced, heritable growth vigor under both greenhouse and field conditions. This boosted vigor appears to be graft transmissible and is partially reversed by treatment with the methylation inhibitor 5-azacytidine, implying the influence of mobile, epigenetic factors and DNA methylation changes. These data provide compelling evidence for the feasibility of epigenetic breeding in a crop plant.

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Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth

Cited by 91 publications

References 43 publications

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

MutS HOMOLOG1-Derived Epigenetic Breeding Potential in Tomato

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