A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis in<i>Arabidopsis</i>Intraspecific Hybrids

Ng, David C.; Miller, Marisa E.; Yu, Helen; Huang, Tseng; Kim, Eundeok; Lu, Jie; Xie, Qiguang; McClung, C. Robertson; Chen, Z. Jeffrey

doi:10.1105/tpc.113.115980

Cited by 65 publications

(64 citation statements)

References 68 publications

(119 reference statements)

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“…We propose that over time, 'long-term' adaptation to the local environment results in genetic and epigenetic variations between parents, which is reprogrammed in hybrids to change the expression of circadian regulators 17,48 and stress-responsive genes, and possibly metabolites 42,49 , leading to heterosis. Consistent with the role of epigenetic variation in heterosis 18 , the overall levels of CG, CHG and CHH (H ¼ A, T or C) methylation in many genes, including biotic and abiotic stress-responsive genes (Fig. 6a,b), were generally increased in hybrids compared with parents 48 ( Fig.…”

Section: Diurnal Repression Of Stress-responsive Genes In Hybridssupporting

confidence: 51%

“…1g-k), consistent with previous observations of increased photosynthetic capacity in hybrids 17,31 . Note that gene expression patterns were slightly and consistently different between the reciprocal F1 crosses (also below), which is known to be because of parent-of-origin effects on circadian rhythms and biomass heterosis 18 . These differences were not further investigated in this study.…”

Section: Diurnal Repression Of Stress-responsive Genes In Hybridsmentioning

confidence: 99%

“…Indeed, matching gene expression rhythms with light-dark cycles promotes growth and fitness in plants and animals [14][15][16] and heterosis in Arabidopsis allopolyploids and hybrids 17 . In Arabidopsis thaliana, the RNA-directed DNA methylation pathway mediates a parent-of-origin effect on circadian rhythms, leading to biomass heterosis in reciprocal F1 hybrids 18 . In A. thaliana diploids, the circadian clock regulates abiotic 19,20 and biotic [21][22][23] stress responses.…”

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Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

et al. 2015

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The genetic distance between hybridizing parents affects heterosis; however, the mechanisms for this remain unclear. Here we report that this genetic distance correlates with natural variation and epigenetic regulation of circadian clock-mediated stress responses. In intraspecific hybrids of Arabidopsis thaliana, genome-wide expression of many biotic and abiotic stress-responsive genes is diurnally repressed and this correlates with biomass heterosis and biomass quantitative trait loci. Expression differences of selected stress-responsive genes among diverse ecotypes are predictive of heterosis in their hybrids. Stress-responsive genes are repressed in the hybrids under normal conditions but are induced to mid-parent or higher levels under stress at certain times of the day, potentially balancing the tradeoff between stress responses and growth. Consistent with this hypothesis, repression of two candidate stress-responsive genes increases growth vigour. Our findings may therefore provide new criteria for effectively selecting parents to produce high-or lowyield hybrids.

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Section: Diurnal Repression Of Stress-responsive Genes In Hybridssupporting

confidence: 51%

Section: Diurnal Repression Of Stress-responsive Genes In Hybridsmentioning

confidence: 99%

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confidence: 99%

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Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

et al. 2015

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“…This result is not inconsistent with previous findings. For instance, although F1 hybrids that are defective in RdDM lose the parent-oforigin effects on circadian rhythm, they still display hybrid vigor compared with their parents (38). Greaves et al (7) also described methylation interactions in hybrids.…”

Section: Discussionmentioning

confidence: 99%

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

Zhang

Wang

Lang

et al. 2016

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

105

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DNA methylation is a conserved epigenetic mark in plants and many animals. How parental alleles interact in progeny to influence the epigenome is poorly understood. We analyzed the DNA methylomes of Arabidopsis Col and C24 ecotypes, and their hybrid progeny. Hybrids displayed nonadditive DNA methylation levels, termed methylation interactions, throughout the genome. Approximately 2,500 methylation interactions occurred at regions where parental DNA methylation levels are similar, whereas almost 1,000 were at differentially methylated regions in parents. Methylation interactions were characterized by an abundance of 24-nt small interfering RNAs. Furthermore, dysfunction of the RNA-directed DNA methylation pathway abolished methylation interactions but did not affect the increased biomass observed in hybrid progeny. Methylation interactions correlated with altered genetic variation within the genome, suggesting that they may play a role in genome evolution.D NA methylation is a conserved epigenetic mark in many eukaryotes (1-6). In plants and mammals, DNA methylation plays important roles in genome stability, genomic imprinting, paramutation, and gene regulation during development and diseases (1-6). Parental genetic alleles interact in the filial 1 (F1) progeny in a Mendelian manner. DNA methylation may affect this interaction such that methylated epialleles may show nonadditive interactions. This notion is supported by recent observations that hybridization results in nonadditive changes in the F1 plant DNA methylome (7,8). It has been proposed that genome-wide interactions between parental epialleles in F1 hybrids are critical for hybrid vigor, the superior performance of hybrids compared with their parents (8-13). Epigenome interactions may confer nonadditive transcriptional and epigenetic activities in hybrid offspring compared with the parental lines. In contrast to additive regulation, which leads to midparent value (MPV) levels equal to the average of the two parental lines, nonadditive regulation results in a deviation from the MPV, such that the F1 hybrid resembles the high-or low-expression parent. In addition, nonadditive regulation can be transgressive, which is beyond the range of the parental levels (14).Studies in rice and Arabidopsis have identified nonadditive changes in DNA methylation levels at loci where parental methylation levels are different [differentially methylated regions (DMRs)] (7,8,11,12,15,16). These "methylation interactions" were attributed to two mechanisms, transchromosomal methylation (TCM) and transchromosomal demethylation (TCdM), whereby the methylation level of one parental allele is altered to resemble the methylation level of the other parental allele (7,8,17). At some genomic loci, the transmethylation events in F1 were shown to be inherited to the next generation, as observed for paramutation (17). Nonetheless, a thorough profile of DNA methylation interactions across the whole Arabidopsis genome has yet to be determined. In particular, it remains unclear whether DNA m...

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“…The circadian clock has been implicated as a target for increasing yield (4)(5)(6). Plant circadian clocks comprise multiple interlocked feedback loops (7)(8)(9).…”

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Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa

Xie

Lou

Hermand

et al. 2015

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

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GIGANTEA (GI) was originally identified by a late-flowering mutant in Arabidopsis, but subsequently has been shown to act in circadian period determination, light inhibition of hypocotyl elongation, and responses to multiple abiotic stresses, including tolerance to high salt and cold (freezing) temperature. Genetic mapping and analysis of families of heterogeneous inbred lines showed that natural variation in GI is responsible for a major quantitative trait locus in circadian period in Brassica rapa. We confirmed this conclusion by transgenic rescue of an Arabidopsis gi-201 loss of function mutant. The two B. rapa GI alleles each fully rescued the delayed flowering of Arabidopsis gi-201 but showed differential rescue of perturbations in red light inhibition of hypocotyl elongation and altered cold and salt tolerance. The B. rapa R500 GI allele, which failed to rescue the hypocotyl and abiotic stress phenotypes, disrupted circadian period determination in Arabidopsis. Analysis of chimeric B. rapa GI alleles identified the causal nucleotide polymorphism, which results in an amino acid substitution (S264A) between the two GI proteins. This polymorphism underlies variation in circadian period, cold and salt tolerance, and red light inhibition of hypocotyl elongation. Loss-of-function mutations of B. rapa GI confer delayed flowering, perturbed circadian rhythms in leaf movement, and increased freezing and increased salt tolerance, consistent with effects of similar mutations in Arabidopsis. Collectively, these data suggest that allelic variation of GI-and possibly of clock genes in general-offers an attractive target for molecular breeding for enhanced stress tolerance and potentially for improved crop yield.abiotic stress tolerance | circadian clock | hypocotyl elongation | flowering time | natural variation T he last half-century has seen dramatic increases in agricultural productivity. Despite the approximate doubling in world population since 1964, the proportion with insufficient food has dropped by ∼75%, although ∼1 billion remain underfed, and twice that many suffer from micronutrient deficiencies (1). Predicted growth in population and in per capita consumption will require an estimated doubling of crop production by 2050 (2). However, yield trends for maize, rice, wheat, and soybean-four major crops that currently produce nearly two-thirds of global agricultural calories-are insufficient to achieve this doubling (3). Therefore, there is a pressing need not simply to sustain, but actually to accelerate yield improvement.One strategy to increase yield is to identify genetic variation in plant regulatory networks that limit yield to define targets for programs of marker-assisted (molecular) breeding. The circadian clock has been implicated as a target for increasing yield (4-6). Plant circadian clocks comprise multiple interlocked feedback loops (7-9). There is natural variation in clock function in both weedy and cultivated species (10-15), although few of the genes responsible for these quantitative trait loc...

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

Cited by 65 publications

References 68 publications

Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

Methylation interactions in Arabidopsis hybrids require RNA-directed DNA methylation and are influenced by genetic variation

Allelic polymorphism of GIGANTEA is responsible for naturally occurring variation in circadian period in Brassica rapa

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