The chromatin remodeler DDM1 promotes hybrid vigor by regulating salicylic acid metabolism

Zhang, Qingzhu; Li, Yanqiang; Xu, Tao; Srivastava, Ashish Kumar; Wang, Dong; Zeng, Liang; He, Li; Zhang, Heng; Zheng, Zhimin; Yang, Donglei; Zhao, Cheng; Dong, Juan; Gong, Zhizhong; Liu, Renyi; Zhu, Jian‐Kang

doi:10.1038/celldisc.2016.27

Cited by 53 publications

(64 citation statements)

References 57 publications

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“…The direction of the change in expression is opposite. We hypothesize that, depending on the parent combinations, the level of a particular gene product associated with heterosis may be different (Zhang et al, 2016a). In FT QTL interval 3_2, we identified a down-regulated candidate gene, encoding EMBRYO DEFECTIVE1703, in the same three epiHybrids.…”

Section: Identification Of Putative Loci Mediating Hybrid Performancementioning

confidence: 81%

“…Prior studies on Arabidopsis heterotic hybrids identified candidate genes underlying heterotic phenotypes in pathways of the circadian clock, flavonoid biosynthesis, auxin transport, or salicylic acid metabolism and response (Ni et al, 2009;Shen et al, 2012;Groszmann et al, 2015;Zhang et al, 2016a). A Gene Ontology analysis on differentially expressed genes in a met1-derived epiHybrid did not show an overrepresentation of particular gene categories; however, the study proposed a gene (RECOGNITION OF PERONOSPORA PARASITICA5) within an epigenetically regulated resistance gene cluster to be a possible candidate (Dapp et al, 2015).…”

Section: Discussionmentioning

confidence: 98%

“…Most studies focused on a biomass-related trait in the vegetative growth phase (i.e. plant fresh/dry weight, leaf width, LA; Ni et al, 2009;Shen et al, 2012;Groszmann et al, 2015;Zhang et al, 2016a), which can be compared with the LA trait measured here. Nonetheless, we did not identify an epigenetic QTL for LA, apart from the suggestive pleiotropic effect of the FT heterosis QTLs on LA.…”

Section: Discussionmentioning

confidence: 99%

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Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

et al. 2017

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Despite the importance and wide exploitation of heterosis in commercial crop breeding, the molecular mechanisms behind this phenomenon are not completely understood. Recent studies have implicated changes in DNA methylation and small RNAs in hybrid performance; however, it remains unclear whether epigenetic changes are a cause or a consequence of heterosis. Here, we analyze a large panel of over 500 Arabidopsis (Arabidopsis thaliana) epigenetic hybrid plants (epiHybrids), which we derived from near-isogenic but epigenetically divergent parents. This proof-of-principle experimental system allowed us to quantify the contribution of parental methylation differences to heterosis. We measured traits such as leaf area, growth rate, flowering time, main stem branching, rosette branching, and final plant height and observed several strong positive and negative heterotic phenotypes among the epiHybrids. Using an epigenetic quantitative trait locus mapping approach, we were able to identify specific differentially methylated regions in the parental genomes that are associated with hybrid performance. Sequencing of methylomes, transcriptomes, and genomes of selected parent-epiHybrid combinations further showed that these parental differentially methylated regions most likely mediate the remodeling of methylation and transcriptional states at specific loci in the hybrids. Taken together, our data suggest that locus-specific epigenetic divergence between the parental lines can directly or indirectly trigger heterosis in Arabidopsis hybrids independent of genetic changes. These results add to a growing body of evidence that points to epigenetic factors as one of the key determinants of hybrid performance.

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Section: Identification Of Putative Loci Mediating Hybrid Performancementioning

confidence: 81%

Section: Discussionmentioning

confidence: 98%

Section: Discussionmentioning

confidence: 99%

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Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

et al. 2017

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“…It is possible that the developmental defects associated with protracted DDM1 deficiency may not only reflect misregulation of development-specific genes, but also the consequences of a metastable genome (Ronemus et al 1996; Zhang et al 2016). The RAM is extraordinarily sensitive to DNA damage, and undergoes PCD in response to genotoxic stress (Fulcher and Sablowski 2009).…”

Section: Discussionmentioning

confidence: 99%

DDM1 guards against telomere truncation in Arabidopsis

Xie

Shippen

2018

Plant Cell Rep

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Epigenetic pathways, including DNA methylation, are crucial for telomere maintenance. Deficient in DNA Methylation 1 (DDM1) encodes a nucleosome remodeling protein, required to maintain DNA methylation in Arabidopsis thaliana. Plants lacking DDM1 can be self-propagated, but in the sixth generation (G6) hypomethylation leads to rampant transposon activation and infertility. Here we examine the role of DDM1 in telomere length homeostasis through a longitudinal study of successive generations of ddm1-2 mutants. We report that bulk telomere length remains within the wild-type range for the first five generations (G1–G5), and then precipitously drops in G6. While telomerase activity becomes more variable in later generation ddm1-2 mutants, there is no correlation between enzyme activity and telomere length. Plants lacking DDM1 also exhibit no dysregulation of several known telomere-associated transcripts, including TERRA. Instead, telomere shortening coincides with increased G-overhangs and extra-chromosomal circles, consistent with deletional recombination. Telomere shortening also correlates with transcriptional activation of retrotransposons, and a hypersensitive DNA damage response in root apical meristems. Since abiotic stresses, including DNA damage, stimulate homologous recombination, we hypothesize that telomere deletion in G6 ddm1-2 mutants is a by-product of elevated genome-wide recombination in response to trans-poson mobilization. Further, we speculate that telomere truncation may be beneficial in adverse environmental conditions by accelerating the elimination of stem cells with aberrant genomes.

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“…In Columbia-0 (Col)/C24 hybrids, an active copy of the chromatin remodeler DECREASE IN DNA METHYLATION (DDM1), which affects DNA methylation in all sequence contexts, is required for a wild-type level of heterosis, whereas the alterations in gene expression produced by transchromosomal methylation via the RNA-directed DNA methylation (RdDM) pathway do not appear to contribute to hybrid vigor (28,29).…”

Section: Discussionmentioning

confidence: 99%

PIF4-controlled auxin pathway contributes to hybrid vigor in Arabidopsis thaliana

Wang

Greaves

et al. 2017

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

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F1 hybrids in Arabidopsis and crop species are uniform and high yielding. The F2 generation loses much of the yield advantage and the plants have heterogeneous phenotypes. We generated pure breeding hybrid mimic lines by recurrent selection and also selected a pure breeding small phenotype line. The hybrid mimics are almost completely homozygous with chromosome segments from each parent. Four particular chromosomal segments from C24 and 8 from Ler were present in all of the hybrid mimic lines, whereas in the F6 small phenotype line, the 12 segments were each derived from the alternative parent. Loci critical for promoting hybrid vigor may be contained in each of these 12 conserved segments. We have identified genes with similar altered expression in hybrid mimics and F1 plants but not in the small phenotype line. These genes may be critical for the generation of hybrid vigor. Analysis of transcriptomes indicated that increased expression of the transcription factor PHYTOCHROME-INTERACTING FACTOR (PIF4) may contribute to hybrid vigor by targeting the auxin biosynthesis gene YUCCA8 and the auxin signaling gene IAA29. A number of auxin responsive genes promoting leaf growth were up-regulated in the F1 hybrids and hybrid mimics, suggesting that increased auxin biosynthesis and signaling contribute to the hybrid phenotype. The hybrid mimic seeds had earlier germination as did the seeds of the F1 hybrids, indicating cosegregation of the genes for rosette size and the germination trait. Early germination may be an indicator of vigorous hybrids.heterosis | transcription factor | biomass | transregulation | germination T wo features common to hybrids in many crops are the increased yield and phenotypic uniformity of the F1 hybrid generation and the reduced yield and phenotypic heterogeneity of the F2 generation (1). These characteristics also apply to the F1 and F2 populations in Arabidopsis hybrids (2). The processes of capture of light and assimilation of CO 2 into photosynthate are the same in the hybrid and parents and as the hybrids have larger leaves than their parents, they produce more photosynthate (3).In a previous paper (2), transcriptome analyses showed that in the hybrids, most genes are expressed at the same levels as in the parents. Compared with the average level of gene expression in the parents, ∼2,000 genes (6% of the genome) have altered expression in the hybrids and are likely to be involved in the generation of the hybrid vigor phenotype. Many of the differentially expressed genes (DEGs) encode proteins in key metabolic pathways such as the plant hormone systems auxin and salicylic acid (SA) and the basal defense response, suggesting that these pathways contribute to the development of hybrid vigor (4). Altered hormone abscisic acid (ABA) and defense response have also been reported in rice hybrids (5). Despite the contrasting phenotypes of the F1 and F2 populations, we were able to develop "pure breeding" F5/F6 lines with phenotypes comparable to the F1 hybrids (hybrid mimics) (2). The hybrid mimic...

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The chromatin remodeler DDM1 promotes hybrid vigor by regulating salicylic acid metabolism

Cited by 53 publications

References 57 publications

Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

DDM1 guards against telomere truncation in Arabidopsis

PIF4-controlled auxin pathway contributes to hybrid vigor in Arabidopsis thaliana

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