Regulation of metabolic gene clusters in <i>Arabidopsis thaliana</i>

Nützmann, Hans-Wilhelm; Osbourn, Anne

doi:10.1111/nph.13189

Cited by 56 publications

(53 citation statements)

References 45 publications

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“…Expression was consistently down-regulated in the hta9/hta11 double mutant, which is mutated in two of the three H2A.Z genes (44), which was also found to be associated with metabolic cluster activation (11,12), but not in any other mutant. Thus, we next investigated the hta9/hta11 mutant in more depth: we assayed the expression of all GOIs as well as the flanking genes of these clusters (Supplemental Figure S12B).…”

Section: Resultsmentioning

confidence: 99%

Genome-wide identification of physically clustered genes suggests chromatin-level co-regulation in male reproductive development in Arabidopsis thaliana

Reimegård

Kundu

Pendle

et al. 2017

Nucleic Acids Research

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Co-expression of physically linked genes occurs surprisingly frequently in eukaryotes. Such chromosomal clustering may confer a selective advantage as it enables coordinated gene regulation at the chromatin level. We studied the chromosomal organization of genes involved in male reproductive development in Arabidopsis thaliana. We developed an in-silico tool to identify physical clusters of co-regulated genes from gene expression data. We identified 17 clusters (96 genes) involved in stamen development and acting downstream of the transcriptional activator MS1 (MALE STERILITY 1), which contains a PHD domain associated with chromatin re-organization. The clusters exhibited little gene homology or promoter element similarity, and largely overlapped with reported repressive histone marks. Experiments on a subset of the clusters suggested a link between expression activation and chromatin conformation: qRT-PCR and mRNA in situ hybridization showed that the clustered genes were up-regulated within 48 h after MS1 induction; out of 14 chromatin-remodeling mutants studied, expression of clustered genes was consistently down-regulated only in hta9/hta11, previously associated with metabolic cluster activation; DNA fluorescence in situ hybridization confirmed that transcriptional activation of the clustered genes was correlated with open chromatin conformation. Stamen development thus appears to involve transcriptional activation of physically clustered genes through chromatin de-condensation.

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Section: Resultsmentioning

confidence: 99%

Genome-wide identification of physically clustered genes suggests chromatin-level co-regulation in male reproductive development in Arabidopsis thaliana

Reimegård

Kundu

Pendle

et al. 2017

Nucleic Acids Research

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“…This inhibitory mechanism is mediated by the deposition of H2A.Z at a set of anthocyanin biosynthesis genes, including TT3 , TT4 , TT5 , TT6 and TT7 . H2A.Z can regulate the expression of gene clusters (Wong & Wolfe, ; Nutzmann & Osbourn, ), as well as a whole gene family whose members are highly conserved but distributed throughout the genome (Cai et al ., ). Here, we showed that H2A.Z‐containing nucleosomes can also mediate the chromatin‐level regulation of multiple genes in a key plant metabolic pathway.…”

Section: Discussionmentioning

confidence: 99%

Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A.Z and H3K4me3

et al. 2018

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The accumulation of anthocyanins in response to specific developmental cues or environmental conditions plays a vital role in plant development and protection against stresses. Extensive research has examined the regulation of anthocyanin biosynthetic genes at the transcriptional and post-transcriptional levels, but the role of chromatin in this regulation remains unknown. Chromatin immunoprecipitation and quantitative reverse transcription-polymerase chain reaction (qRT-PCR) analyses were performed. Genetic interactions between trimethylation of lysine 4 on histone H3 (H3K4me3) and the chromatin remodeling complex SWR1 in the control of anthocyanin biosynthesis were further studied. In this study, we provide evidence that a conserved histone H2 variant, H2A.Z, negatively regulates anthocyanin accumulation through deposition at a set of anthocyanin biosynthetic genes and consequently represses their expression in Arabidopsis thaliana. Our data indicate that the accumulation of anthocyanin in H2A.Z deposition-deficient mutants is associated with increased H3K4me3, which is required for promotion of the expression of anthocyanin biosynthetic genes. We further provide evidence that H3K4me3 in anthocyanin biosynthetic genes is negatively associated with the presence of H2A.Z. Our results reveal an antagonistic relationship between H2A.Z and H3K4me3 in the regulation of the expression of anthocyanin biosynthesis genes, adding another layer of regulation to anthocyanin biosynthesis genes and highlighting the role of chromatin in gene regulation.

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“…Recent work in Arabidopsis has revealed gene cluster‐specific signatures of chromatin modification that are associated with localized, coordinated regulation of the component genes. Specifically, metabolic clusters have been found to be enriched for histone 3 lysine trimethylation (H3K27me3) and histone 2 variant H2A.Z, which are associated with cluster repression and activation, respectively (Nützmann & Osbourn, ; Yu et al ., ). These same chromatin modification signatures also were detected in metabolic gene clusters of maize and oat, suggesting that chromatin‐mediated co‐regulation may be a general phenomenon for at least some classes of metabolic cluster.…”

Section: Discussionmentioning

confidence: 99%

Micro‐ and macroevolutionary adaptation through repeated loss of a complete metabolic pathway

Olsen

Small

2018

New Phytologist

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There is growing evidence for the convergent evolution of physically linked gene clusters encoding chemical defense pathways. Metabolic clusters are proposed to evolve because they ensure co-inheritance of all required genes where the defense is favored, and prevent inheritance of toxic partial pathways where it is not. This hypothesis rests on the assumption that clusters evolve in species where selection favors intraspecific polymorphism for the defense; however, they have not been examined in polymorphic species. We examined metabolic cluster evolution in relation to an adaptive polymorphism for cyanogenic glucoside (CNglc) production in clover. Using 163 accessions, we performed CNglc assays, BAC sequencing, Southern hybridizations and molecular evolutionary analyses. We find that the CNglc pathway forms a 138-kb cluster in white clover, and that the adaptive polymorphism occurs through presence/absence of the complete cluster. Component genes are orthologous to those in the distantly related legume Lotus japonicus. These findings provide empirical support for the co-inheritance hypothesis, and they indicate that adaptive CNglc variation in white clover evolves through recurrent deletions of the entire pathway. They further indicate that the shared ancestor of many important legume crops was likely cyanogenic and that this defense was lost repeatedly over the last 50 Myr.

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Regulation of metabolic gene clusters in Arabidopsis thaliana

Cited by 56 publications

References 45 publications

Genome-wide identification of physically clustered genes suggests chromatin-level co-regulation in male reproductive development in Arabidopsis thaliana

Genome-wide identification of physically clustered genes suggests chromatin-level co-regulation in male reproductive development in Arabidopsis thaliana

Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A.Z and H3K4me3

Micro‐ and macroevolutionary adaptation through repeated loss of a complete metabolic pathway

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