Developmental transitions: integrating environmental cues with hormonal signaling in the chromatin landscape in plants

Xiao, Jun; Jin, Run; Wagner, Doris

doi:10.1186/s13059-017-1228-9

Cited by 56 publications

(34 citation statements)

References 159 publications

(170 reference statements)

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“…Reprogramming of the epigenome is an integral part of development and environmental stimulus-induced gene expression (Feng et al, 2010, Xiao et al, 2017). For example, activation of the transcriptional JA response requires the formation of MYC2/MED25-mediated chromatin looping (Wang et al, 2019).…”

Section: Resultsmentioning

confidence: 99%

Integrated Multi-omic Framework of the Plant Response to Jasmonic Acid

Zander

Lewsey

Clark

et al. 2019

Preprint

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27Understanding the systems-level actions of transcriptional responses to hormones provides 28 insight into how the genome is reprogrammed in response to environmental stimuli. Here, we 29 investigate the signaling pathway of the hormone jasmonic acid (JA), which controls a plethora of 30 critically important processes in plants and is orchestrated by the transcription factor MYC2 and 31 its closest relatives in Arabidopsis thaliana. We generated an integrated framework of the 32 response to JA that spans from the activity of master and secondary-regulatory transcription 33 factors, through gene expression outputs and alternative splicing to protein abundance changes, 34 protein phosphorylation and chromatin remodeling. We integrated time series transcriptome 35 analysis with (phospho)proteomic data to reconstruct gene regulatory network models. These 36 enable us to predict previously unknown points of crosstalk from JA to other signaling pathways 37 and to identify new components of the JA regulatory mechanism, which we validated through 38 targeted mutant analysis. These results provide a comprehensive understanding of how a plant 39 hormone remodels cellular functions and plant behavior, the general principles of which provide 40 a framework for analysis of cross-regulation between other hormone and stress signaling 41 pathways. 42 43 44 45 46 47 48 49 50 51 52 5 2004, Fernandez-Calvo et al. , 2011). myc3 and myc4 single mutants behave like wildtype with 104 regards to JA-induced root growth inhibition. However, in combination with the myc2 mutant, 105 myc2 myc3 double mutants exhibit an increased JA hyposensitivity, almost as pronounced as in 106 myc2 myc3 myc4 triple mutants (Fernandez-Calvo et al., 2011). We consequently selected MYC3 107 for an in-depth analysis. 108In order to better understand how the master TFs MYC2 and MYC3 control the JA-109 induced transcriptional cascade, we determined their genome-wide binding sites using chromatin 110 immunoprecipitation sequencing (ChIP-seq). Four biological replicates of JA-treated (2 hours) 111 three-day-old etiolated Arabidopsis seedlings that express a native promoter-driven and epitope 112 (YPet)-tagged version of MYC2 and three biological replicates of MYC3 (Col-0 MYC2::MYC2-113 Ypet, Col-0 MYC3::MYC3-Ypet) were used (Gimenez-Ibanez et al., 2017). The genome-wide 114distributions of MYC2 and MYC3 binding sites were highly similar (Fig. 1c, d). We identified 6,736 115 MYC2 and 3,982 MYC3 binding sites of high confidence, equating to 6,178 MYC2 and 4,092

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Section: Resultsmentioning

confidence: 99%

Integrated Multi-omic Framework of the Plant Response to Jasmonic Acid

Zander

Lewsey

Clark

et al. 2019

Preprint

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“…Growth and photosynthesis in female poplars were affected via a clear leaf area decrease during drought [55]. Furthermore, in Arabidopsis, leaf differentiation and consequently leaf area is controlled through AtRRA16 activation by the complex of the chromatin remodeler BRM and TCP4 CIN-TCP leading to CK decrease [56,57]. It seems that type A RRs could be involved in sex-specific drought response (AtRRA17) or leaf development and leaf area control (AtRRA16).…”

Section: Discussionmentioning

confidence: 99%

Highlighting type A RRs as potential regulators of the dkHK1 multi-step phosphorelay pathway in Populus

Chefdor¹,

Héricourt²,

Κουδούνας³

et al. 2018

Plant Science

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In previous studies, we highlighted a multistep phosphorelay (MSP) system in poplars composed of two hybridtype Histidine aspartate Kinases, dkHK1a and dkHK1b, which interact with three Histidine Phosphotransfer proteins, dkHPt2, 7, and 9, which in turn interact with six type B Response Regulators. These interactions correspond to the dkHK1a-b/dkHPts/dkRRBs MSP. This MSP is putatively involved in an osmosensing pathway, as dkHK1a-b are orthologous to the Arabidopsis osmosensor AHK1, and able to complement a mutant yeast deleted for its osmosensors. Since type A RRs have been characterized as negative regulators in cytokinin MSP signaling due to their interaction with HPt proteins, we decided in this study to characterize poplar type A RRs and their implication in the MSP. For a global view of this MSP, we isolated 10 poplar type A RR cDNAs, and determined their subcellular localization to check the in silico prediction experimentally. For most of them, the in planta subcellular localization was as predicted, except for three RRAs, for which this experimental approach gave a more precise localization. Interaction studies using yeast two-hybrid and in planta BiFC assays, together with transcript expression analysis in poplar organs led to eight dkRRAs being singled out as partners which could interfere the dkHK1a-b/dkHPts/dkRRBs MSP identified in previous studies. Consequently, the results obtained in this study now provide an exhaustive view of dkHK1a-b partners belonging to a poplar MSP. 1. Introduction Living organisms are exposed to fluctuating environmental conditions, and in the context of global climatic change, those with efficient perception mechanisms will be able to adapt more efficiently. To sense and respond to environmental stimuli, prokaryotic organisms, such as bacteria, employ a well characterized signaling pathway, the canonical two component system (TCS). This system is specific to the stimuli and is comprised of a sensor protein corresponding to a Histidine Kinase and a Response Regulator (RR) [1]. A more elaborate system is also found in prokaryotic and eukaryotic organisms, which involves a His-Asp-His-Asp phosphorelay called a multistep phosphorelay (MSP) system. The system is comprised of sensors, RRs, and a histidine phosphotransfer protein (HPt), which shuttles between them [2]. In plants, the MSP comprises a receptor, a hybrid-type histidine aspartate kinase (HK), HPt proteins, and four types of RR: type A, type B, type C, and pseudo RRs. These signaling pathways are known to mediate plant responses to light, abiotic stresses, and phytohormones such as cytokinin (CK) and ethylene, which regulate growth and plant development [3-7]. The CK pathway is the most studied and characterized MSP in plants. In Arabidopsis, CK receptors AHK2, AHK3 and AHK4 activated by CK binding can autophosphorylate and trigger a phosphorelay involving five HPt proteins (AHP1-5), and 11 type B RRs (AtRRB1-2, AtRRB10-14, AtRRB18-21), which once activated by phosphorylation can activate the transcription of target g...

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“…In contrast to Drosophila, few PRE-like cis-regulatory elements have been characterized in plants (Berger et al, 2011;Förderer et al, 2016;Xiao et al, 2017;Zhou et al, 2018) and mammals (Woo et al, 2010;Schorderet et al, 2013). Furthermore, nucleosome-free and hypomethylated CpG islands in gene regulatory regions were found to act as PRC2 recruitment sites in mammals (Mendenhall et al, 2010;Lynch et al, 2012;Klose et al, 2013;Riising et al, 2014;Højfeldt et al, 2018;Oksuz et al, 2018).…”

Section: A Change Of Paradigm? the Genomic Bookmarking Hypothesismentioning

confidence: 99%

Mitotic Inheritance of PRC2-Mediated Silencing: Mechanistic Insights and Developmental Perspectives

2020

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Maintenance of gene repression by Polycomb Repressive Complex 2 (PRC2) that catalyzes the trimethylation of histone H3 at lysine 27 (H3K27me3) is integral to the orchestration of developmental programs in most multicellular eukaryotes. Faithful inheritance of H3K27me3 patterns across replication ensures the stability of PRC2mediated transcriptional silencing over cell generations, thereby safeguarding cellular identities. In this review, we discuss the molecular and mechanistic principles that underlie H3K27me3 restoration after the passage of the replication fork, considering recent advances in different model systems. In particular, we aim at emphasizing parallels and differences between plants and other organisms, focusing on the recycling of parental histones and the replenishment of H3K27me3 patterns post-replication thanks to the remarkable properties of the PRC2 complex. We then discuss the necessity for fine-tuning this genuine epigenetic memory system so as to allow for cell fate and developmental transitions. We highlight recent insights showing that genome-wide destabilization of the H3K27me3 landscape during chromatin replication participates in achieving this flexible stability and provides a window of opportunity for subtle transcriptional reprogramming.

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Developmental transitions: integrating environmental cues with hormonal signaling in the chromatin landscape in plants

Cited by 56 publications

References 159 publications

Integrated Multi-omic Framework of the Plant Response to Jasmonic Acid

Integrated Multi-omic Framework of the Plant Response to Jasmonic Acid

Highlighting type A RRs as potential regulators of the dkHK1 multi-step phosphorelay pathway in Populus

Mitotic Inheritance of PRC2-Mediated Silencing: Mechanistic Insights and Developmental Perspectives

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