MYC2 Orchestrates a Hierarchical Transcriptional Cascade That Regulates Jasmonate-Mediated Plant Immunity in Tomato

Du, Minmin; Zhao, Jiuhai; Tzeng, David T.W.; Liu, Yuanyuan; Deng, Lijun; Yang, Tianxia; Zhai, Qingzhe; Wu, Fangming; Huang, Zhuo; Zhou, Ming; Wang, Qiaomei; Chen, Qian; Zhong, Silin; Li, Chang Bao; Li, Chuanyou

doi:10.1105/tpc.16.00953

Cited by 265 publications

(297 citation statements)

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“…1c and Supplementary Table 4). MYCs initiate various feed forward loops that allow a rapid activation of the transcriptional JA response (Du et al, 2017, Liu et al, 2019). Our ChIP-seq approach revealed that besides the autoregulation of MYC2 and MYC3, they also regulate JA biosynthesis either indirectly through binding to the AP2-ERF transcription factor gene ORA47 (Chen et al, 2016a) or directly by targeting the JA biosynthesis genes LOX2 and AOS2 (Supplementary Table 4).…”

Section: Resultsmentioning

confidence: 99%

“…This results in degradation of JAZ repressors and permits the activity of a master regulatory bHLH transcription factor MYC2, accompanied by MYC3, MYC4, MYC5 and numerous other transcription factors, all of which have distinct but overlapping roles in driving JA-responsive gene expression (Song et al, 2017, Schweizer et al, 2013b, Fernandez-Calvo et al, 2011, Lorenzo et al, 2004, Bao et al, 2019). The result is a cascade of JA-induced genome reprogramming to modulate plant behavior such as plant immune responses (Du et al, 2017, Hickman et al, 2017). However, our knowledge of the JA-responsive genome regulatory program and, more broadly, in the plants general response to environmental stimuli is limited currently by assessment of only one or a small number of components.…”

Section: Introductionmentioning

confidence: 99%

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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%

Section: Introductionmentioning

confidence: 99%

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

Zander

Lewsey

Clark

et al. 2019

Preprint

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“…The JA signalling pathway plays a critical role in improving plant resistance to fungus, such as Botrytis cinerea , Alternaria brassicicola , Fusarium oxysporum and Plectosphaerella cucumerina (Du et al., ; Yan & Xie, ). If the JA pathway is blocked, endogenous jasmonate does not accumulate.…”

Section: Discussionmentioning

confidence: 99%

“…The JA signalling pathway plays a critical role in improving plant resistance to fungus, such as Botrytis cinerea, Alternaria brassicicola, Fusarium oxysporum and Plectosphaerella cucumerina (Du et al, 2017;Yan & Xie, 2015 in both positive controls and in the BSMV:TaCOI1 group, the leaves were crinkled (Fig. S3).…”

Section: Early Response Is Important For Plant Resistancementioning

confidence: 99%

A COI1 gene in wheat contributes to the early defence response against wheat powdery mildew

Wang

Fan

et al. 2017

Journal of Phytopathology

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The hormone jasmonate (JA) signalling pathway is involved in diverse developmental processes in plants. COI1 is a key regulator in JA pathway. Although COI1 homologous proteins have been identified in a variety of crops, their regulatory mechanisms in wheat defence responses remain unknown. Here, we cloned COI1 from disease resistant wheat Brock, designated TaCOI1. TaCOI1 cDNA was 1988‐bp long, with an ORF encoding 593 deduced amino acids. The phylogenetic tree showed that TaCOI1 was clustered in the same clade of monocotyledons. The predicted protein possesses an F‐box domain, several LRRs and a conserved AMN1 domain. Its transcription was induced in the compatible and incompatible wheat by Blumeria graminis f. sp. tritici (Bgt) fungus, with differences observed in response time. Expression pattern analysis in the susceptible wheat variety Jing411 revealed that TaCOI1 was up‐regulated after Bgt inoculation at 12‐hour postinoculation (hpi). While, in Brock its transcription was rapidly induced and reached a first peak at 2 hpi. These results suggest that TaCOI1 may be involved in the early response to powdery mildew. The expression of TaCOI1 was decreased by virus‐induced gene silencing. The rate of successful penetration by Bgt was higher in all TaCOI1‐silenced Brock, while the percentage of macrocephalic appressoria and resistance reactions was lower than control. These results suggest that silencing of the TaCOI1 gene increased Brock susceptibility to infection. Together, these findings indicate that the TaCOI1 gene could be involved in the early defence response against wheat powdery mildew and may play an important role in wheat–Bgt interactions.

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“…Although the function of AT3G19970 has not been fully characterised, GO terms have been associated with it via identification of functional gene modules 118 lycopersicum is Solyc02g020890 ( Supplementary Fig. 3t); Solyc02g020890 was among 4774 genes in tomato whose expression was significantly affected by application of methyl jasmonate 171 . Table 5).…”

Section: Candidates Found In F Mandshurica and Resistant Taxa In Secmentioning

confidence: 99%

Genes for ash tree resistance to an insect pest identified via comparative genomics

Plumb

Dw³

et al. 2019

Preprint

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Genome-wide discovery of candidate genes for functional traits within a species typically involves the sequencing of large samples of phenotyped individuals 1 , or linkage analysis through multiple generations 2 . When a trait occurs repeatedly among phylogenetically independent lineages within a genus, a more efficient approach may be to identify genes via detection of amino acid residues shared by species possessing that trait 3,4 . Here, by taking this approach, we identify candidate loci in the genus Fraxinus (ash trees) for resistance to the emerald ash borer beetle (EAB; Agrilus planipennis), a pest species that appears innocuous to otherwise healthy ash in its native East Asian range 5 but is highly destructive in North America 6 and poses a threat to ash trees in Europe 7 . Assembling whole genome sequences for 24 diploid species and subspecies of ash, and estimating resistance to EAB for 26 taxa from egg bioassays, we find 53 genes containing amino acid variants shared between two or more independent Fraxinus lineages with EABresistant species, that are unlikely to be due to chance or undetected paralogy. Of these, seven genes have putative roles relating to the phenylpropanoid biosynthesis pathway and 17 are potentially connected to herbivore recognition, defence signalling or programmed cell death. We also find that possible loss-of-function mutations among our 53 candidate genes are more frequent in susceptible species, 2 than in resistant ones. Patterns of polymorphism for the EAB-associated amino acid variants in ash trees representing different European populations suggest that selection may be able to enhance their resistance to EAB.

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MYC2 Orchestrates a Hierarchical Transcriptional Cascade That Regulates Jasmonate-Mediated Plant Immunity in Tomato

Cited by 265 publications

References 72 publications

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

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

A COI1 gene in wheat contributes to the early defence response against wheat powdery mildew

Genes for ash tree resistance to an insect pest identified via comparative genomics

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