The plastidial retrograde signal methyl erythritol cyclopyrophosphate is a regulator of salicylic acid and jasmonic acid crosstalk

Lemos, Mark; Xiao, Yanmei; Bjornson, Marta; Wang, Jinzheng; Hicks, Derrick R.; Souza, Amancio de; Wang, Changquan; Dinesh, P.; Ma, Shisong; Dinesh‐Kumar, Savithramma P.; Dehesh, Katayoon

doi:10.1093/jxb/erv550

Cited by 55 publications

(66 citation statements)

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“…These results indicate that an increased expression of genes in the SA‐signalling pathway induced through an elevation of the MEcPP level does not interfere with the caterpillar‐induced expression of genes in the JA‐signalling pathway or with resistance to P. brassicae caterpillars. Moreover, our results are consistent with previous studies that a high SA level did neither attenuate transcript expression of genes in the JA‐signalling pathway nor the accumulation of JA in plants with high MEcPP levels, that is, hds3 and ceh1 mutant plants (González‐Cabanelas et al, ; Lemos et al, ). It is noteworthy that ceh1 mutant plants used by Lemos et al () are the result of a point mutation in exon 19 at leucine 703 to phenylalanine (Xiao et al, ), whereas the hds3 mutant plants are generated through a point mutation at glycine 696 to aspartic acid in the same exon (Gil et al, ).…”

Section: Discussionsupporting

confidence: 93%

“…Moreover, our results are consistent with previous studies that a high SA level did neither attenuate transcript expression of genes in the JA‐signalling pathway nor the accumulation of JA in plants with high MEcPP levels, that is, hds3 and ceh1 mutant plants (González‐Cabanelas et al, ; Lemos et al, ). It is noteworthy that ceh1 mutant plants used by Lemos et al () are the result of a point mutation in exon 19 at leucine 703 to phenylalanine (Xiao et al, ), whereas the hds3 mutant plants are generated through a point mutation at glycine 696 to aspartic acid in the same exon (Gil et al, ). Furthermore, ceh1 mutant plants have originally been screened to identify novel genes that control the transcript expression of hydroperoxide lyase ( HPL ), encoding an enzyme in the green‐leaf volatile biosynthesis pathway (Lemos et al, ; Xiao et al, ).…”

Section: Discussionsupporting

confidence: 93%

“…It is noteworthy that ceh1 mutant plants used by Lemos et al () are the result of a point mutation in exon 19 at leucine 703 to phenylalanine (Xiao et al, ), whereas the hds3 mutant plants are generated through a point mutation at glycine 696 to aspartic acid in the same exon (Gil et al, ). Furthermore, ceh1 mutant plants have originally been screened to identify novel genes that control the transcript expression of hydroperoxide lyase ( HPL ), encoding an enzyme in the green‐leaf volatile biosynthesis pathway (Lemos et al, ; Xiao et al, ). Although hds3 plants share various phenotypes with ceh1 plants, the basal expression of HPL in hds3 plants was comparable with the expression in WT plants (Figure S6).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, the transcript expression in hds3 plants of genes involved in JA biosynthesis (AOS), JA response (VSP2), and a JA-inducible gene (ERF1) was equally induced in response to P. brassicae caterpillar feeding as in WT plants (Figure 3d high MEcPP levels, that is, hds3 and ceh1 mutant plants (González-Cabanelas et al, 2015;Lemos et al, 2016). It is noteworthy that ceh1 mutant plants used by Lemos et al (2016) are the result of a point mutation in exon 19 at leucine 703 to phenylalanine (Xiao et al, 2012), whereas the hds3 mutant plants are generated through a point mutation at glycine 696 to aspartic acid in the same exon (Gil et al, 2005). Furthermore, ceh1 mutant plants have originally been FIGURE 6 Relative transcript abundance of selected genes involved in indole glucosinolate metabolism, after Brevicoryne brassicae aphid feeding or after exogenous application of MEcPP.…”

Section: Mecpp Impacts the Expression Of Other Genes Mediating Planmentioning

confidence: 96%

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The plastidial metabolite 2‐C‐methyl‐D‐erythritol‐2,4‐cyclodiphosphate modulates defence responses against aphids

Onkokesung

Reichelt

Wright

et al. 2019

Plant Cell & Environment

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Feeding by insect herbivores such as caterpillars and aphids induces plant resistance mechanisms that are mediated by the phytohormones jasmonic acid (JA) and salicylic acid (SA). These phytohormonal pathways often crosstalk. Besides phytohormones, methyl‐D‐erythriol‐2,4‐cyclodiphosphate (MEcPP), the penultimate metabolite in the methyl‐D‐erythritol‐4‐phosphate pathway, has been speculated to regulate transcription of nuclear genes in response to biotic stressors such as aphids. Here, we show that MEcPP uniquely enhances the SA pathway without attenuating the JA pathway. Arabidopsis mutant plants that accumulate high levels of MEcPP (hds3) are highly resistant to the cabbage aphid (Brevicoryne brassicae), whereas resistance to the large cabbage white caterpillar (Pieris brassicae) remains unaltered. Thus, MEcPP is a distinct signalling molecule that acts beyond phytohormonal crosstalk to induce resistance against the cabbage aphid in Arabidopsis. We dissect the molecular mechanisms of MEcPP mediating plant resistance against the aphid B. brassicae. This shows that MEcPP induces the expression of genes encoding enzymes involved in the biosynthesis of several primary and secondary metabolic pathways contributing to enhanced resistance against this aphid species. A unique ability to regulate multifaceted molecular mechanisms makes MEcPP an attractive target for metabolic engineering in Brassica crop plants to increase resistance to cabbage aphids.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Section: Mecpp Impacts the Expression Of Other Genes Mediating Planmentioning

confidence: 96%

See 2 more Smart Citations

The plastidial metabolite 2‐C‐methyl‐D‐erythritol‐2,4‐cyclodiphosphate modulates defence responses against aphids

Onkokesung

Reichelt

Wright

et al. 2019

Plant Cell & Environment

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“…The ceh1 (constitutively expressing hydroperoxide lyase1) mutant accumulates large quantities of MEcPP and displays various stress-associated phenotypes such as compromised growth, high salicylic acid (SA) content, and constitutive activation of the unfolded protein response (UPR) required for restoration of protein-folding homeostasis in the endoplasmic reticulum (ER) (13)(14)(15). We performed bioinformatic analyses of global microarray expression profiles and identified overrepresentation of the RSRE motif in the promoters of robustly induced genes in the ceh1 mutant, including key UPR-regulatory genes such as the ER membrane-localized inositol-requiring protein-1 (IRE1a) and the transcription factor basic leucine zipper 60 (bZIP60) responsible Significance A dual-function plastidial metabolite, methylerythritol cyclodiphosphate (MEcPP), an intermediate of the plastidial pathway for isoprenoids production and a retrograde signaling metabolite, transduces signals to activate general stress-response (GSR) genes by inducing a transcriptionally centered stress hub.…”

mentioning

confidence: 99%

Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3

Benn

Bjornson

et al. 2016

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

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The general stress response (GSR) is an evolutionarily conserved rapid and transient transcriptional reprograming of genes central for transducing environmental signals into cellular responses, leading to metabolic and physiological readjustments to cope with prevailing conditions. Defining the regulatory components of the GSR will provide crucial insight into the design principles of early stressresponse modules and their role in orchestrating master regulators of adaptive responses. Overaccumulation of methylerythritol cyclodiphosphate (MEcPP), a bifunctional chemical entity serving as both a precursor of isoprenoids produced by the plastidial methylerythritol phosphate (MEP) pathway and a stress-specific retrograde signal, in ceh1 (constitutively expressing hydroperoxide lyase1)-mutant plants leads to large-scale transcriptional alterations. Bioinformatic analyses of microarray data in ceh1 plants established the overrepresentation of a stress-responsive cis element and key GSR marker, the rapid stress response element (RSRE), in the promoters of robustly induced genes. ceh1 plants carrying an established 4×RSRE:Luciferase reporter for monitoring the GSR support constitutive activation of the response in this mutant background. Genetics and pharmacological approaches confirmed the specificity of MEcPP in RSRE induction via the transcription factor CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3), in a calcium-dependent manner. Moreover, CAMTA3-dependent activation of IRE1a (inositol-requiring protein-1) and bZIP60 (basic leucine zipper 60), two RSRE containing unfolded protein-response genes, bridges MEcPP-mediated GSR induction to the potentiation of protein-folding homeostasis in the endoplasmic reticulum. These findings introduce the notion of transcriptional regulation by a key plastidial retrograde signaling metabolite that induces nuclear GSR, thereby offering a window into the role of interorgannellar communication in shaping cellular adaptive responses.S tress-triggered transcriptional reprogramming plays fundamental roles in transducing stress signals and ultimately enabling adaptive responses through readjustments of the appropriate physiological and metabolic processes. The initial transcriptional reprograming known as the "general stress response" (GSR), at times referred to as the "cellular stress response" or "core stress response," is a recognized evolutionarily conserved stress response present across kingdoms (1-5).The GSR, a rapid and transient transcriptional reprogramming, is induced by a wide variety of stresses imposed upon organisms by environmental forces on macromolecules such as membrane lipids, proteins, and/or DNA (6). Bioinformatic analysis of the promoters of the rapid wound-response genes (5 min after mechanical damage) in plants led to the identification of an overrepresented functional cis-element, the rapid stress response element (RSRE), which is analogous to the yeast stress response element (STRE) (4, 7). A reporter line containing luciferase (LUC) driven by a synthet...

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Development of strategies for genetic manipulation and fine‐tuning of a chloroplast retrograde signal 3′‐phosphoadenosine 5′‐phosphate

et al. 2018

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Homeostasis of metabolism and regulation of stress-signaling pathways are important for plant growth. The metabolite 3 0 -phosphoadenosine-5 0 -phosphate (PAP)plays dual roles as a chloroplast retrograde signal during drought and high light stress, as well as a toxic by-product of secondary sulfur metabolism, and thus, its levels are regulated by the chloroplastic phosphatase, SAL1. Constitutive PAP accumulation in sal1 mutants improves drought tolerance but can impair growth and alter rosette morphology. Therefore, it is of interest to derive strategies to enable controlled and targeted PAP manipulation that could enhance drought tolerance while minimizing the negative effects on plant growth. We systematically tested the potential and efficiency of multiple established transgenic manipulation tools in altering PAP levels in Arabidopsis. Dexamethasone (dex)-inducible silencing of SAL1 via hpRNAi [pOpOff:SAL1hpRNAi] yielded reduction in SAL1 transcript and protein levels, yet failed to significantly induce PAP accumulation. Surprisingly, this was not due to insufficient silencing of the inducible system, as constitutive silencing using a strong promoter to drive hpRNAi and amiRNA targeting the SAL1 transcript also failed to increase PAP content or induce a sal1-like plant morphology despite significantly reducing the SAL1 transcript levels. In contrast, using dex-inducible expression of SAL1 cDNA to complement an Arabidopsis sal1 mutant successfully modulated PAP levels and restored rosette growth in a dosage-dependent manner.Results from this inducible complementation system indicate that plants with intermediate PAP levels could have improved rosette growth without compromising its drought tolerance. Additionally, preliminary evidence suggests that SAL1 cDNA driven by promoters of genes expressed specifically during early developmental stages such as ABA-Insensitive 3 (ABI3) could be another potential strategy for studying and optimizing PAP levels and drought tolerance while alleviating the negative impact of PAP on plant growth in sal1. Thus, we have identified ways that can allow future dissection into multiple aspects of stress and developmental regulation mediated by this chloroplast signal.--

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The plastidial retrograde signal methyl erythritol cyclopyrophosphate is a regulator of salicylic acid and jasmonic acid crosstalk

Cited by 55 publications

References 54 publications

The plastidial metabolite 2‐C‐methyl‐D‐erythritol‐2,4‐cyclodiphosphate modulates defence responses against aphids

The plastidial metabolite 2‐C‐methyl‐D‐erythritol‐2,4‐cyclodiphosphate modulates defence responses against aphids

Plastidial metabolite MEcPP induces a transcriptionally centered stress-response hub via the transcription factor CAMTA3

Development of strategies for genetic manipulation and fine‐tuning of a chloroplast retrograde signal 3′‐phosphoadenosine 5′‐phosphate

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