The Mitogen-Activated Protein Kinase Cascade MKK3–MPK6 Is an Important Part of the Jasmonate Signal Transduction Pathway in <i>Arabidopsis</i>

Takahashi, Fumiyuki; Yoshida, Riku; Ichimura, Kazuya; Mizoguchi, Tsuyoshi; Seo, Shigemi; Yonezawa, Masahiro; Maruyama, Kyonoshin; Yamaguchi-Shinozaki, Kazuko; Shinozaki, Kazuo

doi:10.1105/tpc.106.046581

Cited by 351 publications

(314 citation statements)

References 59 publications

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“…Further support for this positive feedback loop is the observation that transient overexpression of an active form of MKK4 increases HAE expression twofold (Fig. 6B) (26).…”

Section: Strong Overexpression Of Agl15 Leads To Delay Of Abscission Andmentioning

confidence: 82%

Floral organ abscission is regulated by a positive feedback loop

Patharkar

Walker

2015

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

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Abscission is the process by which plants shed unwanted organs, either as part of a natural developmental program or in response to environmental stimuli. Studies in Arabidopsis thaliana have elucidated a number of the genetic components that regulate abscission of floral organs, including a pair of related receptor-like protein kinases, HAESA and HAESA-like 2 (HAE/HSL2) that regulate a MAP kinase cascade that is required for abscission. HAE is transcriptionally up-regulated in the floral abscission zone just before cell separation. Here, we identify AGAMOUS-like 15 (AGL15; a MADS-domain transcription factor) as a putative regulator of HAE expression. Overexpression of AGL15 results in decreased expression of HAE as well as a delayed abscission phenotype. Chromatin immunoprecipitation experiments indicate that AGL15 binds the HAE promoter in floral receptacles. AGL15 is then differentially phosphorylated through development in floral receptacles in a MITOGEN-ACTIVATED PROTEIN KINASE KINASE 4/5-dependent manner. MAP kinase phosphorylation of AGL15 is necessary for full HAE expression, thus completing a positive feedback loop controlling HAE expression. Together, the network components in this positive feedback loop constitute an emergent property that regulates the large dynamic range of gene expression (27-fold increase in HAE) observed in flowers when the abscission program is initiated. This study helps define the mechanisms and regulatory networks involved in a receptor-mediated signaling pathway that controls floral organ abscission.A bscission is the process that plants use to shed unwanted organs. Various plants can abscise leaves, fruits, and flowers. One of the most noticeable abscission events occurs when deciduous trees and shrubs shed their leaves in the fall. Plants can abscise organs as part of a developmental program or in an inducible manner in response to stimuli like abiotic or biotic stress. For example, tomatoes can abscise leaves and flowers in response to drought or insect feeding (1-3). In order for abscission to occur, a layer of small and cytoplasmically dense cells, known as an abscission zone, must be laid down during development at the boundary between the organ to be abscised and the body of the plant (4).Arabidopsis thaliana has been used to elucidate a number of the molecular and genetic components that regulate abscission of floral organs. In Arabidopsis, floral organs abscise shortly after pollination, which corresponds to stage-16 flowers or approximately floral position 4-6, where anthesis is defined as position 1 and older flowers are defined as increasing numerical positions ( Fig. 1 A and B) (5). A number of genetic components regulating this abscission process have been described thoroughly in recent reviews (6, 7). In brief, a pair of related receptor-like protein kinases, HAESA and HAESA-like 2 (HAE/HSL2), are required for floral abscission (Fig. 1C) and are thought to be triggered by a peptide derived from INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) (8, 9). A mitogen-act...

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“…Further support for this positive feedback loop is the observation that transient overexpression of an active form of MKK4 increases HAE expression twofold (Fig. 6B) (26).…”

Section: Strong Overexpression Of Agl15 Leads To Delay Of Abscission Andmentioning

confidence: 82%

Floral organ abscission is regulated by a positive feedback loop

Patharkar

Walker

2015

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

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“…S1A, S4C, and S11), suggesting their importance in ABA-and JA-regulated processes in Brassicaceae species. Notably, MPK3 and/or MPK6 are activated by ABA and JA and are implicated in ABA-and JA-regulated developmental and stress responses in A. thaliana (46,47). Thus, transcriptional activation of the HAI PP2Cs may provide fitness advantages as regulatory modules of ABA-and JA-signaling pathways for controlling intensity and timing of MPK3/MPK6 activation in A. thaliana and possibly in other Brassicaceae species, and it is sometimes exploited by pathogens.…”

Section: Discussionmentioning

confidence: 99%

Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

Mine

Berens

Nobori

et al. 2017

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

108

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Phytopathogens promote virulence by, for example, exploiting signaling pathways mediated by phytohormones such as abscisic acid (ABA) and jasmonate (JA). Some plants can counteract pathogen virulence by invoking a potent form of immunity called effector-triggered immunity (ETI). Here, we report that ABA and JA mediate inactivation of the immune-associated MAP kinases (MAPKs), MPK3 and MPK6, in Arabidopsis thaliana. ABA induced expression of genes encoding the protein phosphatases 2C (PP2Cs), HAI1, HAI2, and HAI3 through ABF/AREB transcription factors. These three HAI PP2Cs interacted with MPK3 and MPK6 and were required for ABA-mediated MPK3/MPK6 inactivation and immune suppression. The bacterial pathogen Pseudomonas syringae pv. tomato (Pto) DC3000 activates ABA signaling and produces a JAmimicking phytotoxin, coronatine (COR), that promotes virulence. We found that Pto DC3000 induces HAI1 through COR-mediated activation of MYC2, a master transcription factor in JA signaling. HAI1 dephosphorylated MPK3 and MPK6 in vitro and was necessary for COR-mediated suppression of MPK3/MPK6 activation and immunity. Intriguingly, upon ETI activation, A. thaliana plants overcame the HAI1-dependent virulence of COR by blocking JA signaling. Finally, we showed conservation of induction of HAI PP2Cs by ABA and JA in other Brassicaceae species. Taken together, these results suggest that ABA and JA signaling pathways, which are hijacked by the bacterial pathogen, converge on the HAI PP2Cs that suppress activation of the immune-associated MAPKs. Also, our data unveil interception of JA-signaling activation as a host counterstrategy against the bacterial suppression of MAPKs during ETI.MAPK phosphatase | abscisic acid | jasmonate | coronatine | effector-triggered immunity

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“…Finally, we identified a component in the putative phosphorylation cascade that stimulates expression of a nicotine synthesis gene, namely a MAPKK protein, encoded by JAM1. Also in Arabidopsis, MAPK cascades are key relays of the respective JA signal transduction pathways and are involved in the control of MYC2 expression amongst others (Brader et al, 2007;Takahashi et al, 2007;Qiu et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

APETALA2/ETHYLENE RESPONSE FACTOR and basic helix–loop–helix tobacco transcription factors cooperatively mediate jasmonate‐elicited nicotine biosynthesis

et al. 2011

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SUMMARYTranscription factors of the plant-specific apetala2/ethylene response factor (AP2/ERF) family control plant secondary metabolism, often as part of signalling cascades induced by jasmonate (JA) or other elicitors. Here, we functionally characterized the JA-inducible tobacco (Nicotiana tabacum) AP2/ERF factor ORC1, one of the members of the NIC2-locus ERFs that control nicotine biosynthesis and a close homologue of ORCA3, a transcriptional activator of alkaloid biosynthesis in Catharanthus roseus. ORC1 positively regulated the transcription of several structural genes coding for the enzymes involved in nicotine biosynthesis. Accordingly, overexpression of ORC1 was sufficient to stimulate alkaloid biosynthesis in tobacco plants and tree tobacco (Nicotiana glauca) root cultures. In contrast to ORCA3 in C. roseus, which needs only the GCC motif in the promoters of the alkaloid synthesis genes to induce their expression, ORC1 required the presence of both GCC-motif and G-box elements in the promoters of the tobacco nicotine biosynthesis genes for maximum transactivation. Correspondingly, combined application with the JA-inducible Nicotiana basic helix-loop-helix (bHLH) factors that bind the G-box element in these promoters enhanced ORC1 action. Conversely, overaccumulation of JAZ repressor proteins that block bHLH activity reduced ORC1 functionality. Finally, the activity of both ORC1 and bHLH proteins was post-translationally upregulated by a JA-modulated phosphorylation cascade, in which a specific mitogen-activated protein kinase kinase, JA-factor stimulating MAPKK1 (JAM1), was identified. This study highlights the complexity of the molecular machinery involved in the regulation of tobacco alkaloid biosynthesis and provides mechanistic insights about its transcriptional regulators.

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The Mitogen-Activated Protein Kinase Cascade MKK3–MPK6 Is an Important Part of the Jasmonate Signal Transduction Pathway in Arabidopsis

Cited by 351 publications

References 59 publications

Floral organ abscission is regulated by a positive feedback loop

Floral organ abscission is regulated by a positive feedback loop

Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

APETALA2/ETHYLENE RESPONSE FACTOR and basic helix–loop–helix tobacco transcription factors cooperatively mediate jasmonate‐elicited nicotine biosynthesis

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