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Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense.
Plant Physiol. 2018 01; 176(1):511-523.PP

Abstract

Damaged cells send various signals to stimulate defense responses. Recent identification and genetic studies of the plant purinoceptor, P2K1 (also known as DORN1), have demonstrated that extracellular ATP is a signal involved in plant stress responses, including wounding, perhaps to evoke plant defense. However, it remains largely unknown how extracellular ATP induces plant defense responses. Here, we demonstrate that extracellular ATP induces plant defense mediated through activation of the intracellular signaling of jasmonate (JA), a well-characterized defense hormone. In Arabidopsis (Arabidopsis thaliana) leaves, ATP pretreatment induced resistance against the necrotrophic fungus, Botrytis cinerea The induced resistance was enhanced in the P2K1 receptor overexpression line, but reduced in the receptor mutant, dorn1-3 Mining the transcriptome data revealed that ATP induces a set of JA-induced genes. In addition, the P2K1-associated coexpression network contains defense-related genes, including those encoding jasmonate ZIM-domain (JAZ) proteins, which play key roles as repressors of JA signaling. We examined whether extracellular ATP impacts the stability of JAZ1 in Arabidopsis. The results showed that the JAZ1 stability decreased in response to ATP addition in a proteasome-dependent manner. This reduction required intracellular signaling via second messengers-cytosolic calcium, reactive oxygen species, and nitric oxide. Interestingly, the ATP-induced JAZ1 degradation was attenuated in the JA receptor mutant, coi1, but not in the JA biosynthesis mutant, aos, or upon addition of JA biosynthesis inhibitors. Immunoprecipitation analysis demonstrated that ATP increases the interaction between COI1 and JAZ1, suggesting direct cross talk between extracellular ATP and JA in intracellular signaling events. Taken together, these results suggest that extracellular ATP signaling directly impacts the JA signaling pathway to maximize plant defense responses.

Authors+Show Affiliations

Department of Plant Pathology, Washington State University, Pullman, Washington 99164.Divisions of Plant Sciences and Biochemistry, University of Missouri, Columbia, Missouri 65211.Divisions of Plant Sciences and Biochemistry, University of Missouri, Columbia, Missouri 65211.Divisions of Plant Sciences and Biochemistry, University of Missouri, Columbia, Missouri 65211.Department of Plant Pathology, Washington State University, Pullman, Washington 99164 kiwamu.tanaka@wsu.edu.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29180381

Citation

Tripathi, Diwaker, et al. "Extracellular ATP Acts On Jasmonate Signaling to Reinforce Plant Defense." Plant Physiology, vol. 176, no. 1, 2018, pp. 511-523.
Tripathi D, Zhang T, Koo AJ, et al. Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense. Plant Physiol. 2018;176(1):511-523.
Tripathi, D., Zhang, T., Koo, A. J., Stacey, G., & Tanaka, K. (2018). Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense. Plant Physiology, 176(1), 511-523. https://doi.org/10.1104/pp.17.01477
Tripathi D, et al. Extracellular ATP Acts On Jasmonate Signaling to Reinforce Plant Defense. Plant Physiol. 2018;176(1):511-523. PubMed PMID: 29180381.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Extracellular ATP Acts on Jasmonate Signaling to Reinforce Plant Defense. AU - Tripathi,Diwaker, AU - Zhang,Tong, AU - Koo,Abraham J, AU - Stacey,Gary, AU - Tanaka,Kiwamu, Y1 - 2017/11/27/ PY - 2017/10/10/received PY - 2017/11/22/accepted PY - 2017/11/29/pubmed PY - 2018/8/15/medline PY - 2017/11/29/entrez SP - 511 EP - 523 JF - Plant physiology JO - Plant Physiol VL - 176 IS - 1 N2 - Damaged cells send various signals to stimulate defense responses. Recent identification and genetic studies of the plant purinoceptor, P2K1 (also known as DORN1), have demonstrated that extracellular ATP is a signal involved in plant stress responses, including wounding, perhaps to evoke plant defense. However, it remains largely unknown how extracellular ATP induces plant defense responses. Here, we demonstrate that extracellular ATP induces plant defense mediated through activation of the intracellular signaling of jasmonate (JA), a well-characterized defense hormone. In Arabidopsis (Arabidopsis thaliana) leaves, ATP pretreatment induced resistance against the necrotrophic fungus, Botrytis cinerea The induced resistance was enhanced in the P2K1 receptor overexpression line, but reduced in the receptor mutant, dorn1-3 Mining the transcriptome data revealed that ATP induces a set of JA-induced genes. In addition, the P2K1-associated coexpression network contains defense-related genes, including those encoding jasmonate ZIM-domain (JAZ) proteins, which play key roles as repressors of JA signaling. We examined whether extracellular ATP impacts the stability of JAZ1 in Arabidopsis. The results showed that the JAZ1 stability decreased in response to ATP addition in a proteasome-dependent manner. This reduction required intracellular signaling via second messengers-cytosolic calcium, reactive oxygen species, and nitric oxide. Interestingly, the ATP-induced JAZ1 degradation was attenuated in the JA receptor mutant, coi1, but not in the JA biosynthesis mutant, aos, or upon addition of JA biosynthesis inhibitors. Immunoprecipitation analysis demonstrated that ATP increases the interaction between COI1 and JAZ1, suggesting direct cross talk between extracellular ATP and JA in intracellular signaling events. Taken together, these results suggest that extracellular ATP signaling directly impacts the JA signaling pathway to maximize plant defense responses. SN - 1532-2548 UR - https://www.unboundmedicine.com/medline/citation/29180381/Extracellular_ATP_Acts_on_Jasmonate_Signaling_to_Reinforce_Plant_Defense_ L2 - http://www.plantphysiol.org/lookup/pmidlookup?view=long&pmid=29180381 DB - PRIME DP - Unbound Medicine ER -