Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner

Hiroshi Takagi, Yasuhiro Ishiga, Shunsuke Watanabe, Tomokazu Konishi, Mayumi Egusa, Nobuhiro Akiyoshi, Takakazu Matsuura, Izumi Mori, Takashi Hirayama, Hironori Kaminaka, Hiroshi Shimada, Atsushi Sakamoto

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

Allantoin is a metabolic intermediate of purine catabolism that often accumulates in stressed plants. Recently, we used Arabidopsis knockout mutants (aln) of ALLANTOINASE to show that this purine metabolite activates abscisic acid (ABA) production, thereby stimulating stress-related gene expression and enhancing seedling tolerance to abiotic stress. A detailed re-examination of the microarray data of an aln mutant (aln-1) confirmed the increased expression of ABA-related genes and also revealed altered expression of genes involved in jasmonic acid (JA) responses, probably under the control of MYC2, a master switch in the JA signaling pathway. Consistent with the transcriptome profiles, the aln-1 mutant displayed increased JA levels and enhanced responses to mechanical wounding and exogenous JA. Moreover, aln mutants demonstrated modestly increased susceptibility to Pseudomonas syringae and Pectobacterium carotovorum, probably reflecting the antagonistic action of MYC2 on the defense against these bacterial phytopathogens. Exogenously administered allantoin elicited the expression of JA-responsive genes, including MYC2, in wild-type plants, supporting the idea that allantoin might be responsible for the observed JA-related phenotypes of aln mutants. However, mutants deficient in bioactive JA (jar1-1), insensitive to JA (myc2-3), or deficient in ABA (aba2-1 and bglu18) suppressed the effect of exogenous allantoin. The suppression was further confirmed in aln-1 jar1-1 and aln-1 bglu18 double mutants. These results indicate that allantoin can activate the MYC2-regulated JA signaling pathway through ABA production. Overall, this study suggests a possible connection of purine catabolism with stress hormone homeostasis and signaling, and highlights the potential importance of allantoin in these interactions.

Original languageEnglish
Pages (from-to)2519-2532
Number of pages14
JournalJournal of Experimental Botany
Volume67
Issue number8
DOIs
Publication statusPublished - Apr 1 2016

Fingerprint

Allantoin
allantoin
Abscisic Acid
jasmonic acid
purines
abscisic acid
metabolites
mutants
Pectobacterium carotovorum
Pseudomonas syringae
Gene Expression
gene expression
metabolism
knockout mutants
purine
Seedlings
Transcriptome
Arabidopsis
transcriptome
plant pathogens

Keywords

  • ABA
  • Arabidopsis
  • JA
  • purine metabolism
  • small metabolite
  • stress hormone
  • stress response
  • ureide

ASJC Scopus subject areas

  • Plant Science
  • Physiology

Cite this

Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner. / Takagi, Hiroshi; Ishiga, Yasuhiro; Watanabe, Shunsuke; Konishi, Tomokazu; Egusa, Mayumi; Akiyoshi, Nobuhiro; Matsuura, Takakazu; Mori, Izumi; Hirayama, Takashi; Kaminaka, Hironori; Shimada, Hiroshi; Sakamoto, Atsushi.

In: Journal of Experimental Botany, Vol. 67, No. 8, 01.04.2016, p. 2519-2532.

Research output: Contribution to journalArticle

Takagi, H, Ishiga, Y, Watanabe, S, Konishi, T, Egusa, M, Akiyoshi, N, Matsuura, T, Mori, I, Hirayama, T, Kaminaka, H, Shimada, H & Sakamoto, A 2016, 'Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner', Journal of Experimental Botany, vol. 67, no. 8, pp. 2519-2532. https://doi.org/10.1093/jxb/erw071
Takagi, Hiroshi ; Ishiga, Yasuhiro ; Watanabe, Shunsuke ; Konishi, Tomokazu ; Egusa, Mayumi ; Akiyoshi, Nobuhiro ; Matsuura, Takakazu ; Mori, Izumi ; Hirayama, Takashi ; Kaminaka, Hironori ; Shimada, Hiroshi ; Sakamoto, Atsushi. / Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner. In: Journal of Experimental Botany. 2016 ; Vol. 67, No. 8. pp. 2519-2532.
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