The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism

Shunsuke Watanabe, Mayumi Matsumoto, Yuki Hakomori, Hiroshi Takagi, Hiroshi Shimada, Atsushi Sakamoto

Research output: Contribution to journalArticlepeer-review

73 Scopus citations

Abstract

Purine catabolism is regarded as a housekeeping function that remobilizes nitrogen for plant growth and development. However, emerging evidence suggests that certain purine metabolites might contribute to stress protection of plants. Here, we show that in Arabidopsis, the intermediary metabolite allantoin plays a role in abiotic stress tolerance via activation of abscisic acid (ABA) metabolism. The aln loss-of-function of ALN, encoding allantoinase, results in increased allantoin accumulation, genome-wide up-regulation of stress-related genes and enhanced tolerance to drought-shock and osmotic stress in aln mutant seedlings. This phenotype is not caused by a general response to purine catabolism inhibition, but rather results from a specific effect of allantoin. Allantoin activates ABA production both through increased transcription of NCED3, encoding a key enzyme in ABA biosynthesis, and through post-translational activation via high-molecular-weight complex formation of BG1, a β-glucosidase hydrolysing glucose-conjugated ABA. Exogenous application of allantoin to wild-type plants also activates the two ABA-producing pathways that lead to ABA accumulation and stress-responsive gene expression, but this effect is abrogated in ABA-deficient and BG1-knockout mutants. We propose that purine catabolism functions not only in nitrogen metabolism, but also in stress tolerance by influencing ABA production, which is mediated by the possible regulatory action of allantoin.

Original languageEnglish (US)
Pages (from-to)1022-1036
Number of pages15
JournalPlant, Cell and Environment
Volume37
Issue number4
DOIs
StatePublished - Apr 2014

Keywords

  • ABA-GE
  • Arabidopsis thaliana
  • BG1
  • Metabolic intermediate
  • NCED3
  • Purine catabolism
  • Stress response
  • Ureide

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