Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid

被引:140
作者
Caarls, Lotte [1 ,3 ]
Elberse, Joyce [1 ]
Awwanah, Mo [1 ]
Ludwig, Nora R. [1 ]
de Vries, Michel [2 ]
Zeilmaker, Tieme [1 ,4 ]
Van Wees, Saskia C. M. [1 ]
Schuurink, Robert C. [2 ]
Van den Ackerveken, Guido [1 ]
机构
[1] Univ Utrecht, Dept Biol, Plant Microbe Interact, NL-3508 TB Utrecht, Netherlands
[2] Univ Amsterdam, Swammerdam Inst Life Sci, Dept Plant Physiol, NL-1098 XH Amsterdam, Netherlands
[3] Wageningen Univ, Biosystemat Grp, NL-6708 PB Wageningen, Netherlands
[4] SciENZA Biotechnol, NL-1098 XH Amsterdam, Netherlands
关键词
jasmonic acid; 2OG oxygenases; 12-OH-JA; plant defense; BHLH TRANSCRIPTION FACTORS; L-ISOLEUCINE; CATABOLISM; RESPONSES; DIOXYGENASE; OXIDATION; ACCUMULATION; ACTIVATION; REPRESSORS; INFECTION;
D O I
10.1073/pnas.1701101114
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The phytohormone jasmonic acid (JA) is vital in plant defense and development. Although biosynthesis of JA and activation of JA-responsive gene expression by the bioactive form JA-isoleucine have been well-studied, knowledge on JA metabolism is incomplete. In particular, the enzyme that hydroxylates JA to 12-OH-JA, an inactive form of JA that accumulates after wounding and pathogen attack, is unknown. Here, we report the identification of four paralogous 2-oxoglutarate/Fe(II)-dependent oxygenases in Arabidopsis thaliana as JA hydroxylases and show that they down-regulate JA-dependent responses. Because they are induced by JA we named them JASMONATE-INDUCED OXYGENASES (JOXs). Concurrent mutation of the four genes in a quadruple Arabidopsis mutant resulted in increased defense gene expression and increased resistance to the necrotrophic fungus Botrytis cinerea and the caterpillar Mamestra brassicae. In addition, root and shoot growth of the plants was inhibited. Metabolite analysis of leaves showed that loss of function of the four JOX enzymes resulted in overaccumulation of JA and in reduced turnover of JA into 12-OH-JA. Transformation of the quadruple mutant with each JOX gene strongly reduced JA levels, demonstrating that all four JOXs inactivate JA in plants. The in vitro catalysis of 12-OH-JA from JA by recombinant enzyme could be confirmed for three JOXs. The identification of the enzymes responsible for hydroxylation of JA reveals a missing step in JA metabolism, which is important for the inactivation of the hormone and subsequent down-regulation of JA-dependent defenses.
引用
收藏
页码:6388 / 6393
页数:6
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