Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid
Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid
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DOI：
10.1073/pnas.1701101114
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发表时间：
2017-06-13
影响因子：
11.1
通讯作者：
Van den Ackerveken, Guido
中科院分区：
文献类型：
--
作者：
Caarls, Lotte;Elberse, Joyce;Van den Ackerveken, Guido
植物激素茉莉酸（jasmonic acid， JA）在植物防御和发育中起着至关重要的作用。虽然生物活性形式JA-异亮氨酸对JA的生物合成和JA响应基因表达的激活已经得到了很好的研究，但对JA代谢的了解尚不完整。特别是，将JA羟基化成12-OH-JA的酶是未知的，这是一种在损伤和病原体攻击后积累的JA的非活性形式。在这里，我们报道了在拟南芥中鉴定出四种相邻的2-氧戊二酸/铁（II）依赖的加氧酶作为JA羟化酶，并表明它们下调JA依赖的反应。由于它们是由茉莉酸诱导的，我们将其命名为茉莉酸诱导氧合酶（JASMONATE-INDUCED OXYGENASES, JOXs）。在一个四重拟南芥突变体中，这四个基因同时突变，导致防御基因表达增加，对坏死性真菌灰霉病菌和芸苔螟的抗性增强。此外，还抑制了植株的根和茎的生长。叶片代谢物分析表明，四种JOX酶的功能丧失导致JA的过度积累和JA转化为12-OH-JA的减少。每个JOX基因的四重突变体的转化强烈降低了JA水平，表明所有四个JOX基因都使植物中的JA失活。重组酶对JA的12-OH-JA的体外催化作用可以证实为三个jox。对JA羟基化酶的鉴定揭示了JA代谢中缺失的一个步骤，这对于激素的失活和随后的JA依赖性防御的下调是重要的。
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.