A family of methyl esterases converts methyl salicylate to salicylic acid in ripening tomato fruit

A family of methyl esterases converts methyl salicylate to salicylic acid in ripening tomato fruit
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DOI:
10.1093/plphys/kiac509
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发表时间:
2022-11-17
期刊:
影响因子:
7.4
通讯作者:
Klee, Harry J.
Klee, Harry J.
中科院分区:
生物学1区
文献类型:
--
作者:
Frick, Elizabeth M.;Sapkota, Manoj;Klee, Harry J.

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水杨酸甲酯具有药用和冬青的强烈风味和香气,这在番茄果实中是不受欢迎的。植物通过多种生物合成途径控制水杨酸甲酯的数量,包括水杨酸的甲基化形成水杨酸甲酯和随后的糖基化以防止水杨酸甲酯的释放。在这里,我们确定了一个番茄甲基酯酶亚分支,水杨酸甲基酯酶1-4,负责水杨酸甲酯的去甲基化,形成水果中的水杨酸。该家族通过靠近2号染色体上高度显著的水杨酸甲酯全基因组关联研究位点而被鉴定出来。双亲本群体的遗传定位研究证实了2号染色体上有一个主要的水杨酸甲酯位点。SlMES1基因敲除系果实的水杨酸甲酯含量显著高于野生型果实(P < 0.05, t检验)。SlMES2、SlMES3和SlMES4的双重和三重突变体比SlMES1的单敲除释放出更多的水杨酸甲酯,但与单突变体相比,在统计学上没有显著差异。异源表达的SlMES1和SlMES3在体外作用于水杨酸甲酯,其中SlMES1对水杨酸甲酯的亲和力高于SlMES3。双亲本群体亲本的基因组结构分析表明,SlMES位点发生了重大重排。对水杨酸甲酯高产和低高产品种的分析表明,SlMES1和SlMES3基因在水杨酸甲酯低产系中表达量最高。MES基因在水杨酸甲酯高产系中均无明显表达。我们得出结论,SlMES基因家族编码的番茄甲基酯酶可以在成熟的番茄果实中将水杨酸甲酯转化为水杨酸。它们通过转化为水杨酸来降低水杨酸甲酯水平的能力是一个有吸引力的育种目标,可以降低对风味有负面影响的物质的水平。一句话总结:在成熟的番茄果实中,一个甲基酯酶家族将水杨酸转化为令人不快的气味挥发性化合物水杨酸甲酯。
Methyl salicylate imparts a potent flavor and aroma described as medicinal and wintergreen that is undesirable in tomato (Solanum lycopersicum) fruit. Plants control the quantities of methyl salicylate through a variety of biosynthetic pathways, including the methylation of salicylic acid to form methyl salicylate and subsequent glycosylation to prevent methyl salicylate emission. Here, we identified a subclade of tomato methyl esterases, SALICYLIC ACID METHYL ESTERASE1-4, responsible for demethylation of methyl salicylate to form salicylic acid in fruits. This family was identified by proximity to a highly significant methyl salicylate genome-wide association study locus on chromosome 2. Genetic mapping studies in a biparental population confirmed a major methyl salicylate locus on chromosome 2. Fruits from SlMES1 knockout lines emitted significantly (P < 0,05, t test) higher amounts of methyl salicylate than wild-type fruits. Double and triple mutants of SlMES2, SlMES3, and SlMES4 emitted even more methyl salicylate than SlMES1 single knockouts-but not at statistically distinguishable levels-compared to the single mutant. Heterologously expressed SlMES1 and SlMES3 acted on methyl salicylate in vitro, with SlMES1 having a higher affinity for methyl salicylate than SlMES3. The SlMES locus has undergone major rearrangement, as demonstrated by genome structure analysis in the parents of the biparental population. Analysis of accessions that produce high or low levels of methyl salicylate showed that SlMES1 and SlMES3 genes expressed the highest in the low methyl salicylate lines. None of the MES genes were appreciably expressed in the high methyl salicylate-producing lines. We concluded that the SlMES gene family encodes tomato methyl esterases that convert methyl salicylate to salicylic acid in ripe tomato fruit. Their ability to decrease methyl salicylate levels by conversion to salicylic acid is an attractive breeding target to lower the level of a negative contributor to flavor.One-sentence summary: A family of methyl esterase enzymes converts salicylic acid into the unpleasant flavor volatile compound, methyl salicylate, in ripening tomato fruit.