JRE4 is a master transcriptional regulator of defense‐ elated steroidal glycoalkaloids in tomato

First author: Masaru Nakayasu; Affiliations: Kobe University (神户大学): Kobe, Japa

Corresponding author: Tsubasa Shoji (Nara Institute of Science and Technology)

Steroidal glycoalkaloids (SGAs; 甾体生物碱) are specialized anti‐ utritional metabolites (抗营养代谢物) that accumulate in Solanum lycopersicum (tomato; 番茄) and Solanum tuberosum (potato; 马铃薯). A series of SGA biosynthetic genes is known to be upregulated in Solanaceae species by jasmonate‐ esponsive Ethylene Response Factor transcription factors (茉莉酸应答乙烯反应因子转录因子), including JRE4 (otherwise known as GAME9), but the exact regulatory significance in planta of each factor has remained unaddressed. Here, via TILLING‐ased screening (TILLING技术，即定向诱导基因组局部突变技术) of an EMS‐mutagenized tomato population, we isolated a JRE4 loss‐of‐function line that carries an amino acid residue missense (错义) change in a region of the protein important for DNA binding. In this jre4 mutant, we observed downregulated expression of SGA biosynthetic genes and decreased SGA accumulation. Moreover, JRE4 overexpression stimulated SGA production. Further characterization of jre4 plants revealed their increased susceptibility to the generalist herbivore Spodoptera liter (斜纹夜蛾) larvae (幼虫). This susceptibility illustrates that herbivory resistance is dependent on JRE4‐mediated defense responses, which include SGA accumulation. Ethylene treatment attenuated (减弱) the jasmonate‐mediated JRE4 expression induction and downstream SGA biosynthesis in tomato leaves and hairy roots (毛状根). Overall, this study indicated that JRE4 functions as a primary master regulator of SGA biosynthesis, and thereby contributes toward plant defense against chewing insects.

甾体生物碱SGA是特异的抗营养代谢物，在番茄和马铃薯中积累。已知有一系列的SGA生物合成基因在茄科物种中受到包括JRE4在内的茉莉酸应答乙烯反应因子转录因子的上调，然而在植物体内每个因子确切的调控特性还未清楚。通过对番茄的EMS诱变群体基于TILLING技术扫描，作者鉴定出了一个JRE4功能缺失突变体，该突变体在蛋白编码序列的DNA结合区域发生了一次错义突变。在jre4突变体中，SGA生物合成基因的表达下调，SGA积累减少。此外，JRE4过表达会促进SGA的合成。通过对jre4突变株的进一步分析，作者发现jre4突变株对于光谱草食动物斜纹夜蛾幼虫的易感性增强，表明草食动物抗性依赖于JRE4介导的防御响应，包括SGA的积累。乙烯处理会减弱番茄叶片和毛状根中茉莉酸介导的JRE4诱导表达和下游的SGA生物合成。综上，本文的研揭示了JRE4作为SGA生物合成主要的调控子，进而作用于植物对取食昆虫的防御。

通讯：Tsubasa Shoji

个人简介：奈良先端科学技术大学院大学生物科学研究生院植物细胞功能实验室的副教授，实验室网址：http://bsw3.naist.jp/hashimoto/?cate=186。

doi: https://doi.org/10.1111/tpj.13911

Journal: the plant journal

First Published date: 29 April, 2018

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