ZmMYC2s play important roles in maize responses to simulated herbivory and jasmonate

ZmMYC2s play important roles in maize responses to simulated herbivory and jasmonate
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ZmMYC2 在玉米对模拟食草和茉莉酸的反应中发挥重要作用

DOI:
10.1111/jipb.13404
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发表时间:
2022-12-31
影响因子:
11.4
通讯作者:
Wu, Jianqiang
Wu, Jianqiang
中科院分区:
生物学1区
文献类型:
--
作者:
Ma, Canrong;Li, Ruoyue;Wu, Jianqiang

文献摘要

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草食植物和茉莉酸都能激活玉米防御性代谢产物的生物合成,但其机制尚不清楚。我们产生了玉米突变体,其中在JA信号转导中起重要作用的两个转录因子基因ZmMYC2a和ZmMYC2b被单独或同时敲除。通过遗传和生化分析,阐明了ZmMYC2蛋白在玉米对模拟草食和茉莉酸反应中的功能。与野生型玉米相比,双突变体myc2ab对昆虫高度敏感,经模拟取食和茉莉酸处理后,突变体中苯并恶嗪类化合物和挥发性萜类化合物及其生物合成基因转录水平显著低于野生型玉米。此外,ZmMYC2a和ZmMYC2b在玉米抗虫性和茉莉酸信号转导中起冗余作用。靶标下的转录组和切割及标记序列分析(Cut&Tag-Seq)表明,ZmMYC2物理上针对60%的JA反应基因,尽管这些基因中只有33%依赖于ZmMYC2。重要的是,Cut&Tag-Seq和双荧光素酶分析表明,ZmMYC2通过直接与其启动子结合来反式激活苯并恶嗪和挥发性萜烯生物合成基因IGPS1/3、BX10/11/12/14和TPS10/2/3/4/5/8。此外,还鉴定了几个ZmMYC2s物理靶向的转录因子,这些转录因子可能在调控苯并恶嗪类化合物的生物合成中发挥作用。这项工作揭示了JA信号和ZmMYC2s在玉米中的转录调控格局,并为JA信号如何通过ZmMYC2s调节玉米对草食反应的防御提供了全面的机制洞察。
Both herbivory and jasmonic acid (JA) activate the biosynthesis of defensive metabolites in maize, but the mechanism underlying this remains unclear. We generated maize mutants in which ZmMYC2a and ZmMYC2b, two transcription factor genes important in JA signaling, were individually or both knocked out. Genetic and biochemical analyses were used to elucidate the functions of ZmMYC2 proteins in the maize response to simulated herbivory and JA. Compared with the wild-type (WT) maize, the double mutant myc2ab was highly susceptible to insects, and the levels of benzoxazinoids and volatile terpenes, and the levels of their biosynthesis gene transcripts, were much lower in the mutants than in the WT maize after simulated insect feeding or JA treatment. Moreover, ZmMYC2a and ZmMYC2b played a redundant role in maize resistance to insects and JA signaling. Transcriptome and Cleavage Under Targets and Tagmentation-Sequencing (CUT&Tag-Seq) analysis indicated that ZmMYC2s physically targeted 60% of the JA-responsive genes, even though only 33% of these genes were transcriptionally ZmMYC2-dependent. Importantly, CUT&Tag-Seq and dual luciferase assays revealed that ZmMYC2s transactivate the benzoxazinoid and volatile terpene biosynthesis genes IGPS1/3, BX10/11/12/14, and TPS10/2/3/4/5/8 by directly binding to their promoters. Furthermore, several transcription factors physically targeted by ZmMYC2s were identified, and these are likely to function in the regulation of benzoxazinoid biosynthesis. This work reveals the transcriptional regulatory landscapes of both JA signaling and ZmMYC2s in maize and provides comprehensive mechanistic insight into how JA signaling modulates defenses in maize responses to herbivory through ZmMYC2s.