A Maize Cystatin Suppresses Host Immunity by Inhibiting Apoplastic Cysteine Proteases

A Maize Cystatin Suppresses Host Immunity by Inhibiting Apoplastic Cysteine Proteases
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DOI:
10.1105/tpc.111.093732
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发表时间:
2012-03-01
期刊:
影响因子:
11.6
通讯作者:
Doehlemann, Gunther
Doehlemann, Gunther
中科院分区:
生物学1区
文献类型:
--
作者:
van der Linde, Karina;Hemetsberger, Christoph;Doehlemann, Gunther

文献摘要

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玉米黑粉菌 (Ustilago maydis) 是一种引起玉米黑粉病的生物营养病原体。受感染玉米植物的转录组分析表明,编码推定半胱氨酸蛋白酶抑制剂 (CC9) 的基因在被野生型玉米玉蜀黍渗透后被诱导。相比之下,cc9 在感染玉米须菌效应突变体 Delta pep1 后不会被诱导,而 Delta pep1 会引发大量的植物防御。 cc9 的沉默导致强烈诱导的玉米防御基因表达和对玉米 U. maydis 野生型感染的过敏反应。因此,cc9 沉默植物中的真菌定植大大减少,而重组 CC9 则阻止了水杨酸 (SA) 诱导的防御。蛋白酶活性分析显示,SA 处理的叶片中玉米 Cys 蛋白酶的强烈诱导,这可以通过添加 CC9 来抑制。过表达 cc9-mCherry 的转基因玉米植物显示出 CC9 的质外体定位。转基因植物表现出Cys蛋白酶活性和SA依赖性基因表达的阻断。此外,活化的质外体Cys蛋白酶在幼稚植物中诱导SA相关防御基因表达,而CC9可以抑制这种表达。我们证明质外体半胱氨酸蛋白酶在玉米防御信号传导中发挥着关键作用。此外,我们发现胱抑素 CC9 是一种新型相容性因子,可抑制 Cys 蛋白酶活性,从而使玉米与真菌病原体 U. maydis 发生生物营养相互作用。
Ustilago maydis is a biotrophic pathogen causing maize (Zea mays) smut disease. Transcriptome profiling of infected maize plants indicated that a gene encoding a putative cystatin (CC9) is induced upon penetration by U. maydis wild type. By contrast, cc9 is not induced after infection with the U. maydis effector mutant Delta pep1, which elicits massive plant defenses. Silencing of cc9 resulted in a strongly induced maize defense gene expression and a hypersensitive response to U. maydis wild-type infection. Consequently, fungal colonization was strongly reduced in cc9-silenced plants, while recombinant CC9 prevented salicylic acid (SA)-induced defenses. Protease activity profiling revealed a strong induction of maize Cys proteases in SA-treated leaves, which could be inhibited by addition of CC9. Transgenic maize plants overexpressing cc9-mCherry showed an apoplastic localization of CC9. The transgenic plants showed a block in Cys protease activity and SA-dependent gene expression. Moreover, activated apoplastic Cys proteases induced SA-associated defense gene expression in naive plants, which could be suppressed by CC9. We show that apoplastic Cys proteases play a pivotal role in maize defense signaling. Moreover, we identified cystatin CC9 as a novel compatibility factor that suppresses Cys protease activity to allow biotrophic interaction of maize with the fungal pathogen U. maydis.