Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene.

Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene.
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DOI:
10.1371/journal.pgen.1007310
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发表时间:
2018-04
期刊:
影响因子:
4.5
通讯作者:
Eves-van den Akker S
Eves-van den Akker S
中科院分区:
生物学2区
文献类型:
--
作者:
Lilley CJ;Maqbool A;Wu D;Yusup HB;Jones LM;Birch PRJ;Banfield MJ;Urwin PE;Eves-van den Akker S

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植物病原体和寄生虫是全球粮食安全的主要威胁。植物寄生在线虫门中独立出现了四次,导致世界上每种主要粮食作物至少有一种寄生虫。在经济上最重要的目的(Tylenchida)中的一些物种在感染期间向其宿主分泌称为效应子的蛋白质,以重新编程宿主发育和免疫。线虫如何进化出新的效应子的确切细节尚不清楚。在这里,我们重建一个新的效应基因家族的进化历史。我们表明,在进化的植物寄生在Tylenchida,管家谷胱甘肽合成酶(GS)基因被广泛复制。新的GS旁系同源物获得了多个背腺启动子元件,改变了空间表达的分泌背腺,改变了时间表达的主要寄生阶段,并获得了信号肽的分泌。在感染过程中,基因产物被递送到宿主植物细胞中,产生“GS样效应物”。值得注意的是,通过解决GS样效应物的结构,我们表明,在这个过程中,他们也多样化的生化活性,并可能代表一类新的GS样酶的创始成员。我们的研究结果表明,重新利用内源性管家基因,形成一个家庭的效应与修改功能。我们预计,我们的发现将成为了解其他植物寄生线虫效应子进化的蓝图,并为发现新的酶功能奠定基础。植物及其病原体/寄生虫被锁定在进化的军备竞赛中,相当多的注意力集中在寄生虫的“武器”的特定功能上:效应器。虽然我们开始了解这些功能,但我们对植物寄生线虫如何增强其效应子库的了解甚少。在这里,我们提供了一个例子,植物寄生虫的全球经济的重要性,填充其效应库的前所未有的重复和随后的重新部署的内源性管家基因,谷胱甘肽合成酶。我们假设,在这里详细介绍的“武器化”方案的许多方面将是共同的其他植物寄生线虫效应器的起源。鉴于寄生线虫部署了一系列效应子,许多效应子来自内源基因或水平基因转移获得的基因座的适应,这种模式将对理解并最终破坏破坏USDA和EPPO检疫生物的努力产生重大影响。
Plant pathogens and parasites are a major threat to global food security. Plant parasitism has arisen four times independently within the phylum Nematoda, resulting in at least one parasite of every major food crop in the world. Some species within the most economically important order (Tylenchida) secrete proteins termed effectors into their host during infection to re-programme host development and immunity. The precise detail of how nematodes evolve new effectors is not clear. Here we reconstruct the evolutionary history of a novel effector gene family. We show that during the evolution of plant parasitism in the Tylenchida, the housekeeping glutathione synthetase (GS) gene was extensively replicated. New GS paralogues acquired multiple dorsal gland promoter elements, altered spatial expression to the secretory dorsal gland, altered temporal expression to primarily parasitic stages, and gained a signal peptide for secretion. The gene products are delivered into the host plant cell during infection, giving rise to “GS-like effectors”. Remarkably, by solving the structure of GS-like effectors we show that during this process they have also diversified in biochemical activity, and likely represent the founding members of a novel class of GS-like enzyme. Our results demonstrate the re-purposing of an endogenous housekeeping gene to form a family of effectors with modified functions. We anticipate that our discovery will be a blueprint to understand the evolution of other plant-parasitic nematode effectors, and the foundation to uncover a novel enzymatic function. Plants and their pathogens/parasites are locked in an evolutionary arms race, with considerable attention directed towards the specific functions of the parasites’ “weapons”: the effectors. While we are beginning to understand these functions, we have very little understanding of how plant parasitic nematodes have bolstered their effector repertoire. Here we provide an example of how plant parasites of global economic importance have populated their effector repertoire by the unprecedented duplication and subsequent re-deployment of the endogenous housekeeping gene, glutathione synthetase. We hypothesise that many aspects of the “weaponization” programme detailed here will be common to the genesis of other plant-parasitic nematode effectors. Given that parasitic nematodes deploy a battery of effectors, many arising from the adaptation of either endogenous genes or loci acquired by horizontal gene transfer, this paradigm will have substantial impact on the effort to understand and ultimately undermine devastating USDA and EPPO quarantine organisms.
DOI: 10.1186/s13059-016-0985-1
发表时间: 2016-06-10
期刊: Genome biology
影响因子: 12.3
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Eves-van den Akker S;Laetsch DR;Thorpe P;Lilley CJ;Danchin EG;Da Rocha M;Rancurel C;Holroyd NE;Cotton JA;Szitenberg A;Grenier E;Montarry J;Mimee B;Duceppe MO;Boyes I;Marvin JM;Jones LM;Yusup HB;Lafond-Lapalme J;Esquibet M;Sabeh M;Rott M;Overmars H;Finkers-Tomczak A;Smant G;Koutsovoulos G;Blok V;Mantelin S;Cock PJ;Phillips W;Henrissat B;Urwin PE;Blaxter M;Jones JT
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DOI: 10.1093/gbe/evu171
发表时间: 2014-08-13
影响因子: 3.3
作者:
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期刊: PLoS pathogens
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影响因子: 2.7
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