Exploiting breakdown in nonhost effector-target interactions to boost host disease resistance.

Exploiting breakdown in nonhost effector-target interactions to boost host disease resistance.
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DOI:
10.1073/pnas.2114064119
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发表时间:
2022-08-30
影响因子:
11.1
通讯作者:
--
中科院分区:
综合性期刊1区
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植物非宿主抗性(NHR)可防止大多数微生物物种的所有成员的感染,但其分子机制尚不清楚。我们发现来自马铃薯枯萎病病原体致病疫霉的效应蛋白可以增强宿主植物的感染,但不能增强非宿主拟南芥的敏感性。这些致病疫霉效应子通常无法与其马铃薯靶蛋白的拟南芥直系同源物相互作用,而在这些拟南芥直系同源物和来自其适应病原体拟南芥膜孢菌的效应子之间检测到许多相互作用。因此,远缘非寄主植物中效应子-靶标相互作用的破坏可能是 NHR 的关键组成部分。重要的是,我们证明利用这种分解并在宿主植物中表达非宿主目标直向同源物提供了预防作物疾病的策略。由于非宿主抗性(NHR),植物对大多数微生物物种具有抗性,提供广谱和持久的免疫力。然而,对 NHR 贡献的分子成分却知之甚少。我们解决了病原体效应子未能操纵非寄主植物是否在 NHR 中发挥关键作用的问题。来自两种卵菌病原体(致病疫霉和拟南芥霜霉)的 RxLR(精氨酸-任意氨基酸-亮氨酸-精氨酸)效应子在宿主植物(分别是烟草和拟南芥)中表达时增强了病原体感染,但相同的效应子在远缘相关的非宿主病理系统中表现不佳。使用酵母 2 杂交 (Y2H) 筛选,鉴定了宿主植物马铃薯中 64 个致病疫霉 RxLR 效应子的推定靶蛋白。使用基质 Y2H 鉴定和筛选远亲非宿主植物拟南芥中这些靶蛋白的候选直系同源物,以与来自致病疫霉和拟南芥的 RxLR 效应子相互作用。从马铃薯到候选拟南芥靶标直向同源物(cAtOrths),很少有致病疫霉效应子-靶蛋白相互作用是保守的。然而,与 cAtOrths 相互作用的拟南芥 RxLR 效应子有所富集。我们在马铃薯和本塞姆氏烟草中表达了 cAtOrth AtPUB33,与马铃薯直系同源物不同,它不与马铃薯晚疫病菌效应子 PiSFI3 相互作用。 AtPUB33 的表达显着减少了致病疫霉在两种宿主植物中的定植。我们的结果提供了证据,证明病原体效应子未能与远缘相关非寄主植物中的靶蛋白相互作用和/或正确操纵靶蛋白有助于 NHR。此外,利用效应子-非宿主靶标相互作用的这种分解,将效应子靶标直系同源物从非宿主植物转移到宿主植物是减少疾病的策略。
Plant nonhost resistance (NHR) prevents infection by all members of most microbial species, but its molecular mechanisms are not well understood. We found that effector proteins from the potato blight pathogen Phytophthora infestans, which enhance infection in host plants, fail to enhance susceptibility in nonhost Arabidopsis. These P. infestans effectors often failed to interact with Arabidopsis orthologs of their potato target proteins, whereas many interactions were detected between these Arabidopsis orthologs and effectors from its adapted pathogen Hyaloperonospora arabidopsidis. Thus, breakdown in effector–target interactions in distantly related nonhost plants is likely a key component of NHR. Importantly, we demonstrate that exploiting this breakdown and expressing nonhost target orthologs in host plants provide a strategy to prevent crop disease. Plants are resistant to most microbial species due to nonhost resistance (NHR), providing broad-spectrum and durable immunity. However, the molecular components contributing to NHR are poorly characterised. We address the question of whether failure of pathogen effectors to manipulate nonhost plants plays a critical role in NHR. RxLR (Arg-any amino acid-Leu-Arg) effectors from two oomycete pathogens, Phytophthora infestans and Hyaloperonospora arabidopsidis, enhanced pathogen infection when expressed in host plants (Nicotiana benthamiana and Arabidopsis, respectively) but the same effectors performed poorly in distantly related nonhost pathosystems. Putative target proteins in the host plant potato were identified for 64 P. infestans RxLR effectors using yeast 2-hybrid (Y2H) screens. Candidate orthologues of these target proteins in the distantly related non-host plant Arabidopsis were identified and screened using matrix Y2H for interaction with RxLR effectors from both P. infestans and H. arabidopsidis. Few P. infestans effector-target protein interactions were conserved from potato to candidate Arabidopsis target orthologues (cAtOrths). However, there was an enrichment of H. arabidopsidis RxLR effectors interacting with cAtOrths. We expressed the cAtOrth AtPUB33, which unlike its potato orthologue did not interact with P. infestans effector PiSFI3, in potato and Nicotiana benthamiana. Expression of AtPUB33 significantly reduced P. infestans colonization in both host plants. Our results provide evidence that failure of pathogen effectors to interact with and/or correctly manipulate target proteins in distantly related non-host plants contributes to NHR. Moreover, exploiting this breakdown in effector-nonhost target interaction, transferring effector target orthologues from non-host to host plants is a strategy to reduce disease.
DOI: 10.1038/ncomms10311
发表时间: 2016-01-29
影响因子: 16.6
作者:
Boevink PC;Wang X;McLellan H;He Q;Naqvi S;Armstrong MR;Zhang W;Hein I;Gilroy EM;Tian Z;Birch PRJ
通讯作者: Birch PRJ
DOI: 10.1111/j.1365-313x.2012.05079.x
发表时间: 2012-12-01
期刊: PLANT JOURNAL
影响因子: 7.2
作者:
Anderson, Ryan G.;Casady, Megan S.;McDowell, John M.
通讯作者: McDowell, John M.
DOI: 10.1046/j.1365-313x.1998.00343.x
发表时间: 1998-12-01
期刊: PLANT JOURNAL
影响因子: 7.2
作者:
Clough, SJ;Bent, AF
通讯作者: Bent, AF
DOI: 10.1046/j.1364-3703.2003.00195.x
发表时间: 2003-11-01
影响因子: 4.9
作者:
Huitema, E;Vleeshouwers, VGAA;Kamoun, S
通讯作者: Kamoun, S
DOI: 10.1098/rstb.2013.0087
发表时间: 2014-04-05
期刊: Philosophical transactions of the Royal Society of London. Series B, Biological sciences
影响因子: --
作者:
Jones JD;Witek K;Verweij W;Jupe F;Cooke D;Dorling S;Tomlinson L;Smoker M;Perkins S;Foster S
通讯作者: Foster S