Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner.
Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner.
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DOI：
10.1371/journal.pbio.1001835
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发表时间：
2014-04
期刊：
影响因子：
9.8
通讯作者：
Hogenhout SA
中科院分区：
文献类型：
--
作者：
MacLean AM;Orlovskis Z;Kowitwanich K;Zdziarska AM;Angenent GC;Immink RG;Hogenhout SA
植物植原体细菌寄生依靠叶蝉类昆虫传播和繁殖。这项研究揭示了植原体如何颠覆植物的发育，将花变成叶，从而使其宿主对叶蝉更具吸引力。依赖多个宿主完成其生命周期的病原体通常会改变这些宿主的行为和发育，以迫使它们改善病原体的适合性。然而，很少有研究描述宿主胁迫的潜在机制。在这项研究中，我们阐明了昆虫传播的植物病原体通过改变花的发育将花转化为营养组织的机制。我们发现植原体产生一种新的效应蛋白(SAP54)，它与MADS结构域转录因子(MTF)家族的成员相互作用，包括在花发育调控中占据中心地位的关键调控因子SEPALLATA3和APETALA1。SAP54通过与辐射SENSITIVE23(RAD23)家族的蛋白质相互作用来调节MTF的降解，RAD23家族是真核蛋白质，将底物运送到蛋白酶体。拟南芥RAD23突变体在SAP54存在下和植原体感染期间没有表现出花向叶状组织的转化，强调了RAD23对SAP54活性的重要性。值得注意的是，具有SAP54诱导的叶状花的植物更容易被植原体叶蝉载体侵染，这种定殖偏好依赖于RAD23。一种针对和抑制开花同时促进昆虫食草动物定植的效应器是史无前例的。此外，据我们所知，RAD23蛋白在花发育中没有已知的作用，也没有植物对昆虫的防御机制。因此，SAP54在寄主的两条关键途径之间产生短路，改变发育，导致不育植物，并促进这些植物对帮助专性植原体繁殖和繁殖的叶蝉载体(僵尸植物)的吸引力。寄生在多个宿主上的寄生虫通常会迫使这些宿主提高自己的存活率和繁殖率。然而，寄生虫如何做到这一点在很大程度上是未知的。植原体是一种细菌植物寄生虫，需要以汁液为食的昆虫媒介--叶蝉--来繁殖和传播。很长一段时间以来，人们一直知道植原体会在广泛的植物物种中刺激戏剧性的发育变化，例如被称为叶状体的花转化为叶，以及被称为“巫婆的扫帚”的茎的增殖。在这里，我们报告植原体如何以及为什么会引起这些戏剧性的发育变化。我们鉴定了一种植原体毒力蛋白SAP54，它能将花转化为叶片，并将植物转化为更具吸引力的寄主，以便产卵和繁殖其叶蝉载体。我们发现SAP54通过促进开花植物中调节重要发育过程的蛋白质的降解来发挥其作用。这些蛋白是MADS-box家族中高度保守的转录因子，通过SAP54介导的降解降低它们的活性，阻碍花的发育，产生不育植株。这个降解过程需要RAD23，一种将转录因子招募到蛋白质降解机制中的蛋白质。由此产生的不育植物，形成了叶子而不是花，对叶蝉更具吸引力，可以说是植原体掌握了寄生虫世界的操纵者。
The phytoplasma bacterial plant parasite depends on leafhopper insects to spread and propagate itself. This study reveals how phytoplasma subverts plant development to turn flowers into leaves and thus make its host more attractive to leafhoppers. Pathogens that rely upon multiple hosts to complete their life cycles often modify behavior and development of these hosts to coerce them into improving pathogen fitness. However, few studies describe mechanisms underlying host coercion. In this study, we elucidate the mechanism by which an insect-transmitted pathogen of plants alters floral development to convert flowers into vegetative tissues. We find that phytoplasma produce a novel effector protein (SAP54) that interacts with members of the MADS-domain transcription factor (MTF) family, including key regulators SEPALLATA3 and APETALA1, that occupy central positions in the regulation of floral development. SAP54 mediates degradation of MTFs by interacting with proteins of the RADIATION SENSITIVE23 (RAD23) family, eukaryotic proteins that shuttle substrates to the proteasome. Arabidopsis rad23 mutants do not show conversion of flowers into leaf-like tissues in the presence of SAP54 and during phytoplasma infection, emphasizing the importance of RAD23 to the activity of SAP54. Remarkably, plants with SAP54-induced leaf-like flowers are more attractive for colonization by phytoplasma leafhopper vectors and this colonization preference is dependent on RAD23. An effector that targets and suppresses flowering while simultaneously promoting insect herbivore colonization is unprecedented. Moreover, RAD23 proteins have, to our knowledge, no known roles in flower development, nor plant defence mechanisms against insects. Thus SAP54 generates a short circuit between two key pathways of the host to alter development, resulting in sterile plants, and promotes attractiveness of these plants to leafhopper vectors helping the obligate phytoplasmas reproduce and propagate (zombie plants). Parasites that colonize multiple hosts often coerce these hosts into improving their own survival and reproduction rates. However, how parasites do this is largely unknown. Phytoplasmas are bacterial plant parasites that require sap-feeding insect vectors—leafhoppers—for their propagation and dispersal. It has been known for a long time that phytoplasmas stimulate dramatic developmental changes in a broad range of plant species, such as the conversion of flowers into leaves known as phyllody and the proliferation of stems known as “witches' broom.” Here we report how and why phytoplasmas cause these dramatic developmental changes. We identified a phytoplasma virulence protein, SAP54, which transforms flowers into leaves and converts plants into more attractive hosts for the egg-laying and reproduction of their leafhopper vectors. We show that SAP54 exerts its effect by promoting the degradation of proteins that regulate important developmental processes in flowering plants. These proteins are highly conserved transcription factors of the MADS-box family, and reducing their activity through SAP54–mediated degradation curtails flower development, generating sterile plants. This degradation process requires RAD23, a protein that recruits the transcription factors to the protein degradation machinery. The resulting sterile plants, which form leaves in place of flowers, are more attractive to leafhoppers, arguably making phytoplasmas master manipulators of the parasite world.
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影响因子：
14.8
作者：
Gietz, R. Daniel;Schiestl, Robert H.
通讯作者：
Schiestl, Robert H.
影响因子：
6.7
作者：
Angot, Aurelie;Vergunst, Annette;Genin, Stephane;Peeters, Nemo
通讯作者：
Peeters, Nemo
DOI：
10.1007/978-1-61779-154-3_8
发表时间：
2011-01-01
期刊：
PLANT TRANSCRIPTION FACTORS: METHODS AND PROTOCOLS
影响因子：
--
作者：
de Folter, Stefan;Immink, Richard G. H.
通讯作者：
Immink, Richard G. H.
影响因子：
11.4
作者：
Davies, B;EgeaCortines, M;Sommer, H
通讯作者：
Sommer, H
影响因子：
7.2
作者：
Clough, SJ;Bent, AF
通讯作者：
Bent, AF