The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition.

The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition.
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DOI:
10.1371/journal.ppat.1004496
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发表时间:
2014-10
期刊:
影响因子:
6.7
通讯作者:
Faulkner C
Faulkner C
中科院分区:
医学1区
文献类型:
--
作者:
Caillaud MC;Wirthmueller L;Sklenar J;Findlay K;Piquerez SJ;Jones AM;Robatzek S;Jones JD;Faulkner C

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霜霉病菌拟南芥透明operonospora arabidsidis (Hpa)是一种丝状卵菌,通过称为吸器的复杂但鲜为人知的结构侵入植物细胞。吸器与宿主细胞质分离,被来源不明的吸器外膜(EHM)包围。在一些相互作用中,包括hpa -拟南芥,吸器逐渐被宿主衍生的富含胼胝质的物质包裹,但胼胝质在吸器周围积累的分子机制尚不清楚。在这里,我们报道了plasmodesmata定位蛋白1 (PDLP1)在Hpa感染细胞中高水平表达。与其他经常被排除在EHM之外的质膜蛋白不同,PDLP1在被包裹之前位于hpa感染细胞的EHM。PDLP1的跨膜结构域和细胞质尾部足以传递这种定位。PDLP1也与发育中的包装箱有关,但当包装箱完全成熟时,这种联系就消失了。我们发现pdlp1,2,3三重突变体对Hpa更敏感,而过表达pdlp1增强了植物的抗性,这表明pdlp1增强了对Hpa的基础免疫。在pdlp1、2、3突变体植物中,吸器囊中的胼胝质被耗尽,而pdlp1的过表达增加了吸器周围和细胞表面的胼胝质沉积。这些数据表明ppdps参与了Hpa吸器中胼胝质的包裹,并提示吸器中胼胝质的沉积可能与间连丝中胼胝质的沉积机制相似。吸器是一种特殊的侵入性结构,在感染过程中从真菌或卵菌菌丝投射到寄主植物细胞中,作为寄主和病原体之间分子交换的场所。吸器是植物防御反应的目标,包括膜和多糖在吸器周围的包裹结构中的沉积。据推测,外壳物理上将吸器与宿主细胞隔离开来。在这里,我们利用细胞生物学和遗传学方法揭示了胞间连丝相关受体样蛋白PDLP1在拟南芥霜霉病病原体的感染成功中起作用,特别是在包膜的发展中。通过活细胞成像,我们观察到PDLP1迁移到吸器外膜,这是在包膜中沉积多糖胼胝质的必要条件。这直接将病原体的成功与包膜结构联系起来,验证了包膜在宿主防御中的重要性。此外,我们的数据提出的可能性,胼胝质沉积在间连丝和吸器包裹利用类似的机制。我们的发现揭示了吸器中的植物防御以及它们如何抑制病原体的成功。
The downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa) is a filamentous oomycete that invades plant cells via sophisticated but poorly understood structures called haustoria. Haustoria are separated from the host cell cytoplasm and surrounded by an extrahaustorial membrane (EHM) of unknown origin. In some interactions, including Hpa-Arabidopsis, haustoria are progressively encased by host-derived, callose-rich materials but the molecular mechanisms by which callose accumulates around haustoria remain unclear. Here, we report that PLASMODESMATA-LOCATED PROTEIN 1 (PDLP1) is expressed at high levels in Hpa infected cells. Unlike other plasma membrane proteins, which are often excluded from the EHM, PDLP1 is located at the EHM in Hpa-infected cells prior to encasement. The transmembrane domain and cytoplasmic tail of PDLP1 are sufficient to convey this localization. PDLP1 also associates with the developing encasement but this association is lost when encasements are fully mature. We found that the pdlp1,2,3 triple mutant is more susceptible to Hpa while overexpression of PDLP1 enhances plant resistance, suggesting that PDLPs enhance basal immunity against Hpa. Haustorial encasements are depleted in callose in pdlp1,2,3 mutant plants whereas PDLP1 over-expression elevates callose deposition around haustoria and across the cell surface. These data indicate that PDLPs contribute to callose encasement of Hpa haustoria and suggests that the deposition of callose at haustoria may involve similar mechanisms to callose deposition at plasmodesmata. Haustoria are specialised invasive structures that project from fungal or oomycete hyphae into host plant cells during infection, acting as sites for molecular exchange between host and pathogen. Haustoria are targets of plant defence responses, including the deposition of membranes and polysaccharides in an encasement structure that surrounds the haustorium. It is assumed that the encasement physically seals the haustorium off from the host cell. Here we have used cell biological and genetic approaches to reveal that the plasmodesmata-associated receptor-like protein PDLP1 plays a role in infection success of the Arabidopsis downy mildew pathogen, specifically in the development of the encasement. Using live cell imaging, we observed that PDLP1 relocates to the extra-haustorial membrane, and this is required for deposition of the polysaccharide callose in the encasement. This directly correlates pathogen success with the structure of the encasement, verifying the significance of the encasement in host defence. Further, our data pose the possibility that callose deposition at plasmodesmata and the haustorial encasement exploit similar mechanisms. Our findings shed light on plant defences at haustoria and how they inhibit pathogen success.
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