Research Centre for Biosystems, Land Use, and Nutrition, Justus Liebig University, 35392 Giessen, Germany.
Plant Cell. 2012 Feb;24(2):794-809. doi: 10.1105/tpc.111.093260. Epub 2012 Feb 14.
In Arabidopsis thaliana roots, the mutualistic fungus Piriformospora indica initially colonizes living cells, which die as the colonization proceeds. We aimed to clarify the molecular basis of this colonization-associated cell death. Our cytological analyses revealed endoplasmic reticulum (ER) swelling and vacuolar collapse in invaded cells, indicative of ER stress and cell death during root colonization. Consistent with this, P. indica-colonized plants were hypersensitive to the ER stress inducer tunicamycin. By clear contrast, ER stress sensors bZIP60 and bZIP28 as well as canonical markers for the ER stress response pathway, termed the unfolded protein response (UPR), were suppressed at the same time. Arabidopsis mutants compromised in caspase 1-like activity, mediated by cell death-regulating vacuolar processing enzymes (VPEs), showed reduced colonization and decreased cell death incidence. We propose a previously unreported microbial invasion strategy during which P. indica induces ER stress but inhibits the adaptive UPR. This disturbance results in a VPE/caspase 1-like-mediated cell death, which is required for the establishment of the symbiosis. Our results suggest the presence of an at least partially conserved ER stress-induced caspase-dependent cell death pathway in plants as has been reported for metazoans.
在拟南芥的根部，共生真菌离蠕孢菌最初会定殖活细胞，随着定殖的进行，这些活细胞会死亡。我们旨在阐明这种与定殖相关的细胞死亡的分子基础。我们的细胞学分析显示，受侵染的细胞中内质网（ER）肿胀和液泡崩溃，表明 ER 应激和细胞死亡发生在根定殖过程中。与此一致的是，受离蠕孢菌定殖的植物对 ER 应激诱导剂衣霉素敏感。相比之下，ER 应激传感器 bZIP60 和 bZIP28 以及 ER 应激反应途径的经典标记物，称为未折叠蛋白反应（UPR），同时被抑制。拟南芥中半胱氨酸蛋白酶 1 样活性的突变体，由细胞死亡调节液泡加工酶（VPEs）介导，表现出定殖减少和细胞死亡发生率降低。我们提出了一个以前未报道的微生物入侵策略，即在该策略中，离蠕孢菌诱导 ER 应激，但抑制适应性 UPR。这种干扰导致 VPE/半胱天冬酶 1 样介导的细胞死亡，这是共生建立所必需的。我们的结果表明，植物中存在至少部分保守的 ER 应激诱导的半胱氨酸蛋白酶依赖性细胞死亡途径，这与后生动物的报道一致。
