Wang Chaofeng, Zhou Bangjun, Zhang Yi, Zeng Lirong
Center for Plant Science Innovation and Department of Plant Pathology, University of Nebraska, Lincoln, NE, 68588, USA.
South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China.
BMC Plant Biol. 2025 Apr 2;25(1):412. doi: 10.1186/s12870-025-06419-8.
Endoplasmic reticulum (ER)-associated protein degradation (ERAD) is a critical component of the ER-mediated protein quality control (ERQC) system and plays a vital role in plant stress responses. However, the ubiquitination machinery underlying plant ERAD-particularly the ubiquitin-conjugating enzymes (E2s)-and their contributions to stress tolerance remain poorly understood.
In this study, we identified UBC32, UBC33, and UBC34 as ER-localized ubiquitin E2 enzymes involved in ERAD and demonstrated their roles in biotic and abiotic stress tolerance in tomato (Solanum lycopersicum) and Arabidopsis (Arabidopsis thaliana). In response to biotic stress, UBC33 and UBC34 collectively contribute more substantially than UBC32 to plant immunity against Pseudomonas syringae pv. tomato (Pst). Under abiotic stress and ER stress induced by tunicamycin (TM), all three E2s play important roles. Notably, mutation of UBC32 enhances tolerance to TM-induced ER stress, whereas the loss of function in UBC33 or UBC34 suppresses this response. Additionally, UBC32, UBC33, and UBC34 act synergistically in Arabidopsis seed germination under salt stress and abscisic acid (ABA) treatment. While the single mutants atubc32, atubc33, and atubc34 exhibit germination rates comparable to Col-0 under salt stress or ABA treatment, the double mutants atubc32/33, atubc32/34, and atubc33/34 show a significantly greater reduction in germination rate. Interestingly, the atubc32/33/34 triple mutant exhibits a seed germination rate under salt stress and ABA treatment, as well as a level of host immunity to Pst, comparable to that of the atubc33/34 and atubc32/34 double mutants.
Our findings establish UBC32, UBC33, and UBC34 as key components of the plant ERAD machinery, contributing to plant tolerance to both abiotic and biotic stress. Despite their close phylogenetic relationship, these E2 enzymes exhibit redundant, synergistic, or antagonistic roles depending on the specific stress response pathway, underscoring the complexity of their functional interactions.
内质网（ER）相关蛋白降解（ERAD）是ER介导的蛋白质质量控制（ERQC）系统的关键组成部分，在植物应激反应中发挥着至关重要的作用。然而，植物ERAD潜在的泛素化机制，尤其是泛素结合酶（E2s）及其对胁迫耐受性的贡献仍知之甚少。
在本研究中，我们鉴定出UBC32、UBC33和UBC34为参与ERAD的内质网定位泛素E2酶，并证明了它们在番茄（Solanum lycopersicum）和拟南芥（Arabidopsis thaliana）的生物和非生物胁迫耐受性中的作用。在应对生物胁迫时，UBC33和UBC34共同对植物抵抗丁香假单胞菌番茄致病变种（Pst）的免疫作用比UBC32更为显著。在衣霉素（TM）诱导的非生物胁迫和ER胁迫下，所有这三种E2酶都发挥重要作用。值得注意的是，UBC32的突变增强了对TM诱导的ER胁迫的耐受性，而UBC33或UBC34的功能丧失则抑制了这种反应。此外，在盐胁迫和脱落酸（ABA）处理下，UBC32、UBC33和UBC34在拟南芥种子萌发中协同作用。虽然单突变体atubc32、atubc33和atubc34在盐胁迫或ABA处理下的萌发率与Col-0相当，但双突变体atubc32/33、atubc32/34和atubc33/34的萌发率显著降低。有趣的是，atubc32/33/34三突变体在盐胁迫和ABA处理下的种子萌发率，以及对Pst的宿主免疫水平，与atubc33/34和atubc32/34双突变体相当。
我们的研究结果确定UBC32、UBC33和UBC34为植物ERAD机制的关键组成部分，有助于植物对非生物和生物胁迫的耐受性。尽管它们在系统发育上关系密切，但这些E2酶根据特定的应激反应途径表现出冗余、协同或拮抗作用，突显了它们功能相互作用的复杂性。
