Wang Chaofeng, Zhou Bangjun, Chen Xuanyang, Zeng Lirong
Center for Plant Science Innovation and Department of Plant Pathology, University of Nebraska, Lincoln, Nebraska, USA.
Biology Department, University of Arkansas, Little Rock, Arkansas, USA.
Mol Plant Pathol. 2025 Oct;26(10):e70160. doi: 10.1111/mpp.70160.
Plants typically encode multiple ubiquitin-activating enzymes (E1s or UBAs), but their functional equivalence or divergence remains unclear. Here, we demonstrate that the two tomato (Solanum lycopersicum) E1s, SlUBA1 and SlUBA2, differentially regulate development and immunity. Knockdown of SlUBA1 or SlUBA2 caused distinct growth and developmental defects in tomato, while silencing both genes resulted in severe abnormalities, rapid etiolation, and plant death within 5-7 weeks. Notably, silencing SlUBA2, but not SlUBA1, compromised plant immunity against the bacterial pathogen Pseudomonas syringae pv. tomato (Pst). SlUBA1 and SlUBA2 exhibited distinct charging efficiencies for E2s from groups IV (SlUBC32/33/34), V (SlUBC7/14/35/36), VI (SlUBC4/5/6/15) and XII (SlUBC22), with SlUBA2 showing significantly higher efficiency. Swapping the C-terminal ubiquitin-folding domains (UFDs) between SlUBA1 and SlUBA2 largely reversed their E2-charging efficiency for these groups. Furthermore, mutating a key residue (SlUBA2) in the UFD or deleting a conserved 13-amino-acid sequence unique to group V E2s altered the E2-charging profiles of both E1s. These findings suggest dual ubiquitin-activating systems (DUAS) operate in tomato. Given the established role of group IV E2s in plant immunity against Pst, the SlUBA2-group IV E2 module likely plays a central role in modulating host defence. Similarly, the Arabidopsis E1s, AtUBA1 and AtUBA2, differentially charge homologues of tomato group IV E2s, suggesting a conserved mechanism by which plant E1s fulfil distinct physiological roles.
植物通常编码多种泛素激活酶（E1s或UBAs），但其功能的等效性或差异仍不清楚。在这里，我们证明了番茄（Solanum lycopersicum）的两种E1s，即SlUBA1和SlUBA2，对发育和免疫具有不同的调节作用。敲低SlUBA1或SlUBA2会导致番茄出现明显的生长和发育缺陷，而同时沉默这两个基因则会导致严重异常、快速黄化，并在5 - 7周内导致植株死亡。值得注意的是，沉默SlUBA2而非SlUBA1会损害植物对细菌病原体丁香假单胞菌番茄致病变种（Pst）的免疫力。SlUBA1和SlUBA2对来自IV组（SlUBC32/33/34）、V组（SlUBC7/14/35/36）、VI组（SlUBC4/5/6/15）和XII组（SlUBC22）的E2s表现出不同的充电效率，其中SlUBA2的效率显著更高。在SlUBA1和SlUBA2之间交换C末端泛素折叠结构域（UFDs）在很大程度上逆转了它们对这些组的E2充电效率。此外，突变UFD中的一个关键残基（SlUBA2）或删除V组E2s特有的一个保守的13个氨基酸序列会改变这两种E1s的E2充电谱。这些发现表明双泛素激活系统（DUAS）在番茄中起作用。鉴于IV组E2s在植物对Pst的免疫中已确立的作用，SlUBA2 - IV组E2模块可能在调节宿主防御中起核心作用。同样，拟南芥的E1s，AtUBA1和AtUBA2，对番茄IV组E2s的同源物表现出不同的充电作用，这表明植物E1s履行不同生理功能的保守机制。
