Genome-wide characterization of citrus remorin genes identifies an atypical remorin CsREM1.1 responsible for fruit disease resistance

Abstract

Remorins (REMs) are plant-specific proteins associated with plasma membrane (PM) and exhibit diverse biological functions. However, the roles of remorins in fruit crops and fruit disease resistance remain unexplored. Here, we performed a genome-wide characterization of remorin genes from citrus (Citrus sinensis) and identified an atypical remorin CsREM1.1 responsible for fruit resistance to Penicillium digitatum (Pd), a notorious postharvest fungal pathogen of citrus. Ten remorin genes were identified in the C. sinensis genome and they were categorized into five groups. A lot of cis-elements involved in hormone and stress responsiveness were exhibited in the promoter regions of citrus remorin genes. Reverse transcription-quantitative PCR (RT-qPCR) analysis showed that the majority of citrus remorin genes, especially CsREM1.1, were significantly induced in citrus fruit upon Pd infection. Unlike typical remorins, CsREM1.1 exhibited nuclear localization in addition to its traditional PM localization. Transient expression of CsREM1.1 in the model plant Nicotiana benthamiana suppressed plant cell death triggered by BAX, an important pro-apoptotic factor, and enhanced plant resistance to Botrytis cinerea. Moreover, transient overexpression or silencing of CsREM1.1 in citrus fruit indicated the important contribution of CsREM1.1 in fruit resistance to Pd. Our study increases the understanding of plant remorins and provides valuable insights for future research on fruit disease resistance.