Danger peptide signaling enhances internalization of a geminivirus symptom determinant in plant cells during infection

Abstract

Geminiviruses are DNA viruses that cause severe diseases in diverse species of plants, resulting in considerable agricultural losses worldwide. C4 proteins are a major symptom determinant in several geminiviruses, including Beet severe curly top virus (BSCTV). Here, we uncovered a novel mechanism by which danger peptide signaling enhances the internalization of BSCTV C4 in plant cells. Previous studies showed that this signaling is important for activation of bacterium- and fungus-triggered immune responses, but its function in plant-virus interactions was previously unknown. Pep1 RECEPTOR1 (PEPR1) and PEPR2 are receptor kinases recognized by Peps (plant elicitor peptides) in the danger peptide pathway. We found that BSCTV C4 up-regulated and interacted with PEPR2 but not PEPR1. The Pep1-PEPR2 complex stimulated the internalization of C4 in both Arabidopsis and Nicotiana benthamiana cells. Furthermore, C4 induced callus formation in Arabidopsis, which was suppressed by PEPR2 overexpression but enhanced in the pepr2 mutants. In the presence of Pep1, overexpression of PEPR2 suppressed BSCTV infection in N. benthamiana. Exogenous Pep1 also reduced BSCTV infection in Arabidopsis in a PEPR2-dependent manner. Thus, PEPR2 recognizes the symptom determinant C4 and enhances its internalization mediated by danger peptides, suppressing BSCTV infection.