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.

Tomato Yellow Leaf Curl Virus V2 Protein Plays a Critical Role in the Nuclear Export of V1 Protein and Viral Systemic Infection

“…Geminiviruses are a group of plant viruses with a circular, single-stranded DNA genome. Viruses in this family cause devastating diseases in crop plants, leading to worldwide agricultural losses (Nakhla and Maxwell, 1997;Moriones and Navas-Castillo, 2000;Gafni, 2003;Fauquet et al, 2008;Glick et al, 2009;Fondong, 2019;Zeng et al, 2020). While viral protein synthesis occurs in the cytoplasm, replication of geminiviruses occurs in the nucleus of infected host cells (Hanley-Bowdoin et al, 2013).…”

Small but mighty: Functional landscape of the versatile geminivirus-encoded C4 protein

“…A close homologue of BAM1, CLAVATA 1 (CLV1), interacts with C4 from BSCTV, which may interfere with the downstream signaling pathway [ 8 ]. This same C4 protein also interacts with Pep1 RECEPTOR 2 (PEPR2), one of 2 receptors of the plant endogenous peptide Pep1 [ 52 – 54 ]. Pep1 acts as a damage-associated molecular pattern (DAMP), and its perception activates DAMP-triggered immunity (reviewed in [ 55 ]).…”

“…Pep1 acts as a damage-associated molecular pattern (DAMP), and its perception activates DAMP-triggered immunity (reviewed in [ 55 ]). Strikingly, overexpression of PEPR2 and its activation by exogenously applied Pep1 promotes the internalization of C4 from the plasma membrane, and has an antiviral effect [ 54 ], which prompts the speculation that PEPR2 might modify C4 to trigger its plasma membrane release and therefore interfere with its virulence function. Of note, phosphorylation-dependent detachment of N-myristoylated proteins from the plasma membrane occurs in animals [ 56 ], raising the idea that PEPR2 might phosphorylate and free C4 following perception of Pep1 and activation of its intracellular kinase domain.…”

“…The physical association of C4/AC4 proteins with the intracellular domain of RLKs seems to be an extended phenomenon; whether these interactions are specific for a given C4/AC4-RLK combination, or, on the contrary, C4/AC4 proteins target the conserved kinase domain of RLKs and hence can broadly bind members of this protein family is at this point unclear. Nevertheless, the finding that C4 from BSCTV interacts with both CLV1 and PEPR2 [ 8 , 54 ] and that C4 from TYLCV can associate with a number of RLKs from Arabidopsis [ 50 ] seems to favor the latter; certain C4/AC4-RLK interactions might have been selected for in specific geminivirus/plant pathosystems.…”

Protein modification: A critical modulator in the interaction between geminiviruses and host plants

“…The S‐acylated form of BSCTV ( Beet severe curly top virus ) C4 interacts with Clavata 1 (CLV1), an RLK involved in meristem maintenance, resulting in abnormal shoot development during virus infection (Li et al, 2018). S‐acylation on BSCTV C4 also contributes to its interaction with Pep1 receptor 2 (PEPR2) on the plasma membrane, for sequential internalization of C4 in response to the danger peptide signalling (Zeng et al, 2020). Similarly, S‐acylation mediates the localization of MYMV ( Mungbean yellow mosaic virus ) AC4 on the plasma membrane, where it interacts with BAM1 for suppression of intercellular movement of RNAi during virus infection (Carluccio, Prigigallo, Rosas‐Diaz, Lozano‐Duran, & Stavolone, 2018).…”