A Plasmopara viticola RXLR effector targets a chloroplast protein PsbP to inhibit ROS production in grapevine

Abstract

Pathogens secrete a large number of effectors that manipulate host processes to create an environment conducive to pathogen colonization. However, the underlying mechanisms by which Plasmopara viticola effectors manipulate host plant cells remain largely unclear. In this study, we reported that RXLR31154, a P. viticola RXLR effector, was highly expressed during the early stages of P. viticola infection. In our study, stable expression of RXLR31154 in grapevine (Vitis vinifera) and Nicotiana benthamiana promoted leaf colonization by P. viticola and Phytophthora capsici, respectively. By yeast two-hybrid screening, the 23-kDa oxygen-evolving enhancer 2 (VpOEE2 or VpPsbP), encoded by the PsbP gene, in Vitis piasezkii accession Liuba-8 was identified as a host target of RXLR31154. Overexpression of VpPsbP enhanced susceptibility to P. viticola in grapevine and P. capsici in N. benthamiana, and silencing of NbPsbPs, the homologs of PsbP in N. benthamiana, reduced P. capcisi colonization, indicating that PsbP is a susceptibility factor. RXLR31154 and VpPsbP protein were co-localized in the chloroplast. Moreover, VpPsbP reduced H 2 O 2 accumulation and activated the 1 O 2 signaling pathway in grapevine. RXLR31154 could stabilize PsbP. Together, our data revealed that RXLR31154 reduces H 2 O 2 accumulation and activates the 1 O 2 signaling pathway through stabilizing PsbP, thereby promoting disease.

Plasmopara viticola the Causal Agent of Downy Mildew of Grapevine: From Its Taxonomy to Disease Management

“…Evidence points to the potential for RXLR effectors to drive plant cell death following recognition by the corresponding R proteins or unknown mechanisms (Huang et al, 2019 ). Many of RXLR effectors have a second EER-motif (glutamic acid-glutamic acid-arginine optional amino acid motif) participating in the transport from the pathogen to its host, and at varying distance C-terminal to RXLR motif (Stassen and Van Den Ackerveken, 2011 ; Liu et al, 2021 ). Both RXLR and EER motifs are needed to access host cells (Kale and Tyler, 2011 ).…”

Effector Sntf2 Interacted with Chloroplast-Related Protein Mdycf39 Promoting the Colonization of Colletotrichum gloeosporioides in Apple Leaf

“…Different suborganelles in the host often become targets of pathogens [ 23 , 39 ]. Many effectors target different components of the PSII in the host, which interferes with electron transport and inhibits ROS production, interfering with plant defense [ 6 , 28 , 40 ]. The effector RXLR31154 of Plasmopara viticola targets PsbP (a factor of the oxygen-evolving complex of PSII) to inhibit H 2 O 2 production in a grapevine and enhance its susceptibility [ 6 ].…”

“…Many effectors target different components of the PSII in the host, which interferes with electron transport and inhibits ROS production, interfering with plant defense [ 6 , 28 , 40 ]. The effector RXLR31154 of Plasmopara viticola targets PsbP (a factor of the oxygen-evolving complex of PSII) to inhibit H 2 O 2 production in a grapevine and enhance its susceptibility [ 6 ]. In our study, we found that the effector Sntf2 of C. gloeosporioides migrated into the host’s chloroplasts and interacted with Mdycf39.…”

“…Plants have evolved intracellular nucleotide-binding leucine-rich-repeat receptors (NLRs) to recognize pathogen effectors directly or indirectly, leading to activation of the second line of defense, known as effector-triggered immunity (ETI) [ 2 ]. However, pathogens secrete a series of virulence effectors that interfere with the plant’s immune system, promoting pathogen invasion [ 5 , 6 ]. Hence, exploring the virulence mechanisms of effectors is important for revealing the infection strategies of plant pathogens.…”

“…Upon perception of pathogenic threat, chloroplast as the source of calcium, salicylic acid (SA), and reactive oxygen species (ROS) bursts communicates with the nucleus through retrograde signaling [ 24 ], mediates activation of plant immune signaling, and leads to the expression of defense-related genes [ 26 , 27 ]. To interfere with the function of chloroplasts in the interaction between the pathogens and the hosts, pathogens, including bacteria, viruses, fungi, and Oomycetes, have deployed effectors to target chloroplasts [ 6 , 23 , 27 , 28 , 29 ]. However, the underlying mechanisms with which effectors target chloroplasts to manipulate the host’s defenses have remained elusive in Colletotrichum .…”