The Phytophthora infestans AVR2 Effector Escapes R2 Recognition Through Effector Disordering

Abstract

Intrinsic disorder is a common structural characteristic of proteins and a central player in the biochemical processes of species. However, the role of intrinsic disorder in the evolution of plant-pathogen interactions is rarely investigated. Here, we explored the role of intrinsic disorder in the development of the pathogenicity in the RXLR AVR2 effector of Phytophthora infestans. We found AVR2 exhibited high nucleotide diversity generated by point mutation, early-termination, altered start codon, deletion/insertion, and intragenic recombination and is predicted to be an intrinsically disordered protein. AVR2 amino acid sequences conferring a virulent phenotype had a higher disorder tendency in both the N- and C-terminal regions compared with sequences conferring an avirulent phenotype. In addition, we also found virulent AVR2 mutants gained one or two short linear interaction motifs, the critical components of disordered proteins required for protein-protein interactions. Furthermore, virulent AVR2 mutants were predicted to be unstable and have a short protein half-life. Taken together, these results support the notion that intrinsic disorder is important for the effector function of pathogens and demonstrate that SLiM-mediated protein-protein interaction in the C-terminal effector domain might contribute greatly to the evasion of resistance-protein detection in P. infestans.

Evidence for a synergistic effect of post‐translational modifications and genomic composition of eEF‐1α on the adaptation of Phytophthora infestans

“…The long spatial distance between cysteine residues may contribute to the lack of disulfide bonds in the eEF-1α protein. This lack of disulfide bonds reduces the stability of the eEF-1α protein, which is consistent with the analysis that shows the elongation protein is highly disordered in P. infestans (Figure 4f) and some other species (Ramesh & Sattlegger, 2020;Soares et al, 2009;Yang et al, 2020).…”

“…Colonies with single and expected amplicon size were sequenced by GenScript Biological Technology Co., Ltd. (GenScript, Nanjing, China) using an ABI3730 automated DNA sequencer (Applied Biosystems, USA). Details of purification and sequencing are described in previous publications (Wang et al., 2020; Yang et al, 2020).…”

The PTI to ETI Continuum in Phytophthora-Plant Interactions

“…Avr2 is a multiallelic highly divergent class of RXLR effectors that are recognized by the NB-LRR type R protein, R2 (Yang et al, 2020). As described above, PiAvr2 promotes ETS by modulating BR hormone signaling.…”

“…P. infestans strains, virulent on R2 containing potatoes were found to either suppress Avr2 expression or carry a distinct variant of Avr2 that eludes R2 mediated perception (Gilroy et al, 2011a). Recently, Yang et al (2020) discovered that virulent and avirulent Avr2 variants have different protein structures and virulent Avr2 are in fact intrinsically disordered proteins (IDPs). IDPs carry intrinsically disordered regions (IDRs) that may endow these proteins to have functional and evolutionary advantages over structured proteins.…”

“…IDP-type Avr2 variants are predicted to be unstable and have a short protein half-life. The authors have suggested that these properties enable virulent forms of Avr2 effectors to elude recognition by R2 (Yang et al, 2020). This is an excellent example of effector evolution to circumvent ETI and cause ETS.…”