Effector Avr4 in Phytophthora infestans Escapes Host Immunity Mainly Through Early Termination

Abstract

Effector genes play critical roles in the antagonistic interactions between plants and pathogens. However, knowledge of mutation mechanisms and evolutionary processes in effector genes and the contribution of climatic factors to the evolution of effector genes are fragmented but important in sustainable management of plant diseases and securing food supply under changing climates. Here, we used a population genetic approach to explore the evolution of the Avr4 gene in Phytophthora infestans, the causal agent of potato blight. We found that the Avr4 gene exhibited a high genetic diversity generated by point mutation and sequence deletion. Frameshifts caused by a single base-pair deletion at the 194th nucleotide position generate two stop codons, truncating almost the entire C-terminal, which is important for effector function and R4 recognition in all sequences. The effector is under natural selection for adaptation supported by comparative analyses of population differentiation (FST) and isolation-by-distance between Avr4 sequences and simple sequence repeat marker loci. Furthermore, we found that local air temperature was positively associated with pairwise FST in the Avr4 sequences. These results suggest that the evolution of the effector gene is influenced by local air temperature, and the C-terminal truncation is one of the main mutation mechanisms in the P. infestans effector gene to circumvent the immune response of potato plants. The implication of these results to agricultural and natural sustainability in future climate conditions is discussed.

Genetic variation along an altitudinal gradient in the Phytophthora infestans effector gene Pi02860

“…For example, the effector function of P. syringae AvrRpt2 to Arabidopsis RPS2 resistance disappeared when plants were grown for 3 weeks under 28°C ( Wang et al, 2009 ). The strong association of annual mean temperature in the collection sites with nucleotide diversity and/or population differentiation of Avr1 ( Shen et al, 2021 ), Avr2 ( Yang et al, 2020 ), Avr3a ( Yang et al, 2018 ) and Avr4 ( Waheed et al, 2021 ) in P. infestans further supports that local air temperature could influence the evolution of effector genes.…”

“…To maintain these multifaceted functions, effector genes are expected to have a higher evolvability equipped by high genetic variation for quick adaptation to constantly changing biotic and abiotic environments. Indeed, previous studies have reported that the genetic variation in effector genes is higher than many other functional genes in P. infestans and other pathogen species, possibly due to a synergic effect of recombination ( Yang et al, 2018 ; Dale et al, 2019 ), plasticity ( Timilsina et al, 2020 ) and multiple mutation mechanisms including pseudogenization, point mutation, deletion, insertion and truncation ( Shen et al, 2021 ; Waheed et al, 2021 ). The physical locations of many effector genes in the sparse regions of genomes enriching with transposable elements provide unique opportunity for mutations to occur with a minimum fitness penalty to pathogen species ( Haas et al, 2009 ; Dong et al, 2015 ).…”

“…It is widely documented that pathogens in agricultural ecosystems are equipped with an array of mutation mechanisms to drive their escape from host immunity. For example, Phytophthora infestans Avr1 and Avr4 were removed from the effector repertoire by pseudogenization to escape the corresponding R1 and R4 detection in host ( van Poppel et al, 2008 ; Shen et al, 2021 ; Waheed et al, 2021 ). Phytophthora infestans Avr2 escapes host immunity by protein disordering through which shifts the effector from an avirulent type to virulent type ( Yang et al, 2020 ).…”

Mitochondrial Genome Contributes to the Thermal Adaptation of the Oomycete Phytophthora infestans

“…A higher degree of population differentiation in mtDNA than neutral genome represented by SSR provides further evidence supporting an adaptive evolution (Wu et al, 2016 ; Yang et al, 2018 ; Shen et al, 2021 ; Waheed et al, 2021 ) in the P. infestans molecules. Gene flow is the main evolutionary mechanism determining the population differentiation of species (Gao et al, 2020 ).…”

Single Amino Acid Substitution in the DNA Repairing Gene Radiation-Sensitive 4 Contributes to Ultraviolet Tolerance of a Plant Pathogen

“…Evolutionary strategies differ largely between conserved genes and other variant genes such as pathogenicity and tissue-specific genes ( Alrefai et al, 2007 ). For example, many housekeeping genes are conserved in evolution due to their essential roles in providing fundamental service to the survival of a cell ( Zhang and Li, 2004 ), whereas many effector genes of pathogens can quickly evolve in responding to host changes ( Waheed et al, 2021 ). Low genetic variation was found in the RAD4 gene studied.…”