Modelling of structures of ATR1-homologs from sister species of Hyaloperonospora arabidopsidis suggests different patterns for target-mediated and R-protein-mediated selection

The basal immune system of plants fights pathogens by recognising conserved pathogen-associated molecular patterns. To bypass this, pathogens secrete effectors into the host plant, of which some are sensed by resistance genes, triggering host defence reactions. Plant pathogens diversify by host jumping and co-speciation. Little is known about the functional adaptations of effectors to new targets after host jumping, and how R-protein and target-mediated adaptations might differ. In this study, 40 coding sequences of the ATR1 effector from 3 different oomycete species, Hyaloperonospora thlaspeos-perfoliati , H. crispula and H. arabidopsidis have been analysed. Forty-six positively selected sites were identified, when sequences from all the organisms were analysed together. In H. arabidopsidis , more sites are under positive selection in comparison to the other species, owing to an evolutionary arms race of ATR1 with RPP1 resistance proteins from Arabidopsis thaliana . The availability of crystal structure of ATR1 of H. arabidopsidis facilitated homology modelling of the ATR1 of H. thlaspeos-perfoliati and H. crispula . It was found that in all species, more than 90 % of the positively selected residues are on the protein surface. Interestingly, variability of ATR1 was low in H. thlaspeos-perfoliati and H. crispula paralogs, suggesting the absence of a corresponding R-protein in their hosts. The distribution pattern of selected and altered residues differed for the changes incited by the evolutionary arms race and those changes that occurred after adaptation to a new target following a host jump. While in the first case, they were evenly distributed, they were more concentrated around specific domains in the latter case, highlighting that different forces have been shaping ATR1 evolution during arms races and after host jumps.