Targets of selection in a disease resistance network in wild tomatoes

Abstract

Studies combining comparative genomics and information on biochemical pathways have revealed that protein evolution can be affected by the amount of pleiotropy associated with a particular gene. The amount of pleiotropy, in turn, can be a function of the position at which a gene operates in a pathway and the pathway structure. Genes that serve as convergence points and have several partners (so-called hubs) often show the greatest constraint and hence the slowest rate of protein evolution. In this article, we have studied five genes (Pto, Fen, Rin4, Prf and Pfi) in a defence signalling network in a wild tomato species, Solanum peruvianum. These proteins operate together and contribute to bacterial resistance in tomato. We predicted that Prf (and possibly Pfi), which serves as a convergence point for upstream signals, should show greater evolutionary constraint. However, we found instead that two of the genes which potentially interact with pathogen ligands, Rin4 and Fen, have evolved under strong evolutionary constraint, whereas Prf and Pfi, which probably function further downstream in the network, show evidence of balancing selection. This counterintuitive observation may be probable in pathogen defence networks, because pathogens may target positions throughout resistance networks to manipulate or nullify host resistance, thereby leaving a molecular signature of host-parasite co-evolution throughout a single network.