Direct link between convergent evolution at sequence level and phenotypic level of septal pore cap in Agaricomycotina

Abstract

Several apparently homologous morphological characters are known to have independently evolved in different lineages multiple times. However, the genetic backgrounds of such morphological convergences are not well understood. To detect any correlated genes potentially responsible for morphological convergence at the phenotypic level, we focused on the morphology of the septal pore cap (SPC), which is involved in mycelias complex multicellularity in fungi. SPCs are classified into three morphological types: perforate, imperforate, and vesiculate. To understand what evolutionary events occurred at the sequence level during morphological convergence of perforate SPCs in Agaricomycotina, we examined sequence differences between species with different SPC types by comparative genomic analysis. If sequences from species with perforate SPCs formed a cluster, the associated gene might be involved in generating perforate SPCs in multiple lineages. Based on this assumption, we detected eight candidate genes, including an SPC-related gene, spc33. The results showed that some amino acid substitutions independently occurred in both lineages in which species with perforate SPCs emerged. From these results, we speculate that the amino acid substitutions in spc33 were critical in the emergence of perforate SPCs in multiple lineages. We also found that spc33 evolved just before imperforate SPC emergence based on homology search of spc33 and the species phylogeny. These findings illustrate the first step to clarifying the genetic basis of SPC morphological evolution. Our study contributes to both clarifying the genetic basis of morphological convergence and pioneering our understanding of fungal evolutionary morphology.