Portiera as a phylogenetic tool on whiteflies.. Portieragets wild: Genome instability provides insights into theevolution of both whiteflies and their endosymbionts.

Whiteflies (Hemiptera: Sternorrhyncha: Aleyrodidae) are a superfamily of small phloem-feeding insects. They rely on their primary endosymbionts Candidatus Portiera aleyrodidarum to produce essential amino acids not present in their diet. Portiera has been co-diverging with whiteflies since their origin and therefore reflects its host’s evolutionary history. Like in most primary endosymbionts, the genome of Portiera stays stable across the Aleyrodidae superfamily after millions of years of co-divergence. However, Portiera of the sweetpotato whitefly Bemisia tabaci has lost the ancestral genome order, reflecting a rare event in the endosymbiont evolution: the appearance of genome instability. To gain a better understanding of Portiera genome evolution, identify the time point in which genome instability appeared, and contribute to the reconstruction of whitefly phylogeny, we developed a new phylogenetic framework. It targeted five Portiera genes and determined the presence of the DNA polymerase proofreading subunit (dnaQ) gene, previously associated with genome instability, and two alternative gene rearrangements. Our results indicated that Portiera gene sequences provide a robust tool for studying inter-genera phylogenetic relationships in whiteflies. Using the new framework, we found that whitefly species from the Singhiella, Aleurolobus, and Bemisia genera form a monophyletic tribe, the Aleurolobini, and that their Portiera exhibit genome instability. This instability likely arose once in the common ancestor of the Aleurolobini tribe (at least 70 million years ago), drawing a link between the appearance of genome instability in Portiera and the switch from multi-bacteriocyte to a single-bacteriocyte mode of inheritance in this tribe.