Portiera getswild: Genome instability provides insights into the evolution of bothwhiteflies and their endosymbionts

Diego Santos-Garcia*, Natividad Mestre-Rincon, David Ouvrard, Einat Zchori-Fein, Shai Morin

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

12 Scopus citations

Abstract

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 codiverging 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 codivergence. However, Portiera of thewhitefly 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 ofwhitefly phylogeny,we developed a newphylogenetic 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 intergenera phylogenetic relationships in whiteflies. Using these new framework, we found that whitefly species from the Singhiella, Aleurolobus, and Bemisia genera form a monophyletic tribe, the Aleurolobini, and that their Portiera exhibitgenomeinstability. This instability likely aroseonce in the commonancestorof the Aleurolobini tribe (at least 70Ma), drawing a link between the appearance of genome instability in Portiera and the switch from multibacteriocyte to a singlebacteriocyte mode of inheritance in this tribe.

Original languageAmerican English
Pages (from-to)2107-2124
Number of pages18
JournalGenome Biology and Evolution
Volume12
Issue number11
DOIs
StatePublished - 2020

Bibliographical note

Funding Information:
The authors of this work would like to honor the memory of Prof. Dan Gerling (1936–2016), a pioneering and passionate researcher of the whitefly superfamily and its natural enemies. This work was supported by the Israel Science Foundation (Grant Nos. 1039/12 to S.M. and 484/17 to E.Z.-F.). D.S.-G. was a recipient of the Golda Meir Postdoctoral Fellowship from the Hebrew University of Jerusalem. We wish to acknowledge Dr Estrella Hernández Suárez and Dr Hélène Delate for supplying whitefly samples.

Publisher Copyright:
© The Author(s) 2020.

Keywords

  • Divergence dating
  • Genome stasis
  • Long-enduring taxon,molecular evolution
  • Symbiosis
  • Whitefly development
  • Whitefly systematics

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