Amino acid transporter expansions associated with the evolution of obligate endosymbiosis in sap-feeding insects (Hemiptera: sternorrhyncha)

Dahan, Romain A.; Duncan, Rebecca P.; Wilson, Alex C. C.; Dávalos, Liliana M.

doi:10.1186/s12862-015-0315-3

Cited by 25 publications

(29 citation statements)

References 53 publications

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“…Primary symbionts facilitate exploitation of niche resources that are otherwise unavailable to their insect host. Endosymbionts may share metabolic pathways to produce essential amino acids lacking in the insect diet, such as Candidatus Carsonella ruddii and Buchnera aphidicola symbionts of psyllids and aphids, respectively (Wilson et al, 2006; Dahan et al, 2015). They may also aid in the breakdown of cellulose into accessible sugars, as in the complexes of bacteria and yeast found in termite guts.…”

Section: Discussionmentioning

confidence: 99%

Annotation of the Asian Citrus Psyllid Genome Reveals a Reduced Innate Immune System

2016

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Citrus production worldwide is currently facing significant losses due to citrus greening disease, also known as Huanglongbing. The citrus greening bacteria, Candidatus Liberibacter asiaticus (CLas), is a persistent propagative pathogen transmitted by the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae). Hemipterans characterized to date lack a number of insect immune genes, including those associated with the Imd pathway targeting Gram-negative bacteria. The D. citri draft genome was used to characterize the immune defense genes present in D. citri. Predicted mRNAs identified by screening the published D. citri annotated draft genome were manually searched using a custom database of immune genes from previously annotated insect genomes. Toll and JAK/STAT pathways, general defense genes Dual oxidase, Nitric oxide synthase, prophenoloxidase, and cellular immune defense genes were present in D. citri. In contrast, D. citri lacked genes for the Imd pathway, most antimicrobial peptides, 1,3-β-glucan recognition proteins (GNBPs), and complete peptidoglycan recognition proteins. These data suggest that D. citri has a reduced immune capability similar to that observed in A. pisum, P. humanus, and R. prolixus. The absence of immune system genes from the D. citri genome may facilitate CLas infections, and is possibly compensated for by their relationship with their microbial endosymbionts.

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Section: Discussionmentioning

confidence: 99%

Annotation of the Asian Citrus Psyllid Genome Reveals a Reduced Innate Immune System

2016

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“…Recent work in insect nutritional endosymbionts has focused on the evolution of nutrient amino acid transporters in the genomes of insects that feed on plant sap (29)(30)(31)(32). Those studies find that the evolutionary history of amino acid transporter genes in plant sap-feeding insects is dynamic with respect to both duplication events and the recruitment of duplicated genes to the host/symbiont interface (31).…”

Section: Acquisitionmentioning

confidence: 99%

“…Those studies find that the evolutionary history of amino acid transporter genes in plant sap-feeding insects is dynamic with respect to both duplication events and the recruitment of duplicated genes to the host/symbiont interface (31). The dynamic evolution of amino acid transporters in these insects, including some very recent duplications in aphids (32), demonstrates that despite millions of years of host/ endosymbiont coevolution, host genomes are in flux (Fig. 3).…”

Section: Acquisitionmentioning

confidence: 99%

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Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

Wilson

Duncan

2015

Proc. Natl. Acad. Sci. U.S.A.

128

118

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The role of symbiosis in bacterial symbiont genome evolution is well understood, yet the ways that symbiosis shapes host genomes or more particularly, host/symbiont genome coevolution in the holobiont is only now being revealed. Here, we identify three coevolutionary signatures that characterize holobiont genomes. The first signature, host/symbiont collaboration, arises when completion of essential pathways requires host/endosymbiont genome complementarity. Metabolic collaboration has evolved numerous times in the pathways of amino acid and vitamin biosynthesis. Here, we highlight collaboration in branched-chain amino acid and pantothenate (vitamin B5) biosynthesis. The second coevolutionary signature is acquisition, referring to the observation that holobiont genomes acquire novel genetic material through various means, including gene duplication, lateral gene transfer from bacteria that are not their current obligate symbionts, and full or partial endosymbiont replacement. The third signature, constraint, introduces the idea that holobiont genome evolution is constrained by the processes governing symbiont genome evolution. In addition, we propose that collaboration is constrained by the expression profile of the cell lineage from which endosymbiont-containing host cells, called bacteriocytes, are derived. In particular, we propose that such differences in bacteriocyte cell lineage may explain differences in patterns of host/endosymbiont metabolic collaboration between the sap-feeding suborders Sternorrhyncha and Auchenorrhynca. Finally, we review recent studies at the frontier of symbiosis research that are applying functional genomic approaches to characterization of the developmental and cellular mechanisms of host/endosymbiont integration, work that heralds a new era in symbiosis research.

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“…We show that species tree heterogeneity misleads inference of gene duplication and loss rates, with implications for tests of ecological associations (e.g., Chang and Duda 2012;Dahan et al 2015;Ramasamy et al 2016). Although the influence of tree heterogeneity on analyses of speciation rates has been demonstrated (Rabosky and Goldberg 2015;Rojas et al 2018), the conflation of tree heterogeneity with rate shifts in multi-gene family evolution had not been previously demonstrated.…”

Section: Discussionmentioning

confidence: 76%

Species tree disequilibrium positively misleads models of gene family evolution

Lauterbur

Heder

Yohe

et al. 2020

Preprint

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Gene duplication is a key source of evolutionary innovation, and multigene families evolve in a birth-death process, continuously duplicating and pseudogenizing through time. To empirically test hypotheses about adaptive expansion and contraction of multigene families across species, models infer gene gain and loss in light of speciation events and these inferred gene family expansions may lead to interpretations of adaptations in particular lineages. While the relative abundance of a gene subfamily in the subgenome may reflect its functional importance, tests based on this expectation can be confounded by the complex relationship between the birth-death process of gene subfamily evolution and the species phylogeny. Using simulations, we confirmed tree heterogeneity as a confounding factor in inferring multi-gene adaptation, causing spurious associations between shifts in birth-death rate and lineages with higher branching rates. We then used the olfactory receptor (OR) repertoire, the largest gene family in the mammalian genome, of different bat species with divergent diets to test whether expansions in olfactory receptors are associated with shifts to frugivorous diets.After accounting for tree heterogeneity, we robustly inferred that certain OR subfamilies exhibited expansions associated with dietary shifts to frugivory. Taken together, these results suggest ecological correlates of individual OR gene subfamilies can be identified, setting the stage for detailed inquiry into within-subfamily functional differences.

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Amino acid transporter expansions associated with the evolution of obligate endosymbiosis in sap-feeding insects (Hemiptera: sternorrhyncha)

Cited by 25 publications

References 53 publications

Annotation of the Asian Citrus Psyllid Genome Reveals a Reduced Innate Immune System

Annotation of the Asian Citrus Psyllid Genome Reveals a Reduced Innate Immune System

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

Species tree disequilibrium positively misleads models of gene family evolution

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