Plant manipulation through gall formation constrains amino acid transporter evolution in sap-feeding insects

Abstract

BackgroundThe herbivore lifestyle leads to encounters with plant toxins and requires mechanisms to overcome suboptimal nutrient availability in plant tissues. Although the evolution of bacterial endosymbiosis alleviated many of these challenges, the ability to manipulate plant nutrient status has evolved in lineages with and without nutritional symbionts. Whether and how these alternative nutrient acquisition strategies interact or constrain insect evolution is unknown. We studied the transcriptomes of galling and free-living aphidomorphs to characterize how amino acid transporter evolution is influenced by the ability to manipulate plant resource availability.ResultsUsing a comparative approach we found phylloxerids retain nearly all amino acid transporters as other aphidomorphs, despite loss of nutritional endosymbiosis. Free living species show more transporters than galling species within the same genus, family, or infraorder, indicating plant hosts influence the maintenance and evolution of nutrient transport within herbivores. Transcript profiles also show lineage specificity and suggest some genes may facilitate life without endosymbionts or the galling lifestyle.ConclusionsThe transcript abundance profiles we document across fluid feeding herbivores support plant host constraint on insect amino acid transporter evolution. Given amino acid uptake, transport, and catabolism underlie the success of herbivory as a life history strategy, this suggests that plant host nutrient quality, whether constitutive or induced, alters the selective environment surrounding the evolution and maintenance of endosymbiosis.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-1000-5) contains supplementary material, which is available to authorized users.

Phylloxerids share ancestral carotenoid biosynthesis genes of fungal origin with aphids and adelgids

“…This hypothesis is supported by the strong phylogenetic clustering of both genes of these three Sternorrhyncha families, which are separated from homologs of other arthropods and microorganisms (Figs 3 & 4 ). In addition, carotenoid gene-inferred phylogenetic relationships are consistent to what have been suggested among the three families and within the Phylloxeridae based on previous phylogenetic analysis [ 30 ]. Aphididae, Phylloxeridae, and Adelgidae are very closely related, with the latter two families considered to form a superfamily Phylloxeroidea, sister to Aphidoidea [ 35 ].…”

“…We used the pea aphid carotenoid cyclase/synthase (XP_001943170.1) and desaturase (XP_001943225.2) protein sequences as queries to search their homologs from the transcriptomes of nine Phylloxeridae species, including the grape phylloxera Daktulosphaira vitifoliae and eight Phylloxera spp. [ 30 ]. Transcripts of both carotenoid cyclase/synthase and desaturase genes were identified in all the nine species except no carotenoid desaturase was found in P .…”

“…Within Phylloxeridae, both previous studies and this one suggest 1) that some leaf-feeding Phylloxera species first switched to feeding on stem tissues and then recolonized stem organs across different hosts as they speciated, and 2) that in a different genus, D . vitifoliae is separated from all other Phylloxera species [ 30 ]. The more-recent occurrence of stem-galling Phylloxera species is further exemplified in their gaining of an extra 3-nt codon within the second exon of the cyclase/synthase coding region, compared to non-stem-galling Phylloxera species ( Fig 2 ), a potential molecular marker to distinguish stem-galling from leaf-galling Phylloxera spp.…”

“…Nine known species within Phylloxeridae were used for genomic DNA extraction. They were all collected from fields in the United States as previously described [ 30 ]. Briefly, these include eight Phylloxera species that form galls on Carya species and Daktulosphaira vitifoliae that galls both roots and leaves of Vitis species.…”

“…Previously, we generated whole-body transcriptomes of the nine Phylloxeridae species described above [ 30 ]. To identify Phylloxeridae carotenoid genes, we first used the Ac .…”