Novel male-biased expression in paralogs of the aphid slimfast nutrient amino acid transporter expansion

The whitefly (Bemisia tabaci) is a cosmopolitan and devastating pest of agricultural crops and ornamentals. B. tabaci causes extensive damage by feeding on phloem and by transmitting plant viruses. Like many other organisms, insects depend on amino acid transporters (AATs) to transport amino acids into and out of its cells. We present a genome-wide and transcriptome-wide investigation of the following two families of AATs in B. tabaci biotype B: amino acid/auxin permease (AAAP) and amino acid/polyamine/organocation (APC). A total of 14 putative APCs and 25 putative AAAPs were identified, and a 10-paralog B. tabaci-specific expansion of AAAPs was found by maximum likelihood phylogeny. Detailed gene structure information revealed that 9 members of the B. tabaci-specific AAAP family expansion closely situated on a same scaffold. Expression profiling of the B. tabaci B APC and AAAP genes as affected by stage and plant host showed diverse expression patterns. The analysis of evolutionary rates indicated that purifying selection can explain the B. tabaci-specific AAAP expansion. RNA interference (RNAi)-mediated suppression of two AAAP genes (BtAAAP15 and BtAAAP21) significantly increased the mortality of B. tabaci B adults. The results provide a foundation for future functional analysis of APC and AAAP genes in B. tabaci.

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“…dN/dS < 1 demonstrates purifying selection; dN/dS = 1 indicates neutral selection and dN/dS > 1 demonstrates positive selection 12-13.…”

Section: Methodsmentioning

confidence: 99%

Genome-wide Identification and Expression Analysis of Amino Acid Transporters in the Whitefly, Bemisia tabaci (Gennadius)

et al. 2017

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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%

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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“…S1). Previously we established that the A. pisum genome contains 40 putative nutrient amino acid transporters (AATs) that belong to the amino acid polyamine organocation (APC) superfamily (21,22). On the basis of bacteriocyte gene-expression analyses (16,21,23,24) and a quantitative proteome analysis (25), we hypothesize that five transporters have an important functional role in bacteriocytes.…”

mentioning

confidence: 99%

Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts

Price

Feng

Baker

et al. 2013

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

107

158

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Endosymbiotic associations have played a major role in evolution. However, the molecular basis for the biochemical interdependence of these associations remains poorly understood. The aphid–Buchnera endosymbiosis provides a powerful system to elucidate how these symbioses are regulated. In aphids, the supply of essential amino acids depends on an ancient nutritional symbiotic association with the gamma-proteobacterium Buchnera aphidicola. Buchnera cells are densely packed in specialized aphid bacteriocyte cells. Here we confirm that five putative amino acid transporters are highly expressed and/or highly enriched in Acyrthosiphon pisum bacteriocyte tissues. When expressed in Xenopus laevis oocytes, two bacteriocyte amino acid transporters displayed significant levels of glutamine uptake, with transporter ACYPI001018, LOC100159667 (named here as Acyrthosiphon pisum glutamine transporter 1, ApGLNT1) functioning as the most active glutamine transporter. Transporter ApGLNT1 has narrow substrate selectivity, with high glutamine and low arginine transport capacity. Notably, ApGLNT1 has high binding affinity for arginine, and arginine acts as a competitive inhibitor for glutamine transport. Using immunocytochemistry, we show that ApGLNT1 is localized predominantly to the bacteriocyte plasma membrane, a location consistent with the transport of glutamine from A. pisum hemolymph to the bacteriocyte cytoplasm. On the basis of functional transport data and localization, we propose a substrate feedback inhibition model in which the accumulation of the essential amino acid arginine in A. pisum hemolymph reduces the transport of the precursor glutamine into bacteriocytes, thereby regulating amino acid biosynthesis in the bacteriocyte. Structural similarities in the arrangement of hosts and symbionts across endosymbiotic systems suggest that substrate feedback inhibition may be mechanistically important in other endosymbioses.

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Novel male-biased expression in paralogs of the aphid slimfast nutrient amino acid transporter expansion

Cited by 11 publications

References 53 publications

Genome-wide Identification and Expression Analysis of Amino Acid Transporters in the Whitefly, Bemisia tabaci (Gennadius)

Genome-wide Identification and Expression Analysis of Amino Acid Transporters in the Whitefly, Bemisia tabaci (Gennadius)

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

Aphid amino acid transporter regulates glutamine supply to intracellular bacterial symbionts

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