mTOR complex 1 implicated in aphid/Buchnera host/symbiont integration

Edward B. James, Honglin Feng, Alexandra Wilson

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Obligate nutritional endosymbioses are arguably the most intimate of all interspecific associations. While many insect nutritional endosymbioses are well studied, a full picture of how two disparate organisms, a bacterial endosymbiont and a eukaryotic host, are integrated is still lacking. The mTOR pathway is known to integrate nutritional conditions with cell growth and survival in eukaryotes. Characterization and localization of amino acid transporters in aphids suggest the mTOR pathway as a point of integration between an aphid host and its amino acid-provisioning endosymbiont Buchnera aphidicola. The mTOR pathway is unannotated in aphids and unstudied in any nutritional endosymbiosis. We annotated mTOR pathway genes in two aphid species, Acyrthosiphon pisum and Myzus persicae, using both BLASTp searches and Hidden Markov Models. Using previously collected RNAseq data we constructed new reference transcriptomes for bacteriocyte, gut, and whole insect tissue for three lines of M. persicae. Annotation of the mTOR pathway identified homologs of all known invertebrate mTOR genes in both aphid species with some duplications. Differential expression analysis showed that genes specific to the amino acid-sensitive mTOR Complex 1 were more highly expressed in bacteriocytes than genes specific to the amino acid-insensitive mTOR Complex 2. Almost all mTOR genes involved in sensing amino acids showed higher expression in bacteriocytes than in whole insect tissue. When compared to gut, the putative glutamine/ arginine sensing transporter ACYPI000333, an ortholog of SLC38A9, showed 6.5 times higher expression in bacteriocytes. Our results suggest that the mTOR pathway may be functionally important in mediating integration of Buchnera into aphid growth and reproduction.

Original languageEnglish (US)
Pages (from-to)3083-3091
Number of pages9
JournalG3: Genes, Genomes, Genetics
Volume8
Issue number9
DOIs
StatePublished - Sep 1 2018

Fingerprint

Buchnera
Aphids
Symbiosis
Insects
Amino Acids
Genes
Amino Acid Transport Systems
Invertebrates
Growth
Eukaryota
Glutamine
Transcriptome
Reproduction
Arginine
Cell Survival

Keywords

  • MTORC1
  • Myzus persicae
  • Symbiosis
  • Transcriptome

ASJC Scopus subject areas

  • Molecular Biology
  • Genetics
  • Genetics(clinical)

Cite this

mTOR complex 1 implicated in aphid/Buchnera host/symbiont integration. / James, Edward B.; Feng, Honglin; Wilson, Alexandra.

In: G3: Genes, Genomes, Genetics, Vol. 8, No. 9, 01.09.2018, p. 3083-3091.

Research output: Contribution to journalArticle

James, Edward B. ; Feng, Honglin ; Wilson, Alexandra. / mTOR complex 1 implicated in aphid/Buchnera host/symbiont integration. In: G3: Genes, Genomes, Genetics. 2018 ; Vol. 8, No. 9. pp. 3083-3091.
@article{eb18731e8df3469384535cc8b38f0fc6,
title = "mTOR complex 1 implicated in aphid/Buchnera host/symbiont integration",
abstract = "Obligate nutritional endosymbioses are arguably the most intimate of all interspecific associations. While many insect nutritional endosymbioses are well studied, a full picture of how two disparate organisms, a bacterial endosymbiont and a eukaryotic host, are integrated is still lacking. The mTOR pathway is known to integrate nutritional conditions with cell growth and survival in eukaryotes. Characterization and localization of amino acid transporters in aphids suggest the mTOR pathway as a point of integration between an aphid host and its amino acid-provisioning endosymbiont Buchnera aphidicola. The mTOR pathway is unannotated in aphids and unstudied in any nutritional endosymbiosis. We annotated mTOR pathway genes in two aphid species, Acyrthosiphon pisum and Myzus persicae, using both BLASTp searches and Hidden Markov Models. Using previously collected RNAseq data we constructed new reference transcriptomes for bacteriocyte, gut, and whole insect tissue for three lines of M. persicae. Annotation of the mTOR pathway identified homologs of all known invertebrate mTOR genes in both aphid species with some duplications. Differential expression analysis showed that genes specific to the amino acid-sensitive mTOR Complex 1 were more highly expressed in bacteriocytes than genes specific to the amino acid-insensitive mTOR Complex 2. Almost all mTOR genes involved in sensing amino acids showed higher expression in bacteriocytes than in whole insect tissue. When compared to gut, the putative glutamine/ arginine sensing transporter ACYPI000333, an ortholog of SLC38A9, showed 6.5 times higher expression in bacteriocytes. Our results suggest that the mTOR pathway may be functionally important in mediating integration of Buchnera into aphid growth and reproduction.",
keywords = "MTORC1, Myzus persicae, Symbiosis, Transcriptome",
author = "James, {Edward B.} and Honglin Feng and Alexandra Wilson",
year = "2018",
month = "9",
day = "1",
doi = "10.1534/g3.118.200398",
language = "English (US)",
volume = "8",
pages = "3083--3091",
journal = "G3 (Bethesda, Md.)",
issn = "2160-1836",
publisher = "Genetics Society of America",
number = "9",

}

TY - JOUR

T1 - mTOR complex 1 implicated in aphid/Buchnera host/symbiont integration

AU - James, Edward B.

AU - Feng, Honglin

AU - Wilson, Alexandra

PY - 2018/9/1

Y1 - 2018/9/1

N2 - Obligate nutritional endosymbioses are arguably the most intimate of all interspecific associations. While many insect nutritional endosymbioses are well studied, a full picture of how two disparate organisms, a bacterial endosymbiont and a eukaryotic host, are integrated is still lacking. The mTOR pathway is known to integrate nutritional conditions with cell growth and survival in eukaryotes. Characterization and localization of amino acid transporters in aphids suggest the mTOR pathway as a point of integration between an aphid host and its amino acid-provisioning endosymbiont Buchnera aphidicola. The mTOR pathway is unannotated in aphids and unstudied in any nutritional endosymbiosis. We annotated mTOR pathway genes in two aphid species, Acyrthosiphon pisum and Myzus persicae, using both BLASTp searches and Hidden Markov Models. Using previously collected RNAseq data we constructed new reference transcriptomes for bacteriocyte, gut, and whole insect tissue for three lines of M. persicae. Annotation of the mTOR pathway identified homologs of all known invertebrate mTOR genes in both aphid species with some duplications. Differential expression analysis showed that genes specific to the amino acid-sensitive mTOR Complex 1 were more highly expressed in bacteriocytes than genes specific to the amino acid-insensitive mTOR Complex 2. Almost all mTOR genes involved in sensing amino acids showed higher expression in bacteriocytes than in whole insect tissue. When compared to gut, the putative glutamine/ arginine sensing transporter ACYPI000333, an ortholog of SLC38A9, showed 6.5 times higher expression in bacteriocytes. Our results suggest that the mTOR pathway may be functionally important in mediating integration of Buchnera into aphid growth and reproduction.

AB - Obligate nutritional endosymbioses are arguably the most intimate of all interspecific associations. While many insect nutritional endosymbioses are well studied, a full picture of how two disparate organisms, a bacterial endosymbiont and a eukaryotic host, are integrated is still lacking. The mTOR pathway is known to integrate nutritional conditions with cell growth and survival in eukaryotes. Characterization and localization of amino acid transporters in aphids suggest the mTOR pathway as a point of integration between an aphid host and its amino acid-provisioning endosymbiont Buchnera aphidicola. The mTOR pathway is unannotated in aphids and unstudied in any nutritional endosymbiosis. We annotated mTOR pathway genes in two aphid species, Acyrthosiphon pisum and Myzus persicae, using both BLASTp searches and Hidden Markov Models. Using previously collected RNAseq data we constructed new reference transcriptomes for bacteriocyte, gut, and whole insect tissue for three lines of M. persicae. Annotation of the mTOR pathway identified homologs of all known invertebrate mTOR genes in both aphid species with some duplications. Differential expression analysis showed that genes specific to the amino acid-sensitive mTOR Complex 1 were more highly expressed in bacteriocytes than genes specific to the amino acid-insensitive mTOR Complex 2. Almost all mTOR genes involved in sensing amino acids showed higher expression in bacteriocytes than in whole insect tissue. When compared to gut, the putative glutamine/ arginine sensing transporter ACYPI000333, an ortholog of SLC38A9, showed 6.5 times higher expression in bacteriocytes. Our results suggest that the mTOR pathway may be functionally important in mediating integration of Buchnera into aphid growth and reproduction.

KW - MTORC1

KW - Myzus persicae

KW - Symbiosis

KW - Transcriptome

UR - http://www.scopus.com/inward/record.url?scp=85052574944&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85052574944&partnerID=8YFLogxK

U2 - 10.1534/g3.118.200398

DO - 10.1534/g3.118.200398

M3 - Article

VL - 8

SP - 3083

EP - 3091

JO - G3 (Bethesda, Md.)

JF - G3 (Bethesda, Md.)

SN - 2160-1836

IS - 9

ER -