TY - JOUR
T1 - Amino acid transporters implicated in endocytosis of Buchnera during symbiont transmission in the pea aphid
AU - Lu, Hsiao ling
AU - Chang, Chun che
AU - Wilson, Alex C.C.
N1 - Funding Information:
This work was supported by the following Grants from the Ministry of Science and Technology (102‑2917‑I‑002‑006, 104‑2811‑B‑002‑134, 105‑2811‑B‑002‑ 135 and 104‑2313‑B‑002‑022‑MY3) and the National Science Foundation (IOS‑1121847 and IOS‑1354154). The funding bodies had no role in the design of the study, or the collection, analysis, and interpretation of data.
Funding Information:
This work benefitted from useful discussions with Daniel Price, Rebecca Dun‑ can, Honglin Feng, Athula Wikramanayake, and Yi‑min Hsiao. We thank James Baker of the Confocal Microscopy Core facility in the Department of Biology at the University of Miami, Yi‑Chun Chuang of Technology Commons, College of Life Science, National Taiwan University, together with Lingyu Wang and Wei Wu for technical support. Financial support for the project came from Ministry of Science and Technology Awards 102‑2917‑I‑002‑006, 104‑2811‑B‑002‑134 and 105‑2811‑B‑002‑135 (to HLL), and 104‑2313‑B‑002‑022‑MY3 (to CC and to HLL) and National Science Foundation award IOS‑1121847 and IOS‑1354154 (to ACCW).
Publisher Copyright:
© 2016 The Author(s).
PY - 2016/11/21
Y1 - 2016/11/21
N2 - Background: Many insects host their obligate, maternally transmitted symbiotic bacteria in specialized cells called bacteriocytes. One of the best-studied insect nutritional endosymbioses is that of the aphid and its endosymbiont, Buchnera aphidicola. Aphids and Buchnera are metabolically and developmentally integrated, but the molecular mechanisms underlying Buchnera transmission and coordination with aphid development remain largely unknown. Previous work using electron microscopy to study aphid asexual embryogenesis has revealed that Buchnera transmission involves exocytosis from a maternal bacteriocyte followed by endocytotic uptake by a blastula. While the importance of exo- and endocytic cellular processes for symbiont transmission is clear, the molecular mechanisms that regulate these processes are not known. Here, we shed light on the molecular mechanisms that regulate Buchnera transmission and developmental integration. Results: We present the developmental atlas of ACYPI000536 and ACYPI008904 mRNAs during asexual embryogenesis in the pea aphid, Acyrthosiphon pisum. Immediately before Buchnera invasion, transcripts of both genes were detected by whole-mount in situ hybridization in the posterior syncytial nuclei of late blastula embryos. Following Buchnera invasion, expression of both genes was identified in the region occupied by Buchnera throughout embryogenesis. Notably during Buchnera migration, expression of both genes was not concomitant with the entirety of the bacterial mass but rather expression colocalized with Buchnera in the anterior region of the bacterial mass. In addition, we found that ACYPI000536 was expressed in nuclei at the leading edge of the bacterial mass, joining the bacterial mass in subsequent developmental stages. Finally, quantitative reverse transcription real-time PCR suggested that early in development both transcripts were maternally provisioned to embryos. Conclusions: We venture that ACYPI000536 and ACYPI008904 function as nutrient sensors at the site of symbiont invasion to facilitate TOR-pathway-mediated endocytosis of Buchnera by the aphid blastula. Our data support earlier reports of bacteriocyte determination involving a two-step recruitment process but suggest that the second wave of recruitment occurs earlier than previously described. Finally, our work highlights that bacteriocyte-enriched amino acid transporter paralogs have additionally been retained to play novel developmental roles in both symbiont recruitment and bacteriome development.
AB - Background: Many insects host their obligate, maternally transmitted symbiotic bacteria in specialized cells called bacteriocytes. One of the best-studied insect nutritional endosymbioses is that of the aphid and its endosymbiont, Buchnera aphidicola. Aphids and Buchnera are metabolically and developmentally integrated, but the molecular mechanisms underlying Buchnera transmission and coordination with aphid development remain largely unknown. Previous work using electron microscopy to study aphid asexual embryogenesis has revealed that Buchnera transmission involves exocytosis from a maternal bacteriocyte followed by endocytotic uptake by a blastula. While the importance of exo- and endocytic cellular processes for symbiont transmission is clear, the molecular mechanisms that regulate these processes are not known. Here, we shed light on the molecular mechanisms that regulate Buchnera transmission and developmental integration. Results: We present the developmental atlas of ACYPI000536 and ACYPI008904 mRNAs during asexual embryogenesis in the pea aphid, Acyrthosiphon pisum. Immediately before Buchnera invasion, transcripts of both genes were detected by whole-mount in situ hybridization in the posterior syncytial nuclei of late blastula embryos. Following Buchnera invasion, expression of both genes was identified in the region occupied by Buchnera throughout embryogenesis. Notably during Buchnera migration, expression of both genes was not concomitant with the entirety of the bacterial mass but rather expression colocalized with Buchnera in the anterior region of the bacterial mass. In addition, we found that ACYPI000536 was expressed in nuclei at the leading edge of the bacterial mass, joining the bacterial mass in subsequent developmental stages. Finally, quantitative reverse transcription real-time PCR suggested that early in development both transcripts were maternally provisioned to embryos. Conclusions: We venture that ACYPI000536 and ACYPI008904 function as nutrient sensors at the site of symbiont invasion to facilitate TOR-pathway-mediated endocytosis of Buchnera by the aphid blastula. Our data support earlier reports of bacteriocyte determination involving a two-step recruitment process but suggest that the second wave of recruitment occurs earlier than previously described. Finally, our work highlights that bacteriocyte-enriched amino acid transporter paralogs have additionally been retained to play novel developmental roles in both symbiont recruitment and bacteriome development.
KW - Amino acid transporter
KW - Aphid development
KW - Coevolution
KW - Host/symbiont developmental integration
KW - Symbiosis
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U2 - 10.1186/s13227-016-0061-7
DO - 10.1186/s13227-016-0061-7
M3 - Article
AN - SCOPUS:84997822714
VL - 7
JO - EvoDevo
JF - EvoDevo
SN - 2041-9139
IS - 1
M1 - 24
ER -