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Open Access Research article

Tyrosine pathway regulation is host-mediated in the pea aphid symbiosis during late embryonic and early larval development

Andréane Rabatel13, Gérard Febvay23, Karen Gaget23, Gabrielle Duport23, Patrice Baa-Puyoulet23, Panagiotis Sapountzis23, Nadia Bendridi13, Marjolaine Rey23, Yvan Rahbé234, Hubert Charles134, Federica Calevro13* and Stefano Colella23*

Author Affiliations

1 Insa-Lyon, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, Villeurbanne, F-69621, France

2 Inra, UMR203 BF2I, Biologie Fonctionnelle Insectes et Interactions, Villeurbanne, F-69621, France

3 Université de Lyon, Lyon, F-69000, France

4 Inria Rhône-Alpes, Bamboo, Monbonnot Saint-Martin, F-38330, France

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BMC Genomics 2013, 14:235  doi:10.1186/1471-2164-14-235

Published: 10 April 2013

Abstract

Background

Nutritional symbioses play a central role in insects’ adaptation to specialized diets and in their evolutionary success. The obligatory symbiosis between the pea aphid, Acyrthosiphon pisum, and the bacterium, Buchnera aphidicola, is no exception as it enables this important agricultural pest insect to develop on a diet exclusively based on plant phloem sap. The symbiotic bacteria provide the host with essential amino acids lacking in its diet but necessary for the rapid embryonic growth seen in the parthenogenetic viviparous reproduction of aphids. The aphid furnishes, in exchange, non-essential amino acids and other important metabolites. Understanding the regulations acting on this integrated metabolic system during the development of this insect is essential in elucidating aphid biology.

Results

We used a microarray-based approach to analyse gene expression in the late embryonic and the early larval stages of the pea aphid, characterizing, for the first time, the transcriptional profiles in these developmental phases. Our analyses allowed us to identify key genes in the phenylalanine, tyrosine and dopamine pathways and we identified ACYPI004243, one of the four genes encoding for the aspartate transaminase (E.C. 2.6.1.1), as specifically regulated during development. Indeed, the tyrosine biosynthetic pathway is crucial for the symbiotic metabolism as it is shared between the two partners, all the precursors being produced by B. aphidicola. Our microarray data are supported by HPLC amino acid analyses demonstrating an accumulation of tyrosine at the same developmental stages, with an up-regulation of the tyrosine biosynthetic genes. Tyrosine is also essential for the synthesis of cuticular proteins and it is an important precursor for cuticle maturation: together with the up-regulation of tyrosine biosynthesis, we observed an up-regulation of cuticular genes expression. We were also able to identify some amino acid transporter genes which are essential for the switch over to the late embryonic stages in pea aphid development.

Conclusions

Our data show that, in the development of A. pisum, a specific host gene set regulates the biosynthetic pathways of amino acids, demonstrating how the regulation of gene expression enables an insect to control the production of metabolites crucial for its own development and symbiotic metabolism.

Keywords:
Symbiosis; Pea aphid; Metabolism; Development; Viviparous parthenogenesis; Amino acids; Tyrosine pathway; Cuticle formation; Microarrays transcriptome analysis