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Front. Plant Sci. | doi: 10.3389/fpls.2019.01301

Differential Expression of Candidate Salivary Effector Genes in Pea Aphid Biotypes with Distinct Host Plant Specificity

 Hélène Boulain1, 2, Fabrice Legeai2, 3, Julie Jaquiéry2, Endrick Guy2, Stéphanie Morlière2, Jean-Christophe Simon2 and  Akiko Sugio2*
  • 1Swiss Federal Institute of Aquatic Science and Technology, Switzerland
  • 2INRA UMR1349 Institut de Génétique, Environnement et Protection des Plantes, France
  • 3Inria Rennes - Bretagne Atlantique Research Centre, France

Effector proteins play crucial roles in determining the outcome of various plant–parasite interactions. Aphids inject salivary effector proteins into plants to facilitate phloem feeding, but some proteins might trigger defence responses in certain plants. The pea aphid, Acyrthosiphon pisum, forms multiple biotypes, and each biotype is specialized to feed on a small number of closely-related legume species. Interestingly, all the previously-identified biotypes can feed on Vicia faba; hence, it serves as a universal host plant of A. pisum. We hypothesized that the salivary effector proteins have a key role in determining the compatibility between specific host species and A. pisum biotypes and that each biotype produces saliva containing a specific mixture of effector proteins due to differential expression of encoding genes. As the first step to address these hypotheses, we conducted two sets of RNA-seq experiments. RNA-seq analysis of dissected salivary glands from reference alfalfa- and pea-specialized A. pisum lines revealed common and line-specific repertoires of candidate salivary effector genes. Based on the results, we created an extended catalogue of A. pisum salivary effector candidates. Next, we used aphid head samples, which contain salivary glands, to examine biotype-specific expression patterns of candidate salivary genes. RNA-seq analysis of head samples of alfalfa- and pea-specialized biotypes, each represented by three genetically distinct aphid lines reared on either a universal or specific host plant, showed that a majority of the candidate salivary effector genes was expressed in both biotypes at a similar level. Nonetheless, we identified small sets of genes that were differentially regulated in a biotype-specific manner. Little host plant effect (universal vs. specific) was observed on the expression of candidate salivary genes. Analysis of previously-obtained genome re-sequenced data of the two biotypes revealed the copy number variations that might explain the differential expression of some candidate salivary genes. In addition, at least four candidate effector genes that were present in the alfalfa biotype but might not be encoded in the pea biotype were identified. This work sets the stage for future functional characterization of candidate genes potentially involved in the determination of plant specificity of pea aphid biotypes.

Keywords: Host-specificity, Transcriptomics, Copy Number Variation - CNV, Phytophagous insect, Effectors

Received: 09 Jul 2019; Accepted: 18 Sep 2019.

Copyright: © 2019 Boulain, Legeai, Jaquiéry, Guy, Morlière, Simon and Sugio. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Akiko Sugio, INRA UMR1349 Institut de Génétique, Environnement et Protection des Plantes, Le Rheu, 35327, France, akiko.sugio@inra.fr