Campus France Ulysses (907424D) to A.S. and J.C. and IOS-1258028 from the National Science Foundation and Kansas State University to F.W. and J.O. The Q-Exactive quantitative mass spectrometer was funded under the SFI Research Infrastructure Call 2012, Grant Number 12/RI/2346 (3) to Sean Doyle. We are grateful to the Phylloxera Genomic Initiative (and especially Franc¸ois Delmotte, Claude Rispe and Denis Tagu) for providing the 1KITE projects ,
Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae, Plant Biotechnol J, vol.13, issue.6, pp.849-857, 2015. ,
Multiple hypothesis testing to detect lineages under positive selection that affects only a few sites, Mol Biol Evol, vol.24, issue.5, pp.1219-1228, 2007. ,
In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity, Mol Plant Microbe Interact, vol.26, issue.1, pp.67-74, 2013. ,
Expression of insect cystein-rich antifungal peptides in transgenic tobacco enhances resistance to a fungal disease, Plant Sci, vol.162, issue.6, pp.995-1006, 2002. ,
Featurebased prediction of non-classical and leaderless protein secretion, Protein Eng Des Sel, vol.17, issue.4, pp.349-356, 2004. ,
Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions, Annu Rev Phytopathol, vol.45, pp.399-436, 2007. ,
Aphids on the world's crops: an identification and information guide, 2000. ,
A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid), 2010. ,
, PLoS Genet, vol.6, issue.11, p.1001216
BLASTþ: architecture and applications, BMC Bioinformatics, vol.10, p.421, 2009. ,
DOI : 10.1186/1471-2105-10-421
URL : https://doi.org/10.1186/1471-2105-10-421
Predicted effector molecules in the salivary secretome of the pea aphid (Acyrthosiphon pisum): a dual transcriptomic/ proteomic approach, J Proteome Res, vol.10, issue.4, pp.1505-1518, 2011. ,
The secreted salivary proteome of the pea aphid Acyrthosiphon pisum characterised by mass spectrometry, Proteomics, vol.9, issue.9, pp.2457-2467, 2009. ,
GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense, Proc Natl Acad Sci U S A, vol.111, issue.24, pp.8919-8924, 2014. ,
Turning a hobby into a job: how duplicated genes find new functions, Nat Rev Genet, vol.9, issue.12, pp.938-950, 2008. ,
Andromeda: a peptide search engine integrated into the MaxQuant environment, J Proteome Res, vol.10, issue.4, pp.1794-1805, 2011. ,
Midgut adaptation and digestive enzyme distribution in a phloem feeding insect, the pea aphid Acyrthosiphon pisum, J Insect Physiol, vol.49, issue.1, pp.11-24, 2003. ,
URL : https://hal.archives-ouvertes.fr/hal-00402183
STAR: ultrafast universal RNA-seq aligner, Bioinformatics, vol.29, issue.1, pp.15-21, 2013. ,
Dynamics of copy number variation in host races of the pea aphid, Mol Biol Evol, vol.32, issue.1, pp.63-80, 2015. ,
URL : https://hal.archives-ouvertes.fr/hal-01945404
Improved prediction of signal peptides: signalP 3.0, J Mol Biol, vol.340, issue.4, pp.783-795, 2004. ,
The role of protein effectors in plant-aphid interactions, Curr opin Plant Biol, vol.16, issue.4, pp.451-456, 2013. ,
Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein, Mol Plant Microbe Interact, vol.27, issue.7, pp.747-756, 2014. ,
Targeted re-sequencing confirms the importance of chemosensory genes in aphid host race differentiation, Mol Ecol, vol.26, issue.1, pp.43-58, 2017. ,
URL : https://hal.archives-ouvertes.fr/hal-01532713
Differential gene expression according to race and host plant in the pea aphid, Mol. Ecol, vol.25, issue.17, pp.4197-4215, 2016. ,
URL : https://hal.archives-ouvertes.fr/hal-01371828
Influence of the amino acid balance on the improvement of an artificial diet for a biotype of Acyrthosiphon pisum (Homoptera: Aphididae), Can J Zool, vol.66, issue.11, pp.2449-2453, 1988. ,
The global distribution of diet breadth in insect herbivores, Proc Natl Acad Sci U S A, vol.112, issue.2, pp.442-447, 2015. ,
Aphid salivary proteases are capable of degrading sieve-tube proteins, J Exp Bot, vol.66, issue.2, pp.533-539, 2015. ,
Nitric oxide generation in Vicia faba phloem cells reveals them to be sensitive detectors as well as possible systemic transducers of stress signals, New Phytol, vol.178, issue.3, pp.634-646, 2008. ,
High-throughput functional annotation and data mining with the Blast2GO suite, Nucleic Acids Res, vol.36, issue.10, pp.3420-3435, 2008. ,
Characterization of an aphid-specific, cysteine-rich protein enriched in salivary glands, Biophys Chem, vol.189, pp.25-32, 2014. ,
Optimization of agroinfiltration in Pisum sativum provides a new tool for studying the salivary protein functions in the pea aphid complex, Front Plant Sci, vol.7, p.1171, 2016. ,
Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans, Nature, vol.461, issue.7262, pp.393-398, 2009. ,
Aphids as virus vectors, 2014. ,
Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions, J Cell Biol, vol.189, issue.4, pp.739-754, 2010. ,
Ehrlich and Raven Revisited: mechanisms underlying codiversification of plants and enemies, Annu Rev Ecol Evol Syst, vol.42, issue.1, pp.71-89, 2011. ,
Disentangling the causes for faster-X evolution in aphids, Genome Biol Evol, vol.10, pp.507-520, 2018. ,
Genome scans reveal candidate regions involved in the adaptation to host plant in the pea aphid complex, Mol Ecol, vol.21, issue.21, pp.5251-5264, 2012. ,
Expansion of the miRNA pathway in the hemipteran insect Acyrthosiphon pisum, Mol Biol Evol, vol.27, issue.5, pp.979-987, 2010. ,
RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members, Proc Natl Acad Sci, vol.105, issue.12, pp.4874-4879, 2008. ,
,
, Genome Biol. Evol, vol.10, issue.6, pp.1554-1572, 2018.
InterProScan 5: genome-scale protein function classification, Bioinformatics, vol.30, issue.9, pp.1236-1240, 2014. ,
MAFFT version 5: improvement in accuracy of multiple sequence alignment, Nucleic Acids Res, vol.33, issue.2, pp.511-518, 2005. ,
Gene duplication as a mechanism of genomic adaptation to a changing environment, Proc Biol Sci, vol.279, pp.5048-5057, 1749. ,
OrthoDB v8: update of the hierarchical catalog of orthologs and the underlying free software, Nucleic Acids Res, vol.43, issue.D1, pp.250-256, 2015. ,
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes, J Mol Biol, vol.305, issue.3, pp.567-580, 2001. ,
RNA-seq analysis is easy as 1-2-3 with limma, Glimma and edgeR, vol.5, p.1408, 1000. ,
voom: precision weights unlock linear model analysis tools for RNA-seq read counts, Genome Biol, vol.15, issue.2, p.29, 2014. ,
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation, Bioinformatics, vol.23, issue.1, pp.127-128, 2007. ,
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, vol.30, issue.7, pp.923-930, 2014. ,
In vitro evidence supports membrane alanyl aminopeptidase N as a receptor for a plant virus in the pea aphid vector, J Virol, vol.89, issue.22, pp.11203-11212, 2015. ,
An algorithm for progressive multiple alignment of sequences with insertions, Proc Natl Acad Sci U S A, vol.102, issue.30, pp.10557-10562, 2005. ,
Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species, Genome Biol, vol.18, p.27, 2017. ,
URL : https://hal.archives-ouvertes.fr/hal-01588181
Aphids secrete watery saliva into plant tissues from the onset of stylet penetration, Entomol Exp Appl, vol.139, issue.2, pp.145-153, 2011. ,
Insect speciation rules: unifying concepts in speciation research, Annu Rev Entomol, vol.59, issue.1, pp.339-361, 2014. ,
A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant, Proc Natl Acad Sci U S A, vol.105, issue.29, pp.9965-9969, 2008. ,
RNAi Knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum, J Insect Sci, vol.6, pp.1-7, 2006. ,
A secreted MIF cytokine enables aphid feeding and represses plant immune responses, Curr Biol, vol.25, issue.14, pp.1898-1903, 2015. ,
URL : https://hal.archives-ouvertes.fr/hal-01312804
The genome of Diuraphis noxia, a global aphid pest of small grains, BMC Genomics, vol.16, p.429, 2015. ,
Genomic regions repeatedly involved in divergence among plant-specialized pea aphid biotypes, J Evol Biol, vol.27, issue.9, pp.2013-2020, 2014. ,
URL : https://hal.archives-ouvertes.fr/hal-01178940
High expression of a unique aphid protein in the salivary glands of Acyrthosiphon pisum, Physiol Mol Plant Pathol, vol.92, pp.175-180, 2015. ,
Genetic characterisation of new host-specialised biotypes and novel associations with bacterial symbionts in the pea aphid complex, Insect Conserv Divers, vol.8, issue.5, pp.484-492, 2015. ,
URL : https://hal.archives-ouvertes.fr/hal-01252653
Evolutionary history of aphid-plant associations and their role in aphid diversification, C R Biol, vol.333, issue.6-7, pp.474-487, 2010. ,
URL : https://hal.archives-ouvertes.fr/hal-00729508
A continuum of genetic divergence from sympatric host races to species in the pea aphid complex, Proc Natl Acad Sci U S A, vol.106, issue.18, pp.7495-7500, 2009. ,
URL : https://hal.archives-ouvertes.fr/hal-00729934
Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts, Proc Natl Acad Sci U S A, vol.106, issue.38, pp.16315-16320, 2009. ,
SignalP 4.0: discriminating signal peptides from transmembrane regions, Nat Methods, vol.8, issue.10, p.785, 2011. ,
PredGPI: a GPI-anchor predictor, BMC Bioinformatics, vol.9, p.392, 2008. ,
Silencing of aphid genes by dsRNA feeding from plants, PLoS One, vol.6, issue.10, p.25709, 2011. ,
Aphid protein effectors promote aphid colonization in a plant species-specific manner, Mol Plant Microbe Interact, vol.26, issue.1, pp.130-139, 2013. ,
The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR), 2014. ,
Host plant selection by aphids: behavioral, evolutionary, and applied perspectives, Annu Rev Entomol, vol.51, pp.309-330, 2006. ,
Genome expansion and differential expression of amino acid transporters at the aphid/Buchnera symbiotic interface, Mol Biol Evol, vol.28, issue.11, pp.3113-3126, 2011. ,
A small cysteine-rich protein from the Asian soybean rust fungus, Phakopsora pachyrhizi, suppresses plant immunity, PLoS Pathog, vol.12, issue.9, p.1005827, 2016. ,
Toxicity of lectins and processing of ingested proteins in the pea aphid Acyrthosiphon pisum, Entomol Exp Appl, vol.76, issue.2, pp.143-155, 1995. ,
R: A Language and Environment for Statistical Computing, 2017. ,
Large gene family expansion and variable selective pressures for cathepsin B in aphids, Mol Biol Evol, vol.25, issue.1, pp.5-17, 2007. ,
URL : https://hal.archives-ouvertes.fr/inria-00180087
limma powers differential expression analyses for RNA-sequencing and microarray studies, Nucleic Acids Res, vol.43, issue.7, pp.47-47, 2015. ,
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, vol.26, issue.1, pp.139-140, 2010. ,
A scaling normalization method for differential expression analysis of RNA-seq data, Genome Biol, vol.11, issue.3, p.25, 2010. ,
2017. an aphid effector targets trafficking protein VPS52 in a host-specific manner to promote virulence, Plant Physiol, vol.173, issue.3, pp.1892-1903 ,
URL : https://hal.archives-ouvertes.fr/hal-01580190
GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters, Nucleic Acids Res, vol.43, issue.W1, pp.7-14, 2015. ,
Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum, Mol Biol Evol, vol.26, issue.9, pp.2073-2086, 2009. ,
URL : https://hal.archives-ouvertes.fr/hal-01945562
Large-scale candidate gene scan reveals the role of chemoreceptor genes in host plant specialization and speciation in the pea aphid, Evolution, vol.66, issue.9, pp.2723-2738, 2012. ,
URL : https://hal.archives-ouvertes.fr/hal-01945549
RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models, Bioinformatics, vol.22, issue.21, pp.2688-2690, 2006. ,
In silico characterization and molecular evolutionary analysis of a novel superfamily of fungal effector proteins, 2012. ,
, Genome sequence of the pea aphid Acyrthosiphon pisum, The International Aphid Genomics Consortium, vol.29, p.1000313, 2010.
, Evolution and Gene Family Expansions of Aphid Salivary Effectors GBE
, Genome Biol. Evol, vol.10, issue.6, pp.1554-1572, 2018.
Comparative transcriptomics and proteomics of three different aphid species identifies core and diverse effector sets, BMC Genomics, vol.17, issue.1, p.172, 2016. ,
Taking the stage: effectors in the spotlight, Curr Opin Plant Biol, vol.38, pp.25-33, 2017. ,
Armet is an effector protein mediating aphid-plant interactions, FASEB J, vol.29, issue.5, pp.2032-2045, 2015. ,
Angiotensin-converting enzymes modulate aphidplant interactions, Sci Rep, vol.5, issue.1, p.8885, 2015. ,
Whole genome sequence of the soybean aphid, Aphis glycines, Insect Biochem Mol Biol, 2017. ,
URL : https://hal.archives-ouvertes.fr/hal-01555244
Herbivory increases diversification across insect clades, Nat Commun, vol.6, issue.1, p.8370, 2015. ,
The structural sheath protein of aphids is required for phloem feeding, Insect Biochem Mol Biol, vol.57, pp.34-40, 2015. ,
How phloem-feeding insects face the challenge of phloem-located defenses, Front Plant Sci, vol.4, p.336, 2013. ,
New insights into plant responses to the attack from insect herbivores, Annu Rev Genet, vol.44, pp.1-24, 2010. ,
PAML 4: phylogenetic analysis by maximum likelihood, Mol Biol Evol, vol.24, issue.8, pp.1586-1591, 2007. ,
Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models, Mol Biol Evol, vol.17, issue.1, pp.32-43, 2000. ,
Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages, Mol Biol Evol, vol.19, issue.6, pp.908-917, 2002. ,
Codon-substitution models for heterogeneous selection pressure at amino acid sites, Genetics, vol.155, pp.431-449, 2000. ,
Bayes Empirical Bayes inference of amino acid sites under positive selection, Mol Biol Evol, vol.22, issue.4, pp.1107-1118, 2005. ,
Cloning and RNA interference analysis of the salivary protein C002 gene in Schizaphis graminum, J Integr Agric, vol.14, issue.4, pp.698-705, 2015. ,
A massive expansion of effector genes underlies gallformation in the wheat pest Mayetiola destructor, Curr Biol, vol.25, issue.5, pp.613-620, 2015. ,