Past Research I - BF2I, Lyon

Genomics of symbiosis in the pea aphid (2007-2016)

Stefano Colella's Interests and Activities in the early days at INRA in Lyon, France

The "SymTrophique" Team

In November 2007, I joined the BF2I SymTrophique team (équipe – Symbiose : Génomique Fonctionelle des Interactions Trophiques) led by Hubert Charles. Three other scientists in the BF2I laboratory were members of the research team: Federica Calevro, Gérard Febvay and Yvan Rahbé. The team is interested in the use of functional genomics and systems biology approaches to study symbiosis. The research model is the intimate symbiosis between the pea aphid Acyrthosiphon pisum (eukaryote) and the bacteria Buchnera aphidicola (prokaryote), housed in a specialized organ, the bacteriome. Thus, the model comprises two distinct genomes within a single multicellular organism. The genome sequence of the symbiont was published in 2000 (Shigenobu S. et al., 2000) and we have been involved in the annotation of the recently published sequencing and annotation of the pea aphid genome (The International Aphid Genomics Consortium, 2010). A good annotation of the pea aphid genome is key to the development of functional genomics research and novel experimental tools.

The BF2I laboratory is part of the European COST (European Cooperation in the field of Scientific and Technical Research) network: "Arthropod symbiosis: from fundamental studies to pest and disease management" (COST Action FA0701).

Functional genomics of arthropods symbiosis

From the prokaryote symbiont...

In the past few years the team has developed and successfully used an oligo microarray platform for the study of Buchnera transcriptome (Calevro et al., 2004). A specific algorithm for oligo design and optimisation was developed in the laboratory (Reymond N. et al., 2004) and used to develop the oligogonucleotide microarray dedicated to Buchnera. This array have been used to study the transcriptional regulation of Buchnera in response to nutritional stress applied to the aphids (Reymond et al., 2006; Charles et al., 2006), as well as to study Buchnera genome organization and its relationship to transcription (Viñuelas J. et al., 2007).

...to the eukaryotic host (A. pisum)

The availability of the genome sequence of pea aphid is the stepping stone to further develop functional genomics approaches to study this symbiosis. At present, we developed a high-density oligonucleotide microarray platform (in collaboration with Nimblegen) for the analysis of the pea aphid transcriptome (Array Express: A-MEXP-1999). Such a platform is a key research tool to integrate the eukaryotic host and its symbiotic bacteria transcriptome analyses in order to characterise the genetic regulatory network of this successful symbiosis association. We successfully used this array to study the pea aphid development (Rabatel A. et al. 2013).

Ad hoc tools development

In collaboration and as part of the Bamboo INRIA Team (led by Marie-France Sagot, INRIA) at the Université Claude Bernard Lyon 1, we used Pathway Tools to build a BioCyc database for the pea aphid (AcypiCyc). You can access the database from the AcypiCyc home page; in the database you will be already able to compare the pea aphid metabolism to that of Drosophila melanogaster, Tribolium castaneum and the symbiont Buchnera aphidicola.

To allow easy updates of a BioCyc database starting from multiple genome annotation resources available over time, we have developed a data management system (CycADS: Cyc Annotation Database System). The CycADS tools are centred on an ad hoc modified SQL database, complemented by a set of Java scripts to import and export relevant information. This work started as part of BBSRC/ANR funded METNET project, an international collaboration with the University of York.

More recently we used CycADS to develop ArthopodaCyc a metabolic database for arthropods, whose genome have been sequenced.

Publications

Peer-reviewed papers

Brinza L, Viñuelas J, Cottret L, Calevro F, Rahbé Y, Febvay G, Duport G, Colella S, Rabatel A, Gautier C, Fayard JM, Sagot MF and Charles H. Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. C. R. Biol. 332(11):1034-49, 2009. [PubMed]
International Aphid Genomics Consortium. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. Feb 23;8(2):e1000313, 2010.[PubMed] [PLoS Biology - Open Access]
Wilson AC, Ashton PD, Calevro F, Charles H, Colella S, Febvay G, Jander G, Kushlan PF, Macdonald SJ, Schwartz JF, Thomas GH, Douglas AE. Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol. 19 Suppl 2:249-58, 2010. [PubMed]
Tagu D, Dugravot S, Outreman Y, Rispe C, Simon JC, Colella S. The anatomy of an aphid genome: from sequence to biology. C. R. Biol. 333(6-7):464-73, 2010. [PubMed]
Vellozo AF, Véron AS, Baa-Puyoulet P, Huerta-Cepas J, Cottret L, Febvay G, Calevro F, Rahbé Y, Douglas AE, Gabaldón T, Sagot MF, Charles H and Colella S. CycADS: an annotation database system to ease the development and update of BioCyc databases. Database, doi: 10.1093/database/bar008, 2011. [PubMed] [Database - Open Access]
Viñuelas J, Febvay G, Duport G, Colella S, Fayard J-M, Charles H, Rahbé Y, Calevro F. Multimodal dynamic response of the Buchnera aphidicola pLeu plasmid to variations in leucine demand of its host, the pea aphid Acyrthosiphon pisum. Mol Microbiol. Jul 28. doi: 10.1111/j.1365-2958.2011.07760.x. 2011. [PubMed]
Charles H, Balmand S, Lamelas A, Cottret L, Pérez-Brocal V, Burdin B, Latorre A, Febvay G, Colella S, Calevro F and Rahbé Y. A genomic reappraisal of symbiotic function in the aphid/Buchnera symbiosis: reduced transporter sets and variable membrane organisations. PLoS One 6(12):e29096, 2011. [PubMed] [PLoS One - Open Access]
Rabatel A, Febvay G, Gaget K, Duport G, Baa-Puyoulet P, Sapountzis P, Bendridi N, Rey M, Rahbé Y, Charles H, Calevro F** and Colella S**. Tyrosine pathway regulation is host-mediated in the pea aphid symbiosis during late embryonic and early larval development. BMC Genomics. 2013 Apr 10;14(1):235, 2013. [PubMed] [BMC Genomics - Open Access]
Sapountzis P, Duport G, Balmand S, Gaget K, Jaubert-Possamai S, Febvay G, Charles H, Rahbé Y, Colella S** and Calevro F**. New insight into the RNA interference response against cathepsin-L gene in the pea aphid, Acyrthosiphon pisum: molting or gut phenotypes specifically induced by injection or feeding treatments. Insect Biochem Mol Biol. Aug 51:20-32, 2014.[PubMed] [Insect Biochem Mol Biol - Open Access]
Simonet P, Duport G, Gaget K, Weiss-Gayet M, Colella S, Febvay G, Charles H, Viñuelas J, Heddi A, Calevro F. Direct flow cytometry measurements reveal a fine-tuning of symbiotic cell dynamics according to the host developmental needs in aphid symbiosis. Sci Rep. Jan 29;6:19967. doi: 10.1038/srep19967, 2016. [PubMed][Sci Rep - Open Access]
Baa-Puyoulet P, Parisot N, Febvay G, Huerta-Cepas J, Vellozo AF, Gabaldon T, Calevro F, Charles H and Colella S. ArthropodaCyc: a CycADS powered collection of BioCyc databases to analyse and compare metabolism of arthropods. Database, doi: 10.1093/database/baw081, 2016. [Database - Open Access]
Simonet P, Gaget K, Parisot N, Duport G, Rey M, Febvay G, Charles H, Callaerts P, Colella S and Calevro F. Disruption of phenylalanine hydroxylase reduces adult lifespan and fecundity, and impairs embryonic development in parthenogenetic pea aphids. Sci Rep. Oct 3;6:34321. doi: 10.1038/srep34321, 2016.[PubMed] [Sci Rep - Open Access]
Mathers TC,* Chen Y,* Kaithakottil G, Legeai F, Mugford ST, Baa-Puyoulet P, Bretaudeau A, Clavijo B, Colella S, Collin O, Dalmay T, Derrien T, Feng H, Gabaldón T, Jordan A, Julca I, Kettles GJ, Kowitwanich K, Lavenier D, Lenzi P, Lopez-Gomollon S, Loska D, Mapleson D, Maumus F, Moxon S, Price DRG, Sugio A, van Munster M, Uzest M, Waite D, Jander G, Tagu D, Wilson ACC, van Oosterhout C, Swarbreck D^^, Hogenhout SA^^. Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species. Genome Biol. Feb 13;18(1):27. doi: 10.1186/s13059-016-1145-3, 2017. [PubMed] [Genome Biology - open access]
Colella S*^^, Parisot N*, Simonet P, Gaget K, Duport G, Baa-Puyoulet P, Rahbé Y, Charles H, Febvay G, Callaerts P and Calevro F.^^ Bacteriocyte reprogramming to cope with nutritional stress in a phloem sap feeding hemipteran, the pea aphid Acyrthosiphon pisum. Front. Physiol. Oct 25;9:1498. doi: 10.3389/fphys.2018.01498, 2018. [PubMed][Frontiers - open access]
Panfilio KA, Vargas Jentzsch IM, Benoit JB, Erezyilmaz D, Suzuki Y, Colella S, Robertson HM, Poelchau MF, Waterhouse RM, Ioannidis P, Weirauch MT, Hughes DST, Murali SC, Werren JH, Jacobs CGC, Duncan EJ, Armisén D, Vreede BMI, Baa-Puyoulet P, Berger CS, Chang C-C, Chao H, Chen M-JM, Chen Y-T, Childers CP, Chipman AD, Cridge AG, Crumière AJJ, Dearden PK, Didion EM, Dinh H, Doddapaneni H, Dolan A, Dugan S, Extavour CG, Febvay G, Friedrich M, Ginzburg N, Han Y, Heger P, Holmes CJ, Horn T, Hsiao Y-M, Jennings EC, Johnston JS, Jones TE, Jones JW, Khila A, Koelzer S, Kovacova V, Leask M, Lee SL, Lee C-Y, Lovegrove MR, Lu H-L, Lu Y, Moore PJ, Munoz-Torres MC, Muzny DM, Palli SR, Parisot N, Pick L, Porter M, Qu J, Refki PN, Richter R, Rivera-Pomar R, Rosendale AJ, Roth S, Sachs L, Santos ME, Seibert J,Sghaier E, Shukla JN, Stancliffe RJ, Tidswell O, Traverso L, van der Zee M, Viala S, Worley KC, Zdobnov EM, Gibbs RA, Richards S. Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. Genome Biol. Apr 2; 20:64. doi: 10.1186/s13059-019-1660-0, 2019. [PubMed] [Genome Biology - open access]
Parisot N*, Vargas-Chavez C*, Goubert C*, Baa-Puyoulet P, Balmand S, Béranger L, Blanc C, Bonnamour A, Boulesteix M, Burlet N, Calevro F, Callaerts P, Chancy T, Charles H, Colella S, Da Silva Barbosa A, Dell'Aglio E, Di Genova A, Febvay A, Gabaldon T, Galvão Ferrarini M, Gerber A, Gillet B, Hubley R, Hughes S, Jacquin-Joly E, Maire J, Marcet-Houben M, Masson F, Meslin C, Montagné N, Moya A, Ribeiro de Vasconcelos AT, Richard G, Rosen J, Sagot M-F, Smit AFA, Storer J, Vincent-Monégat C, Vallier A, Vigneron A, Zaidman-Rémy A, Zamoum W, Vieira C*, Rebollo R*, Latorre A*, Heddi A.* The transposable element-rich genome of the cereal pest Sitophilus oryzae. BMC Biol. Nov 9;19(1):241. doi: 10.1186/s12915-021-01158-2, 2021. [PubMed] [BMC Biology - open access]

Book chapter

Tagu D, Calevro F, Colella S, Gabaldón T, Sugio A. Chapter 3: Functional and evolutionary genomics in aphids. BIOLOGY & ECOLOGY OF APHIDS, Andreas Vilcinskas Editor, Taylor & Francis Group. March 10, 2016 [CRC Press]

In the bioRxiv archive for life sciences

Mathers TC*, Chen Y*, Kaithakottil G, Legeai F, Mugford ST, Baa-Puyoulet P, Bretaudeau A, Clavijo B, Colella S, Collin O, Dalmay T, Derrien T, Feng H, Gabaldón T, Jordan A, Julca I, Kettles GJ, Kowitwanich K, Lavenier D, Lenzi P, Lopez-Gomollon S, Loska D, Mapleson D, Maumus F, Moxon S, Price DRG, Sugio A, van Munster M, Uzest M, Waite D, Jander G, Tagu D, Wilson ACC, van Oosterhout C, Swarbreck D **, Hogenhout SA**. Rapid transcriptional plasticity of duplicated gene clusters enables a clonally reproducing aphid to colonise diverse plant species.bioRxiv 063610, July 19, 2016. doi: https://doi.org/10.1101/063610 [bioRXiv - open acces]. Now published in Genome Biology doi: 10.1186/s13059-016-1145-3
Panfilio KA, Vargas Jentzsch IM, Benoit JB, Erezyilmaz D, Suzuki Y, Colella S, Robertson HM, Poelchau MF, Waterhouse RM, Ioannidis P, Weirauch MT, Hughes DST, Murali SC, Werren JH, Jacobs CGC, Duncan EJ, Armisén D, Vreede BMI, Baa-Puyoulet P, Berger CS, Chang C-C, Chao H, Chen M-JM, Chen Y-T, Childers CP, Chipman AD, Cridge AG, Crumière AJJ, Dearden PK, Didion EM, Dinh H, Doddapaneni H, Dolan A, Dugan-Perez S, Extavour CG, Febvvay G, Friedrich M, Ginzburg N, Han Y, Heger P, Horn T, Hsiao Y-M, Jennings EC, Johnston JS, Jones TE, Jones JW, Khila A, Koelzer S, Kovacova V, Leask M, Lee SL, Lee C-Y, Lovegrove MR, Lu H-L, Lu Y, Moore PJ, Munoz-Torres MC, Muzny DM, Palli SR, Parisot N, Pick L, Porter M, Qu J, Refki PN, Richter R, Rivera-Pomar R, Rosendale AJ, Roth S, Sachs L, Santos ME, Seibert J,Sghaier E, Shukla JN, Stancliffe RJ, Tidswell O, Traverso L, van der Zee M, Viala S, Worley KC, Zdobnov EM, Gibbs RA, Richards S. Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. bioRxiv 201731 (v3), October 31, 2018. doi: https://doi.org/10.1101/201731 [bioRXiv - open acces]. Now published in Genome Biology doi: 10.1186/s13059-019-1660-0
Parisot N*, Vargas-Chavez C*, Goubert C*, Baa-Puyoulet P, Balmand S, Béranger L, Blanc C, Bonnamour A, Boulesteix M, Burlet N, Calevro F, Callaerts P, Chancy T, Charles H, Colella S, Da Silva Barbosa A, Dell'Aglio E, Di Genova A, Febvay A, Gabaldon T, Galvão Ferrarini M, Gerber A, Gillet B, Hubley R, Hughes S, Jacquin-Joly E, Maire J, Marcet-Houben M, Masson F, Meslin C, Montagné N, Moya A, Ribeiro de Vasconcelos AT, Richard G, Rosen J, Sagot M-F, Smit AFA, Storer J, Vincent-Monégat C, Vallier A, Vigneron A, Zaidman-Rémy A, Zamoum W, Vieira C*, Rebollo R*, Latorre A*, Heddi A.* The genome sequence of the cereal pest Sitophilus oryzae: an unprecedented transposable element content. bioRxiv 2021.03.03.408021; doi: https://doi.org/10.1101/2021.03.03.408021 [bioRXiv - open acces]. Now published in BMC Biology doi: 10.1186/s12915-021-01158-2

* These authors contributed equally to this work. ^^ Co-corresponding authors.

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