EVOLUTION OF GENOME AND DEVELOPMENT IN TUNICATES

The evolution of Chordates and how they diversified into three main subphyla (vertebrates, cephalochordates, tunicates) remains enigmatic, partly because of comparatively scarce information from fossil records. Together with Eric Thompson’s group, we have established a new model system of non-vertebrate chordates with Oikopleura dioica, a tunicate larvaceanwhich in contrast to ascidians keeps tail and general chordate body plan during all its life. This species is also appealing for genetic analysis due to a very short life cycle (6 days at 15˚C). Its female fecundity is fairly high (several hundred eggs) and its culture in the lab over many generations has become well controlled.  During the last decade, our group has been particularly active in genomic studies, with the following key findings:

•  The Oikopleura genome organization and gene complement are very divergent from the expected chordate ancestor (Seo et al., 2001). This divergence results from a particularly high mutation rate in the history of larvaceans. We recently demonstrated with in silico and experimental approaches the loss of a most conserved DNA repair mechanism in the larvacean lineage (Deng et al., 2018).

• The extremely rapid evolution of larvaceangenomes proved instrumental to capture transient features characteristic of genomic changes, such as intron gains (Denoeud et al., 2010). To study the history of genome changes, we considerably extended our panel of larvacean genomes during the last few years (Naville et al., 2019). We could reveal the prevalence of highly diverse non-canonical introns in the genome of Fritillariaborealis, and could show that their splicing uses a modified U2 spliceosome (Henriet et al., 2019). 

• Incorporating Oikopleura coding sequences into phylogenetic studies led to revise the whole chordate tree, with tunicates and not cephalochordates now considered to be the sister group of vertebrates (Delsuc et al.,2006).

Based on the new evolutive scenarios emerging from our genomic studies, we now put moreemphasis on how larvaceans may have been simplified from anatomically more complex chordate ancestors. This type of studies became possible after the establishment of tools allowing to manipulate its development (RNAi and CRISPR). We are interested in transcription factors and their targets, Hox genes (Seo et al.,2004), as well as multiple genes which govern the synthesis of the Oikopleura house, an extraordinary innovation of larvaceans used for filter feeding.

Academic article

• Simon Henriet; Berta Colom Sanmarti; Sara Sumic et al. (2019). Evolution of the U2 Spliceosome for Processing Numerous and Highly Diverse Non-canonical Introns in the Chordate Fritillaria borealis. (external link)
• Simon Henriet; Sara Sumic; Carletta Doufoundou-Guilengui et al. (2015). Embryonic expression of endogenous retroviral RNAs in somatic tissues adjacent to the Oikopleura germline. (external link)
• Yana Mikhaleva; Ragnhild Skinnes; Sara Sumic et al. (2018). Development of the house secreting epithelium, a major innovation of tunicate larvaceans, involves multiple homeodomain transcription factors. (external link)
• Daniel Chourrout; Frédéric Delsuc; P Chourrout et al. (2006). Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. (external link)
• Sutada Mungpakdee; Hee-Chan Seo; Daniel Chourrout (2008). Spatio-temporal expression patterns of anterior Hox genes in Atlantic salmon (Salmo salar). (external link)
• Anna Rita Angotzi; Sutada Mungpakdee; Sigurd Olav Stefansson et al. (2011). Involvement of Prop1 homeobox gene in the early development of fish pituitary gland. (external link)
• France Denoeud; Simon Henriet; Sutada Mungpakdee et al. (2010). Plasticity of Animal Genome Architecture Unmasked by Rapid Evolution of a Pelagic Tunicate. (external link)
• Wei Deng; Simon Henriet; Daniel Chourrout (2018). Prevalence of Mutation-Prone Microhomology-Mediated End Joining in a Chordate Lacking the c-NHEJ DNA Repair Pathway. (external link)
• Frédéric Delsuc; Henner Brinkmann; Daniel Chourrout et al. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. (external link)
• Fekadu Yadetie; Stephen Butcher; Hilde Elise Sundsøy Førde et al. (2012). Conservation and divergence of chemical defense system in the tunicate Oikopleura dioica revealed by genome wide response to two xenobiotics. (external link)

See a complete overview of publications in Cristin.

TEN SELECTED PUBLICATIONS (*corresponding author)

Henriet S, Sanmarti BC, Sumic S and Chourrout D* (2019) Evolution of the U2 Spliceosome for Processing Numerous and Highly Diverse Non-canonical Introns in the Chordate Fritillaria borealis. 
Curr Biol 29, 3193‐3199 

Deng W*, Henriet S and Chourrout D* (2018) Prevalence of Mutation-Prone Microhomology-Mediated End Joining in a Chordate Lacking the c-NHEJ DNA Repair Pathway. 
Curr Biol 28:3337-3341 

Wang S, Zhang J, Jiao W, Li J, Xun X, Sun Y, Guo X, Huan P, Dong B, Zhang L, Hu X, Sun X, Wang J, Zhao C, Wang Y, Wang D, Huang X, Wang R, Lv J, Li Y, Zhang Z, Liu B, Lu W, Hui Y, Liang J, Zhou Z, Hou R, Li X, Liu Y, Li H, Ning X, Lin Y, Zhao L, Xing Q, Dou J, Li Y, Mao J, Guo H, Dou H, Li T, Mu C, Jiang W, Fu Q, Fu X, Miao Y, Liu J, Yu Q, Li R, Liao H, Li X, Kong Y, Jiang Z, Chourrout D*, Li R* and Bao Z* (2017) Scallop genome provides insights into evolution of bilaterian karyotype and development. 
Nature Ecology Evolution 1:120-

Denoeud F, Henriet S, Mungpakdee S, Aury JM, Da Silva C, Brinkmann H, Mikhaleva J, Olsen LC, Jubin C, Cañestro C, Bouquet JM, Danks G, Poulain J, Campsteijn C, Adamski M, Cross I, Yadetie F, Muffato M, Louis A, Butcher S, Tsagkogeorga G, Konrad A. Singh S, Jensen MF, Cong EH, Eikeseth-Otteraa H, Anthouard V, Kachouri-Lafond R, Nishino A, Ugolini M, Chourrout P, Nishida H, Aasland R, Huzurbazar S, Westhof E, Delsuc F, Lehrach H, Reinhardt R, Weissenbach J, Roy SW, Artiguenave F, Postlethwait JH, Manak JR, Thompson EM, Jaillon O, Du Pasquier L, Boudinot P, Liberles DA, Volff JN, Philippe H, Lenhard B, Crollius HR, Wincker P* and Chourrout D* (2010). Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. 
Science 330:1381-1385 

Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G (2007) Genome regulation by polycomb and trithorax proteins. 
Cell 128:735-745. 

Chourrout D*, Delsuc F, Chourrout P, Edvardsen RB, Rentzsch F, Renfer E, Jensen MF, Zhu B, de Jong P, Steele RE, Technau U* (2006) Minimal ProtoHox cluster inferred from bilaterian and cnidarian Hox complements. 
Nature 442:684-687. 

Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates. 
Nature 439:965-968. 

Seo HC, Edvardsen RB, Maeland AD, Bjordal M, Jensen MF, Hansen A, Flaat M, Weissenbach J, Lehrach H, Wincker P, Reinhardt R, Chourrout D* (2004) Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica.. 
Nature 431:67-71. 

Seo HC, Kube M, Edvardsen RB, Jensen MF, Beck A, Spriet E, Gorsky G, Thompson EM, Lehrach H, Reinhardt R, Chourrout D* (2001) Miniature genome in the marine chordate Oikopleura dioica. 
Science 294:2506. 

Joly JS, Bourrat F, Nguyen V, Chourrout D (1997): Ol-Prx 3, a member of a new class of homeobox genes, is unimodally expressed in several domains of the developing and adult CNS of the medakafish (Oryzias latipes). 
Proc Natl Acad Sci USA 94:12987-12992.