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.
- (2018). Development of the house secreting epithelium, a major innovation of tunicate larvaceans, involves multiple homeodomain transcription factors. Developmental Biology. 117-126.
- (2015). Oikopleura dioica culturing made easy: A Low-Cost facility for an emerging animal model in EvoDevo. Genesis. 183-193.
- (2015). Modification of the larval swimming behavior in Oikopleura dioica, a chordate with a miniaturized central nervous system by dsRNA injection into fertilized eggs. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 114-127.
- (2015). Embryonic expression of endogenous retroviral RNAs in somatic tissues adjacent to the Oikopleura germline. Nucleic Acids Research (NAR). 3701-3711.
- (2008). Spatio-temporal expression patterns of anterior Hox genes in Atlantic salmon (Salmo salar). Gene Expression Patterns. 508-514.
- (2008). Independent and dynamic reallocation of pitx gene expression during vertebrate evolution, with emphasis on fish pituitary development. Gene. 19-26.
- (2008). Differential evolution of the 13 Atlantic salmon Hox clusters. Molecular Biology and Evolution (MBE). 1333-1343.
- (2007). Development of the caudal nerve cord, motoneurons, and muscle innervation in the appendicularian urochordate Oikopleura dioica. Journal of Comparative Neurology. 224-243.
- (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature. 965-968.
- (2007). Genome regulation by polycomb and trithorax proteins. Cell. 735-745.
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.
Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G (2007) Genome regulation by polycomb and trithorax proteins.
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.
Delsuc F, Brinkmann H, Chourrout D, Philippe H (2006) Tunicates and not cephalochordates are the closest living relatives of vertebrates.
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..
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.
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.
Daniel Chourrout is the former Director of the Sars Centre, and established the centre in 1997. His research is focused on the evolution of chordate development, using Oikopleura and other tunicate larvaceans as model systems. The activity of his group includes comparative genome and development studies. Before moving to Norway, Daniel Chourrout was heading the Laboratory of Fish Genetics at INRA (French Institute of Research for Agriculture), with his own research on rainbow trout genetics and later on medaka development. His training is in Genetics (PhD from the University Pierre et Marie Curie in Paris).