title: Whole-genome duplications followed by tandem duplications drive diversification of the protein modifier SUMO in Angiosperms.
abstract: The ubiquitin-like modifier (UBL) SUMO (Small Ubiquitin-Like Modifier) regulates protein function. Structural rather than sequence homology typifies UBL families. However, individual UBL types, such as SUMO, show remarkable sequence conservation. Selection pressure also operates at the SUMO gene copy number, as increased SUMO levels activate immunity and alter flowering time in Arabidopsis. We show how, despite this selection pressure, the SUMO family has diversified into eight paralogues in Arabidopsis. Relationships between the paralogues were investigated using genome collinearity and gene tree analysis. We show that palaeopolyploidy followed by tandem duplications allowed expansion and then diversification of the SUMO genes. For example, Arabidopsis SUMO5 evolved from the pan-eudicot palaeohexaploidy event (gamma), which yielded three SUMO copies. Two gamma copies were preserved as archetype SUMOs, suggesting subfunctionalization, whereas the third copy served as a hotspot for SUMO diversification. The Brassicaceae-specific alpha duplication then caused the duplication of one archetype gamma copy, which, by subfunctionalization, allowed the retention of both SUMO1 and SUMO2. The other archetype gamma copy was simultaneously pseudogenized (SUMO4/6). A tandem duplication of SUMO2 subsequently yielded SUMO3 in the Brassicaceae crown group. SUMO3 potentially neofunctionalized in Arabidopsis, but it is lost in many Brassicaceae. Our advanced methodology allows the study of the birth and fixation of other paralogues in plants.
authors.affiliation: Molecular Plant Pathology, Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1089 XH, Amsterdam, the Netherlands.
authors.forename: Valentin
authors.initials: V
authors.lastname: Hammoudi
authors.affiliation: Molecular Plant Pathology, Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1089 XH, Amsterdam, the Netherlands.
authors.forename: Georgios
authors.initials: G
authors.lastname: Vlachakis
authors.affiliation: Biosystematics Group, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, the Netherlands.
authors.forename: M Eric
authors.initials: ME
authors.lastname: Schranz
authors.affiliation: Molecular Plant Pathology, Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1089 XH, Amsterdam, the Netherlands.
authors.forename: Harrold A
authors.initials: HA
authors.lastname: van den Burg
mesh_terms: D029681:Arabidopsis Proteins / Q000235:genetics; D019607:Brassicaceae / Q000235:genetics; D019143:Evolution, Molecular; D020440:Gene Duplication; D018745:Genome, Plant; D019684:Magnoliopsida / Q000235:genetics*; D014452:Ubiquitins / Q000235:genetics* / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; C477512:SUM1 protein, Arabidopsis; C477513:SUM2 protein, Arabidopsis; C403233:SUMO protein, plant; D014452:Ubiquitins
keywords: SUMO; evolution; immunity; neofunctionalization; palaeoploidy; paralogue; protein modification; ubiquitin-like modifier