Abstract
Extracellular matrices regulate biological processes at the level of cells, tissues, and in some cases, entire multicellular organisms. The subphylum Urochordata exemplifies the latter case, where animals are partially or completely enclosed in “houses” or “tunics”. Despite this common strategy, we show that the house proteome of the appendicularian, Oikopleura, has very little in common with the proteome of the sister class, ascidian, Ciona. Of 80 identified house proteins (oikosins), ∼half lack domain modules or similarity to known proteins, suggesting de novo appearance in appendicularians. Gene duplication has been important in generating almost 1/3 of the current oikosin complement, with serial duplications up to 8 paralogs in one family. Expression pattern analyses revealed that individual oikosins are produced from specific fields of cells within the secretory epithelium, but in some cases, migrate up to at least 20 cell diameters in extracellular space to combine in defined house structures. Interestingly, peroxidasin and secretory phospholipase A2 domains, implicated in innate immune defence are secreted from the anlage associated with the food-concentrating filter, suggesting that this extra-organismal structure may play, in part, such a role in Oikopleura. We also show that sulfation of proteoglycans is required for the hydration and inflation of pre-house rudiments into functional houses. Though correct proportioning in the production of oikosins would seem important in repetitive assembly of the complex house structure, the genomic organization of oikosin loci appears incompatible with common enhancers or locus control regions exerting such a coordinate regulatory role. Thus, though all tunicates employ extracellular matrices based on a cellulose scaffold as a defining feature of the subphylum, they have evolved radically different protein compositions associated with this common underlying structural theme.
Highlights
Cellulose produced by plants, bacteria and some fungi, is the most abundant biopolymer on earth
Secretion of Oikosins The protein mass spectrometric analysis of pre-house rudiments performed in this study identified 66 new oikosin proteins to add to the complement of 14 oikosins that had been previously characterized [8,10,11]
Since they were isolated from extracellular, pre-house rudiments, oikosins were generally classified as secreted proteins
Summary
Bacteria and some fungi, is the most abundant biopolymer on earth. Animals are incapable of cellulose synthesis, with one exception, marine tunicates. Among the three tunicate sister classes, Appendicularians, or Larvaceans, retain the larval appearance throughout their life cycle and remain pelagic, in contrast to benthic ascidians. They secrete a complex extracellular filter-feeding house, which in the Oikopleuridae completely surrounds the animal. The ability of tunicates to synthesise cellulose has most probably evolved after a horizontal gene transfer event, as the tunicate cellulose synthase (CesA) is more closely related to prokaryotic enzymes than plant CesA [4,5]. Appendicularians possess two CesA genes with distinct temporal and functional specializations during larval tail development and post-metamorphic house synthesis [5], as opposed to sister ascidians with only one cellulose synthase gene
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
