title: Evolution of oleosin in land plants.
abstract: Oleosins form a steric barrier surface on lipid droplets in cytoplasm, preventing them from contacting and coalescing with adjacent droplets. Oleosin genes have been detected in numerous plant species. However, the presence of oleosin genes in the most basally diverging lineage of land plants, liverworts, has not been reported previously. Thus we explored whether liverworts have an oleosin gene. In Marchantia polymorpha L., a thalloid liverwort, one predicted sequence was found that could encode oleosin, possessing the hallmark of oleosin, a proline knot (-PX5SPX3P-) motif. The phylogeny of the oleosin gene family in land plants was reconstructed based on both nucleotide and amino acid sequences of oleosins, from 31 representative species covering almost all the main lineages of land plants. Based on our phylogenetic trees, oleosin genes were classified into three groups: M-oleosins (defined here as a novel group distinct from the two previously known groups), low molecular weight isoform (L-oleosin), and high molecular weight isoform (H-oleosin), according to their amino-acid organization, phylogenetic relationships, expression tissues, and immunological characteristics. In liverworts, mosses, lycophytes, and gymnosperms, only M-oleosins have been described. In angiosperms, however, while this isoform remains and is highly expressed in the gametophyte pollen tube, two other isoforms also occur, L-oleosins and H-oleosins. Phylogenetic analyses suggest that the M-oleosin isoform is the precursor to the ancestor of L-oleosins and H-oleosins. The later two isoforms evolved by successive gene duplications in ancestral angiosperms. At the genomic level, most oleosins possess no introns. If introns are present, in both the L-isoform and the M-isoform a single intron inserts behind the central region, while in the H-isoform, a single intron is located at the 5'-terminus. This study fills a major gap in understanding functional gene evolution of oleosin in land plants, shedding new light on evolutionary transitions of lipid storage strategies.
authors.affiliation: School of Life Science, East China Normal University, Shanghai, China; University and Jepson Herbaria, and Department of Integrative Biology, University of California, Berkeley, California, United State of America.
authors.forename: Yuan
authors.initials: Y
authors.lastname: Fang
authors.affiliation: School of Life Science, East China Normal University, Shanghai, China.
authors.forename: Rui-Liang
authors.initials: RL
authors.lastname: Zhu
authors.affiliation: University and Jepson Herbaria, and Department of Integrative Biology, University of California, Berkeley, California, United State of America.
authors.forename: Brent D
authors.initials: BD
authors.lastname: Mishler
mesh_terms: D000595:Amino Acid Sequence; D029681:Arabidopsis Proteins / Q000145:classification / Q000235:genetics; D001483:Base Sequence; D019295:Computational Biology; D019143:Evolution, Molecular; D020440:Gene Duplication / Q000235:genetics; D016013:Likelihood Functions; D047008:Marchantia / Q000737:chemistry*; D008957:Models, Genetic; D008969:Molecular Sequence Data; D008970:Molecular Weight; D010802:Phylogeny; D010940:Plant Proteins / Q000145:classification* / Q000235:genetics*; D020033:Protein Isoforms / Q000235:genetics; D017422:Sequence Analysis, DNA
chemical_list: D029681:Arabidopsis Proteins; D010940:Plant Proteins; D020033:Protein Isoforms; C079353:oleosin protein, Arabidopsis
references.citation: Science. 2013 Dec 20;342(6165):1241089
references.pmid: 24357323
references.citation: Bioinformatics. 2007 Nov 1;23(21):2947-8
references.pmid: 17846036
references.citation: BMC Plant Biol. 2011 Sep 29;11:132
references.pmid: 21958236
references.citation: J Biochem. 1997 Oct;122(4):819-24
references.pmid: 9399587
references.citation: Plant Physiol. 1996 Apr;110(4):1055-61
references.pmid: 8934621
references.citation: Biochem J. 1996 Aug 1;317 ( Pt 3):956-8
references.pmid: 8760389
references.citation: Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):8007-12
references.pmid: 12808149
references.citation: Physiol Plant. 2001 Jul;112(3):301-307
references.pmid: 11473685
references.citation: Plant Mol Biol. 1996 May;31(2):429-33
references.pmid: 8756608
references.citation: J Plant Physiol. 2011 Nov 15;168(17):2015-20
references.pmid: 21803444
references.citation: Plant Mol Biol. 1992 Jun;19(3):443-53
references.pmid: 1377966
references.citation: Syst Biol. 2008 Oct;57(5):758-71
references.pmid: 18853362
references.citation: Annu Rev Genet. 2005;39:339-58
references.pmid: 16285864
references.citation: Nature. 2013 May 30;497(7451):579-84
references.pmid: 23698360
references.citation: Biosci Biotechnol Biochem. 2002 Oct;66(10):2146-53
references.pmid: 12450125
references.citation: J Biol Chem. 2002 Jun 21;277(25):22677-84
references.pmid: 11929861
references.citation: Trends Cell Biol. 2007 Aug;17(8):363-9
references.pmid: 17766117
references.citation: J Plant Physiol. 2007 Jan;164(1):104-7
references.pmid: 16762452
references.citation: Plant Physiol. 1991 Aug;96(4):1395-7
references.pmid: 16668353
references.citation: Proteomics. 2009 Jun;9(12):3268-84
references.pmid: 19562800
references.citation: Plant Mol Biol. 1995 Jun;28(3):583-8
references.pmid: 7632926
references.citation: Gene. 1988 Dec 20;73(2):259-71
references.pmid: 3072259
references.citation: Plant Mol Biol. 1994 Dec;26(6):1981-7
references.pmid: 7858232
references.citation: Prog Lipid Res. 1993;32(3):247-80
references.pmid: 8140114
references.citation: Am J Bot. 2011 Mar;98(3):352-69
references.pmid: 21613131
references.citation: Science. 2001 Jun 29;292(5526):2482-5
references.pmid: 11431566
references.citation: J Plant Physiol. 2006 May;163(7):691-708
references.pmid: 16442665
references.citation: J Biol Chem. 1990 Feb 5;265(4):2238-43
references.pmid: 2298748
references.citation: Planta. 1995;195(3):469-70
references.pmid: 7766048
references.citation: Plant Physiol. 2013 Apr;161(4):1862-74
references.pmid: 23391579
references.citation: Plant Physiol. 1993 Feb;101(2):697-8
references.pmid: 8278515
references.citation: Plant Mol Biol. 1992 Apr;18(6):1177-9
references.pmid: 1600152
references.citation: Cell. 1997 Dec 26;91(7):875-9
references.pmid: 9428511
references.citation: Planta. 1994;193(3):461-9
references.pmid: 7764875
references.citation: Eukaryot Cell. 2010 Jan;9(1):97-106
references.pmid: 19915074
references.citation: Plant Physiol Biochem. 2011 Mar;49(3):352-6
references.pmid: 21251844
references.citation: Plant Cell. 1997 Sep;9(9):1621-31
references.pmid: 9338964
references.citation: Plant Cell Physiol. 2007 Jun;48(6):812-21
references.pmid: 17468126
references.citation: BMC Genomics. 2010 Feb 11;11:106
references.pmid: 20149226
references.citation: Bioinformatics. 2006 Nov 1;22(21):2688-90
references.pmid: 16928733
references.citation: Nucleic Acids Res. 2010 Jul;38(Web Server issue):W695-9
references.pmid: 20439314
references.citation: Prog Lipid Res. 2001 Sep;40(5):325-438
references.pmid: 11470496
references.citation: Planta. 2012 Jul;236(1):19-33
references.pmid: 22231009
references.citation: J Chromatogr B Biomed Sci Appl. 1998 Feb 27;706(1):131-40
references.pmid: 9544815
references.citation: J Mol Biol. 1990 Oct 5;215(3):403-10
references.pmid: 2231712
references.citation: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references.pmid: 15034147
references.citation: Biochim Biophys Acta. 2009 Jun;1791(6):399-407
references.pmid: 18996222
references.citation: Plant Physiol. 2009 Jul;150(3):1192-203
references.pmid: 19420327
references.citation: Plant Mol Biol. 1991 Nov;17(5):1095-8
references.pmid: 1932682
references.citation: Plant Physiol. 2004 Nov;136(3):3427-34
references.pmid: 15542496