Limits...
Evolution of oleosin in land plants.

Fang Y, Zhu RL, Mishler BD - PLoS ONE (2014)

Bottom Line: The later two isoforms evolved by successive gene duplications in ancestral angiosperms.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.

View Article: PubMed Central - PubMed

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.

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.

Show MeSH

Related in: MedlinePlus

The intron position in each of the three oleosin isoforms.At the nucleotide level, Joint Genome Institute database predict that most of oleosins possess no introns, whereas oleosin genes with intron insertion sites a single intron preceding or following the sequence encoding the central domain. The intron insertion sites are variable in oleosins, but nearly conserved within each isoform. The region of the central domain is labeled in the ‘consensus’ row. The intron positions are in between of the two encoding regions: exon1 and exon2. (A) M-oleosins; (B) L-oleosins; (C) H-oleosins.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4126676&req=5

pone-0103806-g007: The intron position in each of the three oleosin isoforms.At the nucleotide level, Joint Genome Institute database predict that most of oleosins possess no introns, whereas oleosin genes with intron insertion sites a single intron preceding or following the sequence encoding the central domain. The intron insertion sites are variable in oleosins, but nearly conserved within each isoform. The region of the central domain is labeled in the ‘consensus’ row. The intron positions are in between of the two encoding regions: exon1 and exon2. (A) M-oleosins; (B) L-oleosins; (C) H-oleosins.

Mentions: The topology is rooted by Marchantia polymorpha representing the most basally diverging lineage of land plants, liverworts. The three oleosin isoforms are framed separately. The information followed the second underscore in each terminal node shows the position of intron in oleosin nucleotide sequences. Abbreviations used in Figures 4, 5 and 7 are as follows: OLE, published or submitted oleosin genes in GenBank (For more information, see Table S1 online); ole (lower case), predicted oleosin genes from sequenced species in Joint Genome Institute database in this study; 0 (the number behind the second underscore in terminal node), no intron insertion in encoding region; 1(P), the site of intron insertion before the central domain coding region; (P)1, the site of intron insertion after the central domain coding region.


Evolution of oleosin in land plants.

Fang Y, Zhu RL, Mishler BD - PLoS ONE (2014)

The intron position in each of the three oleosin isoforms.At the nucleotide level, Joint Genome Institute database predict that most of oleosins possess no introns, whereas oleosin genes with intron insertion sites a single intron preceding or following the sequence encoding the central domain. The intron insertion sites are variable in oleosins, but nearly conserved within each isoform. The region of the central domain is labeled in the ‘consensus’ row. The intron positions are in between of the two encoding regions: exon1 and exon2. (A) M-oleosins; (B) L-oleosins; (C) H-oleosins.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4126676&req=5

pone-0103806-g007: The intron position in each of the three oleosin isoforms.At the nucleotide level, Joint Genome Institute database predict that most of oleosins possess no introns, whereas oleosin genes with intron insertion sites a single intron preceding or following the sequence encoding the central domain. The intron insertion sites are variable in oleosins, but nearly conserved within each isoform. The region of the central domain is labeled in the ‘consensus’ row. The intron positions are in between of the two encoding regions: exon1 and exon2. (A) M-oleosins; (B) L-oleosins; (C) H-oleosins.
Mentions: The topology is rooted by Marchantia polymorpha representing the most basally diverging lineage of land plants, liverworts. The three oleosin isoforms are framed separately. The information followed the second underscore in each terminal node shows the position of intron in oleosin nucleotide sequences. Abbreviations used in Figures 4, 5 and 7 are as follows: OLE, published or submitted oleosin genes in GenBank (For more information, see Table S1 online); ole (lower case), predicted oleosin genes from sequenced species in Joint Genome Institute database in this study; 0 (the number behind the second underscore in terminal node), no intron insertion in encoding region; 1(P), the site of intron insertion before the central domain coding region; (P)1, the site of intron insertion after the central domain coding region.

Bottom Line: The later two isoforms evolved by successive gene duplications in ancestral angiosperms.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.

View Article: PubMed Central - PubMed

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.

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.

Show MeSH
Related in: MedlinePlus