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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.

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The model transition of the three oleosin isoform distributions (percentage) in genomes of land plants throughout evolution.
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pone-0103806-g006: The model transition of the three oleosin isoform distributions (percentage) in genomes of land plants throughout evolution.

Mentions: The newly obtained liverwort oleosin gene allowed us to perform the first detailed phylogenetic analysis of oleosin gene evolution including the most basally diverging lineage of land plants. The separate protein and nucleotide analyses yielded similar tree topologies with M-oleosins, L-oleosins, and H-oleosins forming three distinct groups (Figure 4 and 5). There appears to have been only one oleosin gene in the common ancestor of vascular plants, because in Marchantia, Physcomitrella, and Selaginella, oleosin genes within the same species form a clade indicating proliferation of gene families following their divergence. However, H-oleosins and L-oleosins coexist in monocots and eudicots along with the maintenance of M-isoforms (Figure 6). No H-oleosin gene was found in current available Amborella genome, which possesses the other two oleosin isoforms. Thus, there appears to have been at least two oleosin genes in the common ancestor of angiosperms, with subsequent proliferation of additional copies in some lineages.


Evolution of oleosin in land plants.

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

The model transition of the three oleosin isoform distributions (percentage) in genomes of land plants throughout evolution.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0103806-g006: The model transition of the three oleosin isoform distributions (percentage) in genomes of land plants throughout evolution.
Mentions: The newly obtained liverwort oleosin gene allowed us to perform the first detailed phylogenetic analysis of oleosin gene evolution including the most basally diverging lineage of land plants. The separate protein and nucleotide analyses yielded similar tree topologies with M-oleosins, L-oleosins, and H-oleosins forming three distinct groups (Figure 4 and 5). There appears to have been only one oleosin gene in the common ancestor of vascular plants, because in Marchantia, Physcomitrella, and Selaginella, oleosin genes within the same species form a clade indicating proliferation of gene families following their divergence. However, H-oleosins and L-oleosins coexist in monocots and eudicots along with the maintenance of M-isoforms (Figure 6). No H-oleosin gene was found in current available Amborella genome, which possesses the other two oleosin isoforms. Thus, there appears to have been at least two oleosin genes in the common ancestor of angiosperms, with subsequent proliferation of additional copies in some lineages.

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