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Stepwise and independent origins of roots among land plants.

ABSTRACT: Roots are one of the three fundamental organ systems of vascular plants1, and have roles in anchorage, symbiosis, and nutrient and water uptake2-4. However, the fragmentary nature of the fossil record obscures the origins of roots and makes it difficult to identify when the sole defining characteristic of extant roots-the presence of self-renewing structures called root meristems that are covered by a root cap at their apex1-9-evolved. Here we report the discovery of what are-to our knowledge-the oldest meristems of rooting axes, found in the earliest-preserved terrestrial ecosystem10 (the 407-million-year-old Rhynie chert). These meristems, which belonged to the lycopsid Asteroxylon mackiei11-14, lacked root caps and instead developed a continuous epidermis over the surface of the meristem. The rooting axes and meristems of A. mackiei are unique among vascular plants. These data support the hypothesis that roots, as defined in extant vascular plants by the presence of a root cap7, were a late innovation in the vascular lineage. Roots therefore acquired traits in a stepwise fashion. The relatively late origin in lycophytes of roots with caps is consistent with the hypothesis that roots evolved multiple times2 rather than having a single origin1, and the extensive similarities between lycophyte and euphyllophyte roots15-18 therefore represent examples of convergent evolution. The key phylogenetic position of A. mackiei-with its transitional rooting organ-between early diverging land plants that lacked roots and derived plants that developed roots demonstrates how roots were 'assembled' during the course of plant evolution.

SUBMITTER: Hetherington AJ

PROVIDER: S-EPMC6175059 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Stepwise and independent origins of roots among land plants.

Hetherington Alexander J AJ Dolan Liam L

Nature 20180822 7722

Roots are one of the three fundamental organ systems of vascular plants1, and have roles in anchorage, symbiosis, and nutrient and water uptake2-4. However, the fragmentary nature of the fossil record obscures the origins of roots and makes it difficult to identify when the sole defining characteristic of extant roots-the presence of self-renewing structures called root meristems that are covered by a root cap at their apex1-9-evolved. Here we report the discover ...[more]

PMID: 30135586

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Project description: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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Stepwise and independent origins of roots among land plants.

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Stepwise and independent origins of roots among land plants.

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