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A unique life cycle transition in the red seaweed Pyropia yezoensis depends on apospory.

ABSTRACT: Plant life cycles consist of two temporally separated stages: a haploid gametophyte and a diploid sporophyte. In plants employing a haploid-diploid sexual life cycle, the transition from sporophyte to gametophyte generally depends on meiosis. However, previous work has shown that in the red seaweed Pyropia yezoensis, this transition is independent of meiosis, though how and when it occurs is unknown. Here, we explored this question using transcriptomic profiling of P. yezoensis gametophytes, sporophytes, and conchosporangia parasitically produced on sporophytes. We identify a knotted-like homeobox gene that is predominately expressed in the conchosporangium and may determine its identity. We also find that spore-like single cells isolated from the conchosporangium develop directly into gametophytes, indicating that the gametophyte identity is established before the release of conchospores and prior to the onset of meiosis. Based on our findings, we propose a triphasic life cycle for P. yezoensis involving production of gametophytes by apospory.

SUBMITTER: Mikami K

PROVIDER: S-EPMC6685973 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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A unique life cycle transition in the red seaweed Pyropia yezoensis depends on apospory.

Mikami Koji K Li Chengze C Li Chengze C Irie Ryunosuke R Hama Yoichiro Y

Communications biology 20190807

Plant life cycles consist of two temporally separated stages: a haploid gametophyte and a diploid sporophyte. In plants employing a haploid-diploid sexual life cycle, the transition from sporophyte to gametophyte generally depends on meiosis. However, previous work has shown that in the red seaweed Pyropia yezoensis, this transition is independent of meiosis, though how and when it occurs is unknown. Here, we explored this question using transcriptomic profiling of P. yezoensis< ...[more]

PMID: 31396579

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Project description:BackgroundPyropia haitanensis and P. yezoensis are two economically important marine crops that are also considered to be research models to study the physiological ecology of intertidal seaweed communities, evolutionary biology of plastids, and the origins of sexual reproduction. This plastid genome information will facilitate study of breeding, population genetics and phylogenetics.Principal findingsWe have fully sequenced using next-generation sequencing the circular plastid genomes of P. hatanensis (195,597 bp) and P. yezoensis (191,975 bp), the largest of all the plastid genomes of the red lineage sequenced to date. Organization and gene contents of the two plastids were similar, with 211-213 protein-coding genes (including 29-31 unknown-function ORFs), 37 tRNA genes, and 6 ribosomal RNA genes, suggesting a largest coding capacity in the red lineage. In each genome, 14 protein genes overlapped and no interrupted genes were found, indicating a high degree of genomic condensation. Pyropia maintain an ancient gene content and conserved gene clusters in their plastid genomes, containing nearly complete repertoires of the plastid genes known in photosynthetic eukaryotes. Similarity analysis based on the whole plastid genome sequences showed the distance between P. haitanensis and P. yezoensis (0.146) was much smaller than that of Porphyra purpurea and P. haitanensis (0.250), and P. yezoensis (0.251); this supports re-grouping the two species in a resurrected genus Pyropia while maintaining P. purpurea in genus Porphyra. Phylogenetic analysis supports a sister relationship between Bangiophyceae and Florideophyceae, though precise phylogenetic relationships between multicellular red alage and chromists were not fully resolved.ConclusionsThese results indicate that Pyropia have compact plastid genomes. Large coding capacity and long intergenic regions contribute to the size of the largest plastid genomes reported for the red lineage. Possessing the largest coding capacity and ancient gene content yet found reveal that Pyropia are more primitive multicellular red algae.

Project description:BackgroundAlginate lyases belonging to polysaccharide lyase family-7 (PL-7) are the most well studied on their structures and functions among whole alginate lyases. However, all characterized PL-7 alginate lyases are from prokaryotic bacteria cells. Here we report the first identification of eukaryotic PL-7 alginate lyase from marine red alga Pyropia yezoensis.MethodsThe cDNA encoding an alginate lyase PyAly was cloned and was used for the construction of recombinant PyAly (rPyAly) expression system in Escherichia coli. Purified rPyAly was assayed to identify its enzymatic properties. Its expression pattern in P. yessoensis was also investigated.ResultsPyAly is likely a secreted protein consisting of an N-terminal signal peptide of 25 residues and a catalytic domain of 216 residues. The amino-acid sequence of the catalytic domain showed 19-29% identities to those of bacterial characterized alginate lyases classified into family PL-7. Recombinant PyAly protein, rPyAly, which was produced with E. coli BL21(DE3) by cold-inducible expression system, drastically decreased the viscosity of alginate solution in the early stage of reaction. The most preferable substrate for rPyAly was the poly(M) of alginate with an optimal temperature and pH at 35oC and 8.0, respectively. After reaction, unsaturated tri- and tetra-saccharides were produced from poly(M) as major end products. These enzymatic properties indicated that PyAly is an endolytic alginate lyase belonging to PL-7. Moreover, we found that the PyAly gene is split into 4 exons with 3 introns. PyAly was also specifically expressed in the gametophytic haplopid stage.ConclusionThis study demonstrates that PyAly in marine red alga P. yezoensis is a novel PL-7 alginate lyase with an endolytic manner. PyAly is a gametophyte-specifically expressed protein and its structural gene is composed of four exons and three introns. Thus, PyAly is the first enzymatically characterized eukaryotic PL-7 alginate lyase.

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A unique life cycle transition in the red seaweed Pyropia yezoensis depends on apospory.

Publications

A unique life cycle transition in the red seaweed <i>Pyropia yezoensis</i> depends on apospory.

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