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A comparative test of the gamete dynamics theory for the evolution of anisogamy in Bryopsidales green algae.

ABSTRACT: Gamete dynamics theory proposes that anisogamy arises by disruptive selection for gamete numbers versus gamete size and predicts that female/male gamete size (anisogamy ratio) increases with adult size and complexity. Evidence has been that in volvocine green algae, the anisogamy ratio correlates positively with haploid colony size. However, green algae show notable exceptions. We focus on Bryopsidales green algae. While some taxa have a diplontic life cycle in which a diploid adult (=fully grown) stage arises directly from the zygote, many taxa have a haplodiplontic life cycle in which haploid adults develop indirectly: the zygote first develops into a diploid adult (sporophyte) which later undergoes meiosis and releases zoospores, each growing into a haploid adult gametophyte. Our comparative analyses suggest that, as theory predicts: (i) male gametes are minimized, (ii) female gamete sizes vary, probably optimized by number versus survival as zygotes, and (iii) the anisogamy ratio correlates positively with diploid (but not haploid) stage complexity. However, there was no correlation between the anisogamy ratio and diploid adult stage size. Increased environmental severity (water depth) appears to drive increased diploid adult stage complexity and anisogamy ratio: gamete dynamics theory correctly predicts that anisogamy evolves with the (diploid) stage directly provisioned by the zygote.

SUBMITTER: Togashi T

PROVIDER: S-EPMC8074922 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe Viridiplantae (green algae and land plants) consist of two monophyletic lineages: the Chlorophyta and the Streptophyta. Most green algae belong to the Chlorophyta, while the Streptophyta include all land plants and a small group of freshwater algae known as Charophyceae. Eukaryotes attach a poly-A tail to the 3' ends of most nuclear-encoded mRNAs. In embryophytes, animals and fungi, the signal for polyadenylation contains an A-rich sequence (often AAUAAA or related sequence) 13 to 30 nucleotides upstream from the cleavage site, which is commonly referred to as the near upstream element (NUE). However, it has been reported that the pentanucleotide UGUAA is used as polyadenylation signal for some genes in volvocalean algae.ResultsWe set out to investigate polyadenylation signal differences between streptophytes and chlorophytes that may have emerged shortly after the evolutionary split between Streptophyta and Chlorophyta. We therefore analyzed expressed genes (ESTs) from three streptophyte algae, Mesostigma viride, Klebsormidium subtile and Coleochaete scutata, and from two early-branching chlorophytes, Pyramimonas parkeae and Scherffelia dubia. In addition, to extend the database, our analyses included ESTs from six other chlorophytes (Acetabularia acetabulum, Chlamydomonas reinhardtii, Helicosporidium sp. ex Simulium jonesii, Prototheca wickerhamii, Scenedesmus obliquus and Ulva linza) and one streptophyte (Closterium peracerosum). Our results indicate that polyadenylation signals in green algae vary widely. The UGUAA motif is confined to late-branching Chlorophyta. Most streptophyte algae do not have an A-rich sequence motif like that in embryophytes, animals and fungi. We observed polyadenylation signals similar to those of Arabidopsis and other land plants only in Mesostigma.ConclusionPolyadenylation signals in green algae show considerable variation. A new NUE (UGUAA) was invented in derived chlorophytes and replaced not only the A-rich NUE but the complete poly(A) signal in all chlorophytes investigated except Scherffelia (only NUE replaced) and Pyramimonas (UGUAA completely missing). The UGUAA element is completely absent from streptophytes. However, the structure of the poly(A) signal was often modified in streptophyte algae. In most species investigated, an A-rich NUE is missing; instead, these species seem to rely mainly on U-rich elements.

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A comparative test of the gamete dynamics theory for the evolution of anisogamy in Bryopsidales green algae.

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