Sex‐specific Positioning of the Mating Structure in Scale‐bearing Gametes of Monostroma angicava and Collinsiella cava (Ulvophyceae, Chlorophyta): A Possible Widespread Difference between Male and Female Gametes

Abstract

The gametes of chlorophytes can be divided into two morphological types (types α and β) based on the position of the mating structure relative to the flagella and eyespot. To elucidate the relationship between the morphological types and the sexes, we studied spatial relationships between the flagellar apparatus‐eyespot‐mating structures in biflagellate male and female gametes and their fate after fertilization in the anisogamous (Monostroma angicava) and the slightly anisogamous species (Collinsiella cava) using field emission scanning electron microscopy and transmission electron microscopy. The smaller male and larger female gametes of M. angicava had two basal bodies arranged at a 180° angle and the cell surface coated with square‐shaped body scales, except for the flagella and mating structures. The mating structure of the female gamete was located on the same side of the flagellar beat plane as the eyespot (type β), whereas that of the male gamete was located on the opposite side (type α). This mating structure arrangement was also confirmed in C. cava. The initial fusion when male and female gametes were mixed involved the mating structures. In a fusing pair of gametes, each flagellum of one gamete lay alongside one flagellum of the other gamete. As fusion proceeded, the gamete pair transformed into a quadriflagellate planozygote, in which the four basal bodies were arranged in a cruciate pattern. The eyespots were positioned side‐by‐side on the same side of the cell. These results suggest that the two morphological types of gametes are intimately correlated with the particular sexes.

Gamete dimorphism of the isogamous green alga (Chlamydomonas reinhardtii), is regulated by the mating type-determining gene, MID

“…Therefore, it is unknown whether MID orthologs are involved in the positioning of the mating structure in other volvocine species. In contrast, mating type- or sex-specific positioning of the mating structure is established in ulvophycean green seaweeds examined to date, in which male and female gametes always belong to the type α and β gametes 42 , respectively, but the mating type- or sex-determining gene has not been identified. Nevertheless, this relationship between the mating type (sex) and MSP (type α and β) was confirmed in the slightly anisogamous species U. prolifera and U. partita , respectively, using the mt – (male) and mt + (female) specific genes in the mating type locus, such as PRA1m (mt – ), and PRA1p (mt + ) 21 , 22 , which were identified using genome sequencing for both mating types of U. partita 21 and confirmed as mating type-specific genes by polymerase chain reaction (PCR)-based genotyping in U. prolifera 22 .…”

“…Gametophytes that produced type α and β gametes always had mt – - and mt + -specific genes, respectively, suggesting that MSP in Ulva is probably regulated by a mating type locus and mating type (sex)-determining gene, as in C. reinhardtii . Presumably, this is also true for other ulvophycean species because male and female gametes always exhibit the type α and β phenotypes, respectively 42 . However, the relationships between MSP and other mating type (sex)-specific traits (e.g.…”

“…6a ), this possibility has not been empirically verified in C. reinhardtii . However, these gamete and planozygote traits are prevalent in many chlorophyte species 41 , 42 , which usually produce biflagellate gametes with one eyespot and quadriflagellate planozygotes with two eyespots, and negative phototaxis is common in the planozygotes of C. reinhardtii and ulvophycean species (Supplementary Table 1 ). These findings suggest that asymmetric positioning of the mating structure, coordinated alignment of planozygote flagella and eyespot(s), and phototaxis are conserved in chlorophytes.…”

Swimming zygote formation mediated by symmetrically arranged cell fusion sites in the gametes of Chlamydomonas eugametos (Chlorophyceae, Chlorophyta)

“…Although the mating type-or sex-specific asymmetric positioning of the mating structure and/or cell fusion site seems to be widespread in the chlorophyte algae ranging from Nephroselmis olivacea (Nephroselmidophyceae) and seaweeds (Ulvophyceae) to C. reinhardtii (Chlorophyceae) (Nakayama & Inouye 2000;Suda et al 2004;Miyamura et al 2021), it remains unknown why this trait has been selected and conserved during the evolution of chlorophytes. Holmes and Dutcher (1989) noted the functional relationships between flagella, eyespot, and phototaxis in C. reinhardtii, and proposed that the mating type-specific asymmetric arrangement of the mating structure has evolved to ensure the proper arrangement of flagella and eyespots in the quadriflagellate swimming zygote for phototaxis during the evolution of Chlamydomonas; two flagella with the same physiological function derived from mt + and mt À gametes become a pair and align in parallel for coordinated movement and two eyespots derived from each parent align on the same side of the cell for proper phototaxis (Fig.…”

“…Overall, the symmetric arrangement of the mating structure/cell fusion site of the gamete and uncoordinated positioning of flagella and eyespots in the swimming zygote of C. eugametos is considered one of the traits found in the sexual reproduction of chlorophytes examined to date. The asymmetric type occurs more widely in the chlorophytes (Nephroselmidophyceae, Ulvophyceae, and Chlorophyceae) compared to the symmetric type (Nakayama & Inouye 2000;Suda et al 2004;Miyamura et al 2021) and from a phylogenetic viewpoint is likely an ancestral trait. In contrast, the symmetric type is known only in C. eugametos (Moewusinia, Chlorophyceae), although it may also be found in the vis-à-vis pair of Chlorococcum echinozygotum Starr (Moewusinia) (fig.…”