Role of endoreduplication and apomeiosis during parthenogenetic reproduction in the model brown alga Ectocarpus

Abstract

Summary• The filamentous brown alga Ectocarpus has a complex life cycle, involving alternation between independent and morphologically distinct sporophyte and gametophyte generations. In addition to this basic haploid-diploid life cycle, gametes can germinate parthenogenetically to produce parthenosporophytes. This article addresses the question of how parthenosporophytes, which are derived from a haploid progenitor cell, are able to produce meiospores in unilocular sporangia, a process that normally involves a reductive meiotic division.• We used flow cytometry, multiphoton imaging, culture studies and a bioinformatics survey of the recently sequenced Ectocarpus genome to describe its life cycle under laboratory conditions and the nuclear DNA changes which accompany key developmental transitions.• Endoreduplication occurs during the first cell cycle in about one-third of parthenosporophytes. The production of meiospores by these diploid parthenosporophytes involves a meiotic division similar to that observed in zygote-derived sporophytes. By contrast, meiospore production in parthenosporophytes that fail to endoreduplicate occurs via a nonreductive apomeiotic event.• Our results highlight Ectocarpus's reproductive and developmental plasticity and are consistent with previous work showing that its life cycle transitions are controlled by genetic mechanisms and are independent of ploidy.

OUROBOROS is a master regulator of the gametophyte to sporophyte life cycle transition in the brown alga Ectocarpus

“…For example, several lines of evidence indicated that life cycle generation can be uncoupled from ploidy. Haploid, diploid, or tetraploid partheno-sporophytes (25,26) and haploid, diploid, and aneuploid gametophytes (26)(27)(28) have been observed in culture. Here we have shown that zygotes derived from a cross between male and female oro mutants give rise to functional, diploid gametophytes.…”

Seaweed reproductive biology: environmental and genetic controls

“…Knowledge of life cycle progression at the molecular level is accumulating rapidly for Ectocarpus, a brown algal model species with a haploiddiploid life cycle with subtle but distinct morphological differentiation between the sporophyte and gametophyte phases ( Figure 1B). The complex life cycle of Ectocarpus has shown that life cycle transitions are controlled by genetic mechanisms instead of ploidy level, and can show a large degree of developmental plasticity (Müller 1967, Bothwell et al 2010. However the identity of the molecular players is only just being revealed thanks to the combination of a whole genome sequence for Ectocarpus and life cycle mutants .…”

Genomics of brown algae: current advances and future prospects

“…These diploid individuals can then initiate meiotic cell division in the same manner as diploid sporophytes derived from the fusion of two gametes. A complementary bioinformatic analysis of the genome sequence identified a number of genes that potentially play a role in mediating the endoreduplicative cell division (Bothwell et al, 2010b). These results therefore explained how one third of the partheno-sporophytes produce meio-spores, but what about the remaining two thirds?…”

“…How they are able to do this has been a mystery because meio-spores are normally derived from a meiotic cell division that is followed by several mitotic divisions, and it has been difficult to see how this could occur when the initial cells of the partheno-sporophytes are haploid gametes. However, careful analysis of ploidy levels in the cells of developing partheno-sporophytes indicated that about one third of these individuals underwent an endoreduplication event very early in development (Bothwell et al, 2010a;Bothwell et al, 2010b). These diploid individuals can then initiate meiotic cell division in the same manner as diploid sporophytes derived from the fusion of two gametes.…”