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

Abstract

The brown alga Ectocarpus siliculosus has a haploid–diploid life cycle that involves an alternation between two distinct generations, the sporophyte and the gametophyte. We describe a mutant, ouroboros ( oro ), in which the sporophyte generation is converted into a functional, gamete-producing gametophyte. The life history of the mutant thus consists of a continuous reiteration of the gametophyte generation. The oro mutant exhibited morphological features typical of the gametophyte generation and accumulated transcripts of gametophyte generation marker genes. Genetic analysis showed that oro behaved as a single, recessive, Mendelian locus that was unlinked to the IMMEDIATE UPRIGHT locus, which has been shown to be necessary for full expression of the sporophyte developmental program. The data presented here indicate that ORO is a master regulator of the gametophyte-to-sporophyte life cycle transition and, moreover, that oro represents a unique class of homeotic mutation that results in switching between two developmental programs that operate at the level of the whole organism.

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

“…Although brown algae have complex multicellularity, the total number of their TFs is not significantly increased, in contrast to what is found in metazoans and embryophytes. This may be explained by the presence of heterokont or brown-algae specific TFs that have not yet been described due to the paucity of functional studies in this group (39,40). Alternatively, the fact that Ectocarpus siliculosus has modular growth instead of stereotypical embryonic development (39) may account for the lack of complexity in their TFome.…”

Seaweed reproductive biology: environmental and genetic controls

“…Results have been published on two mutants, immediate upright (imm) and ouroboros (oro). The imm mutant exhibits partial conversion of the sporophyte generation into a gametophyte during early development, and the oro mutant generates a homeotic conversion of the sporophyte generation into a fully functional gametophyte (Peters et al 2008, Coelho et al 2011, Macaisne et al 2017. Ongoing studies focus on detecting the genes underlying the imm and oro mutants, which would allow comparison of the diploid program with other model systems.…”

The Ectocarpus IMMEDIATE UPRIGHT gene encodes a member of a novel family of cysteine-rich proteins with an unusual distribution across the eukaryotes

“…Biological replicates (duplicates) were cultivated in 90 mm Petri dishes in natural sea water supplemented with 0.01% Provasoli enrichment (Starr and Zeikus, 1993) under a 12 h light:12 h dark cycle of white fluorescent light (10-30 mol m −2 s −1 photon fluence rate). Total RNA was extracted from between 0.05 and 0.1 g of tissue as described previously (Coelho et al, 2011). Total RNA was quantified and cDNA, synthesised from an oligo(dT) primer for each replicate, was independently fragmented, prepared and sequenced by Fasteris (Plan-les-Ouates, Switzerland) using an Illumina HiSeq 2000 platform to generate 100 bp single-end reads.…”

“…Total RNA was extracted as previously described (Coelho et al, 2011) from five or six biological replicates each of imm mutant partheno-sporophytes (Ec419), wild-type partheno-sporophytes (Ec32), wild-type heterozygous diploid sporophytes (Ec17) and wild-type gametophytes (Ec32). These samples were not the same as those used for the RNA-seq analysis.…”

“…has a haploid-diploid life cycle that involves alternation between two generations, which both consist of uniserate filaments with a small number of different cell types and bearing simple reproductive structures . The morphological similarity of the two generations has allowed mutants affected both in switching between generations (Coelho et al, 2011) and in generation-related developmental processes (Peters et al, 2008) to be isolated. The immediate upright (imm) mutant is particularly interesting because it has major effects on the early development of the sporophyte generation but causes no visible phenotype during the gametophyte generation (Peters et al, 2008).…”