Abstract
Although sexual reproduction is believed to play a major role in the high diversification rates and species richness of diatoms, a mechanistic understanding of diatom life cycle control is virtually lacking. Diatom sexual signalling is controlled by a complex, yet largely unknown, pheromone system. Here, a sex-inducing pheromone (SIP+) of the benthic pennate diatom Seminavis robusta was identified by comparative metabolomics, subsequently purified, and physicochemically characterized. Transcriptome analysis revealed that SIP+ triggers the switch from mitosis-to-meiosis in the opposing mating type, coupled with the transcriptional induction of proline biosynthesis genes, and the release of the proline-derived attraction pheromone. The induction of cell cycle arrest by a pheromone, chemically distinct from the one used to attract the opposite mating type, highlights the existence of a sophisticated mechanism to increase chances of mate finding, while keeping the metabolic losses associated with the release of an attraction pheromone to a minimum.
Highlights
Sexual reproduction is believed to play a major role in the high diversification rates and species richness of diatoms, a mechanistic understanding of diatom life cycle control is virtually lacking
The location and morphology of the chloroplasts of growth-arrested cells are indicative for the G1 phase. These results suggest that cells below the SST secrete mating type-specific pheromones with the ability to arrest the cell cycle of the cells of the compatible mating type in the G1 phase
Using a comparative metabolomics approach, a pheromone, called SIP+, that is exclusively produced by MT+ cells below the SST was purified
Summary
Sexual reproduction is believed to play a major role in the high diversification rates and species richness of diatoms, a mechanistic understanding of diatom life cycle control is virtually lacking. Diatoms are a key ecological and extremely diverse group of microalgae[1] that contribute to about 20 percent of the global carbon fixation[2] Their unique diplontic life cycle, involving a size-dependent transition from mitotically dividing cells to cells capable of sexual reproduction[3,4], is a defining feature of diatom biology[5]. It has been long suspected that diatoms employ chemical cues to facilitate mate-finding and sexual reproduction[4,6,7,8,9], the first molecular structure of a diatom pheromone was only recently revealed for the model species Seminavis robusta[10] In this species, a two-step signalling system has been identified, in which mating-compatible cells below the SST produce sex-inducing pheromones (in the following abbreviated as SIP) that trigger the production of the proline-derived diketopiperazine (in the following abbreviated as diproline)[10] (Fig. 1). We verified the existence of a chemically distinct SIP that is produced by MT− cells (SIP−) and found that both chemically distinct SIPs, besides sexualizing cells, reciprocally arrest the cell cycle at the G1 phase
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