Sex‐Specific Genes and their Expression in the Life History of the Red Alga Bostrychia moritziana (Ceramiales, Rhodomelaceae)

Abstract

Diverse sex determination mechanisms have been reported in eukaryotes, but little is known about the genetic pathways leading to sex determination in red algae. Sex‐specific genes that could be involved in sex determination and sexual differentiation were investigated in the red alga Bostrychia moritziana by analyzing the transcriptomes of various phases including males, females, and tetrasporophytes. Sex dominantly expressed genes which showed >10‐fold difference between sexes was isolated using comparative RNA‐seq analysis. We found 19 gene homologues, 10 from males, and nine from females, that were found only in one sex in genomic amplification using strains collected from five different localities. Most of the sex‐specific genes are involved in important cellular processes including chromosome segregation, nucleo‐cytoplasmic protein shuttling, or tRNA modification. Quantitative PCR analysis showed that some sex‐specific genes were differently regulated during critical events of sexual reproduction like fertilization and carposporophyte development. We could localize the expression of a male‐specific gene in spermatia before and after gamete binding using RNA in situ hybridization. Amino acid sequence identity between male and female homologues of importin alpha gene and PreQ(0) reductase were highly divergent (75% and 74%, respectively), suggesting that these divergent homologues are on non–recombining UV‐type chromosomes in their respective sexes. Another set of transcripts were found that were sex dominantly expressed, but not sex‐specific. Nineteen out of 39 sex dominantly expressed transcripts were annotated to transposable elements. Our results suggest that sexual differentiation in B. moritziana may be achieved by multi‐level regulation of cellular processes, both from genes present only in one sex and differential expression of shared genes.

Field survey of the phase and sex ratios of the brown alga Dictyota dichotoma (Dictyotales, Phaeophyceae) using sex‐specific molecular markers

“…The development of microsatellite-based markers, such as RAPD primers and ddRAD-seq variants, requires library construction and screening large numbers of primer sets, which are time-consuming and laborious steps (Lipinska et al 2015). Our approach for identifying genes with sex-specific expression based on comparisons with genome information for E. siliculosus can be performed using RNA-seq data for female and male strains, without whole genome data, and can be applied to non-model organisms (e.g., Shim et al 2021;Nishitsuji et al 2022).…”

“…Our approach for identifying genes with sex‐specific expression based on comparisons with genome information for E. siliculosus can be performed using RNA‐seq data for female and male strains, without whole genome data, and can be applied to non‐model organisms (e.g., Shim et al . 2021; Nishitsuji et al . 2022).…”

Synchronous nuclear division and the role of the cytoskeleton in the multinucleate red alga <italic>Griffithsia monilis</italic>

“…It is possible that the synchronization of nuclear division in G. monilis is regulated by Ca 2+ -mediated ROS signaling: a study of the woundhealing process in the same species showed that the hydrogen peroxide production induced by the intracellular calcium influx mediates wound healing, including the division of repair cells (Moon et al 2022). The same type of signaling has also been reported to mediate the fertilization process in other red algae (Shim et al 2021). Further studies are needed to determine whether Ca 2+ -mediated ROS signaling is also involved in the coordination of nuclear division in multinucleate cells.…”

“…Studies of the function of the cytoskeletal component in red algae have mainly been carried out during fertilization (Shim et al 2020), as it is relatively easy for inhibitors to enter the reproductive cells. Actin has been shown to mediate the movement of spermatial nuclei within the trichogynes of several red algae during fertilization (Kim and Kim 1999, Wilson et al 2002, Shim et al 2021). However, investigations on the involvement of microtubules in various cellular responses in red algae have only recently begun (Moon et al 2022).…”

Red macroalgae in the genomic era

“…Genetic diversity, speciation, and ecology have been documented within the Bostrychia genus (Karsten et al ., 1993; Zuccarello & West, 2011) where aspects of reproduction have also been investigated, including fertilisation (e.g. Pickett‐Heaps & West, 1998; Shim et al ., 2020) and haploid sex determination (Shim et al ., 2021). Finally, species within (or formerly attributed) to the Polysiphonia genus have been subjected to extensive electron microscopic studies in the past (Scott et al ., 1980; Delivopoulos & Kugrens, 1984) and are perhaps the most classic ‘textbook’ examples of red algae that are used to describe the ‘triphasic’ life cycle.…”