doi: 10.1038/s42003-023-04949-1.
Reorganization of the ancestral sex-determining regions during the evolution of trioecy in Pleodorina starrii
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- PMID: 37296191
- PMCID: PMC10256686
- DOI: 10.1038/s42003-023-04949-1
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Reorganization of the ancestral sex-determining regions during the evolution of trioecy in Pleodorina starrii
Kohei Takahashi et al.
Commun Biol.
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Abstract
The coexistence of three sexual phenotypes (male, female and bisexual) in a single species, 'trioecy', is rarely found in diploid organisms such as flowering plants and invertebrates. However, trioecy in haploid organisms has only recently been reported in a green algal species, Pleodorina starrii. Here, we generated whole-genome data of the three sex phenotypes of P. starrii to reveal a reorganization of the ancestral sex-determining regions (SDRs) in the sex chromosomes: the male and bisexual phenotypes had the same "male SDR" with paralogous gene expansions of the male-determining gene MID, whereas the female phenotype had a "female SDR" with transposition of the female-specific gene FUS1 to autosomal regions. Although the male and bisexual sex phenotypes had the identical male SDR and harbored autosomal FUS1, MID and FUS1 expression during sexual reproduction differed between them. Thus, the coexistence of three sex phenotypes in P. starrii is possible.
© 2023. The Author(s).
Conflict of interest statement
The authors declare no competing interests.
Figures
Note that the unisexual male phenotype has a putative male sex-determining region (SDR, blue) in the V sex chromosome and lacks the bisexual factor (BF) in autosomes. The bisexual phenotype has a putative male SDR, but also has a BF in autosomes. The unisexual female phenotype has a putative female SDR (pink) in the U sex chromosome and harbors or lacks BF. Yellow and gray rectangles represent sex chromosomes and autosomes, respectively. sp sperm packet (bundle of male gametes), mg male gamete, fg female gamete. All scale bars = 50 μm.
a Comparison of SDRs and adjacent regions of three sex phenotypes. Light blue and pink regions represent male and female SDRs, respectively. Genes with dark blue and red background represent male- and female-specific genes, respectively. Yellow regions represent pseudo-autosomal regions. Gray shading indicates a syntenic bloc. b Phylogeny of homologs of MID in the volvocine lineage, inferred based on 142 deduced amino acid sequences by the maximum likelihood (ML) method using the JTT + G model. Blue represents male- or mating type minus-specific genes. Black represents homologs of homothallic species. All positions containing gaps and missing data were eliminated from the alignment. Branch lengths are proportional to the evolutionary distances indicated by the scale bar. Numbers at left and right above branches indicate bootstrap values (BV) of the ML (≥50%) and posterior probabilities (PP) of Bayesian inference (≥0.90), respectively. Asterisks at the branches indicate 100% BV and 1.00 PP according to the two methods. c Comparison of autosomal regions harboring FUS1 homologs of three sex phenotypes. Gray shading indicates a syntenic bloc. d Phylogeny of homologs of FUS1 in the volvocine lineage, inferred based on 501 amino acid sequences deduced by ML using the LG + G + I model. Pink represents mating type plus-specific or female-specific genes within a SDR or possible SDR. Purple indicates autosomal genes harbored in all sex phenotypes of each species. For the others, see (b). e Phylogeny of homologs of MTD1 in the volvocine lineage, inferred based on 495 amino acid sequences deduced by the ML method using the JTT + G model. Purple indicates autosomal genes harbored in all sex phenotypes of each species. For the others, see (b).
a Diagram of the GCS1/HAP2 cluster localized within a 100 kbp autosomal region of three sex phenotypes (Supplementary Fig. 13). b Exon-intron structures of the seven paralogs from unisexual male. Filled and open boxes represent exon sequences and non-coding (UTR) sequences, respectively. Lines between boxes indicate intron sequences. The number above the box indicates the homologous exon in GCS1_1. Numbers below boxes and lines indicate the numbers of nucleotides. Light blue regions represent the HAP2-GCS1 domain coding sequences. The positions of GCS1_1 specific primers (Supplementary Table 10) used for reverse transcription quantitative PCR (RT-qPCR) analysis (Fig. 4) are also indicated. c Phylogeny of seven paralogs of P. starrii in the volvocine lineage, inferred from amino acid sequences of GCS1 (698 amino acids, see Supplementary Fig. 15) deduced by the maximum likelihood (ML) method using the WAG + G + I model. All aligned positions were used for ML analysis (MEGAX option, Gaps/Missing Data Treatment: Use all sites). Branch lengths are proportional to the evolutionary distances indicated by the scale bar. Numbers at left and right above branches indicate bootstrap values (BV) of the ML (≥50%) and posterior probabilities (PP) of Bayesian inference (≥0.90), respectively. Asterisks at the branches indicate 100% BV and 1.00 PP according to the two methods.
Normalized expression of four sex-related genes in P. starrii asexual and sexual colonies relative to the expression of the unisexual male sexual colony (male colony) for MID, MTD1, and GCS1_1 and unisexual female sexual colony (female colony) for FUS1. Bars show standard error of the mean (SEM). *, no expression detected; –, not sexually induced; +, sexually induced; a, asexual colony; m, male colony; f, female colony. For the original numerical data, see Supplementary Data 2.
Comment in
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Sex chromosomes: How to make a hermaphrodite.Ekwealor JTB, Roy SW. Ekwealor JTB, et al. Curr Biol. 2023 Nov 6;33(21):R1150-R1152. doi: 10.1016/j.cub.2023年09月03日8. Curr Biol. 2023. PMID: 37935128
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