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. 2023 Sep 27;19(9):20230352. doi: 10.1098/rsbl.2023.0352

Mitochondrial uniparental inheritance achieved after fertilization challenges the nuclear–cytoplasmic conflict hypothesis for anisogamy evolution

Tatsuya Togashi 1,✉, Geoff A Parker 2, Yusuke Horinouchi 1,3
PMCID: PMC10523090  PMID: 37752851

Abstract

In eukaryotes, a fundamental phenomenon underlying sexual selection is the evolution of gamete size dimorphism between the sexes (anisogamy) from an ancestral gametic system with gametes of the same size in both mating types (isogamy). The nuclear–cytoplasmic conflict hypothesis has been one of the major theoretical hypotheses for the evolution of anisogamy. It proposes that anisogamy evolved as an adaptation for preventing nuclear–cytoplasmic conflict by minimizing male gamete size to inherit organelles uniparentally. In ulvophycean green algae, biparental inheritance of organelles is observed in isogamous species, as the hypothesis assumes. So we tested the hypothesis by examining whether cytoplasmic inheritance is biparental in Monostroma angicava, a slightly anisogamous ulvophycean that produces large male gametes. We tracked the fates of mitochondria in intraspecific crosses with PCR-RFLP markers. We confirmed that mitochondria are maternally inherited. However, paternal mitochondria enter the zygote, where their DNA can be detected for over 14 days. This indicates that uniparental inheritance is enforced by eliminating paternal mitochondrial DNA in the zygote, rather than by decreasing male gamete size to the minimum. Thus, uniparental cytoplasmic inheritance is achieved by an entirely different mechanism, and is unlikely to drive the evolution of anisogamy in ulvophyceans.

Keywords: anisogamy, isogamy, organelle inheritance, ulvophycean green algae

1. Introduction

Gamete size dimorphism between males and females (anisogamy) is the first step in the evolution of sexual dimorphism. It is generally believed that anisogamy originated from gametes of equal size between two mating types (isogamy) (e.g. [1–5]). In various organisms including animals and plants, anisogamy underlies sexual selection [1,6–10]. Its evolution is therefore a fundamental problem in evolutionary biology [5].

Uniparental inheritance of the DNA-containing organelles is claimed to avoid conflicts between organelles derived from different parents and spread of cytoplasmic parasites (e.g. bacteria and viruses) [11–13]. The nuclear–cytoplasmic conflict hypothesis is a major theoretical framework of the evolution of anisogamy [5]. It proposes that sperm have been minimized as an adaptation for preventing nuclear–cytoplasmic conflicts by constraining organelles to be inherited uniparentally [13]. This hypothesis predicts that organelles will be biparentally inherited if male gametes are large. However, empirical evidence for this hypothesis remains poor, and in particular, the hypothesis provides no obvious explanation for the persistence of slight anisogamy with large male gametes in multicellular organisms.

Ulvophycean marine green algae are important as models for testing the evolution of anisogamy. They exhibit a variety of gametic systems from isogamy to strong anisogamy: each species shows one gametic system and certain species are uniquely characterized by showing a first stage in the evolution of anisogamy, slight anisogamy [14]. In ulvophyceans, uniparental inheritance of organelles appears to be imperfect in isogamous species: mitochondrial and chloroplast genomes are inherited biparentally as well as uniparentally in some crosses [15,16]. In this study, we focus on a slightly anisogamous ulvophycean green alga, Monostroma angicava, that has a low anisogamy ratio (female gamete volume/male gamete volume [17]) (see [18] for more strongly anisogamous species). This alga has a dioecious heteromorphic haplo-diplontic life cycle with a haploid multicellular male or female gametophyte generation and a diploid unicellular sporophyte generation [17,19–23] (figure 1). Haploid gametes are produced mitotically by the haploid gametophytes. We test the hypothesis by examining cytoplasmic inheritance in M. angicava that produces male gametes of a large size [20] with useful mitochondria genetic markers developed in this study: if the hypothesis is supported, mitochondria might be biparentally inherited because its male gametes might be too large to suppress paternal mitochondrial passage to the zygote at fertilization.

Figure 1.

Figure 1.

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Haplo-diplontic sexual life cycle of M. angicava with haploid multicellular male or female gametophyte generation and diploid unicellular sporophyte generation. n: Haploid stage; 2n: diploid stage.

2. Material and methods

(a) . Collection of field materials and culture experiments

We collected 22 matured parental gametophytes of Monostroma angicava (11 males and 11 females) split into three groups (A, B and C) in the field at Botofurinai, Muroran, Hokkaido, Japan (42°31′N, 140°98′E) [24], and crossed their gametes produced from male and female parental gametophytes to obtain 23 genetically different offspring zygote strains in total (table 1). We cultured zygotes and fixed zygote samples from each strain with 1% glutaraldehyde at time intervals (from 0 h to 21 days after fertilization) for ZCA and ZEB zygote strains, and after 21 days and later for Z11, Z13, Z14, Z15, Z31, Z33, Z34, Z35, Z41, Z43, Z44, Z45, Z51, Z53, Z54, Z55, Z1 and Z2 zygote strains (electronic supplementary material, text S1 for general information on culture conditions). After they developed into sporophytes, some of the sporophytes were induced to produce zoospores through meiosis. The sex of offspring gametophytes was examined using sex-specific DNA markers (see [25] for details).

Table 1.

Offspring zygote strains obtained by crossing male (n = 11) and female (n = 11) parental gametophytes of M. angicava collected in the field. Groups A, B and C are indicated by blue, green and purple, respectively. aM–eM indicate the mitochondrial haplotypes (see table 2 for details).

♂1 (aM) ♂3 (bM) ♂4 (dM) ♂5 (aM) ♂Hb (bM) ♂Bd (bM) ♂A (aM) ♂C (bM) ♂D (aM) ♂E (bM) ♂F (aM)
♀1 (aM) Z11 Z31 Z41 Z51 — — — — — — —
♀3 (cM) Z13 Z33 Z43 Z53 — — — — — — —
♀4 (aM) Z14 Z34 Z44 Z54 — — — — — — —
♀5 (aM) Z15 Z35 Z45 Z55 — — — — — — —
♀Bb (aM) — — — — Z1 — — — — — —
♀Hb (cM) — — — — — Z2 — — — — —
♀A (aM) — — — — — — — ZCA — — —
♀B (aM) — — — — — — — — — ZEB —
♀C (eM) — — — — — — ZAC — — — —
♀D (aM) — — — — — — — — ZDD — —
♀E (aM) — — — — — — — — — — ZFE
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(b) . Detection of mitochondrial DNA polymorphisms

Genomes, including mitochondrial sequences obtained from PacBio next-generation sequencing (NGS) data of male (MA060316B-mg) and female (MA060316B-fd) M. angicava strains, were corrected using HiSeq X NGS data (see electronic supplementary material, text S2 for the general protocols for the NGS). Contigs that include the whole mitochondrial genome were identified using BioEdit [26]. To obtain the complete circular mitochondrial genome, we manually trimmed overlapping regions at both ends of these contigs. This genome was annotated by transferring annotation information from the Clamydomonas reinhardtii mitochondrial genome (NC_001638.1) using AGORA [27]. Mitochondrial DNA polymorphisms were identified by aligning the two sets (male and female) of mitochondrial DNA sequence data followed by manual single nucleotide polymorphism (SNP) detection.

(c) . Development of mitochondrial PCR-RFLP markers

To distinguish between male and female-derived mitochondria, we developed PCR-restriction fragment length polymorphism (RFLP) markers based on the above SNPs in mitochondrial genomes. To identify a restriction enzyme that recognizes only one allelic form of an SNP, we submitted five nucleotides around each SNP to Takara Cut-Site Navigator (https://www.takara-bio.co.jp/research/enzyme/enzyme_search.php). Then we submitted 100 nucleotides around the RFLP candidate site to Takara Cut-Site Navigator again to confirm that it has no other restriction-enzyme-recognizing sequences. We designed primers that amplify DNA regions containing an RFLP candidate site so that (i) each primer set produces a PCR product of ca 500–1000 bp, and (ii) both of the products digested by the corresponding restriction enzyme are longer than 100 bp, and then we tested the candidates of mitochondrial PCR-RFLP markers.

(d) . Analysing mitochondrial inheritance

We performed PCR-RFLP with the Phire Plant Direct PCR Kit (Thermo Fisher, Waltham, USA) for parental gametophytes, offspring zygotes, offspring sporophytes and offspring gametophytes. The reaction conditions were as follows: 5 min at 98°C followed by 40 cycles of 30 s at 98°C, 30 s at the relevant annealing temperature (electronic supplementary material, table S1), 1 min at 72°C, and a final incubation at 72°C for 5 min before storage at 4°C. After amplification, 4 µl of PCR product was incubated for 3 h in an incubator (5200-00; Anatech, Tokyo, Japan) and digested by the relevant enzyme (electronic supplementary material, table S1). Digestion products were separated and analysed on 1% agarose gels (Nippon gene, Tokyo, Japan). Given that the restriction fragment patterns of paternal and maternal mitochondria produced by the same RFLP marker are different, such markers enable analysis of the pattern of mitochondrial inheritance by comparing the band patterns of electrophoresed PCR products between parents and offspring. To confirm this pattern, we sequenced one to three mitochondrial RFLP sites of parental gametophytes and offspring sporophytes in group A.

3. Results

(a) . Mitochondrial PCR-RFLP markers

In the NGS data of the two Monostroma angicava strains, we identified 81 kbp mitochondrial genomes (GenBank accession numbers: OL856094 for MA060316B-mg and OL856095 for MA060316B-fd) (electronic supplementary material, figure S1) with 77 SNPs. In these SNPs, we found 20 RFLP candidate sites and obtained eight (M5, M8, M9, M10, M13, M15, M17 and M20) primer sets as the candidates of mitochondrial PCR-RFLP markers (electronic supplementary material, table S1). All eight PCR-RFLP markers were confirmed by PCR and restriction enzyme digestion (figure 2a, electronic supplementary material, figure S1).

Figure 2.

Figure 2.

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Tests of mitochondria PCR-RFLP markers, mitochondria PCR-RFLP band patterns of offspring zygotes/sporophytes/gametophytes and sex-specific molecular marker band patterns of offspring gametophytes. P: paternal RFLP band pattern. M: maternal RFLP band pattern. Bars on the left side indicate 500 bp. (a) Tests for the candidates of mitochondria PCR-RFLP markers. We designed each primer set to exhibit different band patterns between male (mg: MA060316B-mg) and female (fd: MA060316B-fd) strains. (b,c) Mitochondria DNA inheritance in offspring zygotes/sporophytes at early developmental stages with M8 marker. (b) The results from fertilization to the 21st day (ZCA strain). Paternal mitochondria DNA disappeared after the 21st day (highlighted by a dotted square). (c) The detailed results from fertilization to the 14th day (ZEB strain). Both paternal and maternal mitochondria DNAs persisted for at least 14 days. (d–f) Mitochondria PCR-RFLP and sex-specific molecular marker band patterns of offspring gametophytes. Offspring gametophytes were produced by a sporophyte of Z41 zygote strain. Numbers (1–10) indicate individual offspring gametophytes. (d) Mitochondria marker M5. (e) Male-specific marker. (f) Female-specific marker.

(b) . Haplotype of mitochondria in parental gametophytes

The band patterns of PCR-RFLP differed among parental gametophytes collected in the field (table 2). In this study, we mainly used M5, M8, M9, M10, M15 and M17 mitochondrial markers because we found no variation of the M13 SNP-allele in gametophytes examined in this study, and because the reaction temperature for product digestion of M20 with the restriction enzyme (Taq I) was very different from that for other mitochondrial markers (electronic supplementary material, table S1). We identified five haplotypes in mitochondria (aM–eM): the proportion of these haplotypes was aM : bM : cM : dM : eM = 13 : 5 : 2 : 1 : 1 (see also electronic supplementary material, text S3 and figure S2).

Table 2.

The PCR-RFLP patterns and the haplotypes of mitochondria in parental gametophytes of M. angicava. R: restricted; —: not restricted. ‘Restricted’ and ‘not restricted’ indicate that a PCR product was and was not specifically digested by the relevant restriction enzyme, respectively.

gametophyte mitochondria PCR-RFLP markers
M5 M8 M9 M10 M15 M17 haplotype
♂1 R R R R — — aM
♂3 — — — R R R bM
♂4 — R R R — R dM
♂5 R R R R — — aM
♂Hb — — — R R R bM
♂Bd — — — R R R bM
♂A R R R R — — aM
♂C — — — R R R bM
♂D R R R R — — aM
♂E — — — R R R bM
♂F R R R R — — aM
♀1 R R R R — — aM
♀3 — — — — R R cM
♀4 R R R R — — aM
♀5 R R R R — — aM
♀Bb R R R R - — aM
♀Hb — — — — R R cM
♀A R R R R — — aM
♀B R R R R — — aM
♀C — — — R — — eM
♀D R R R R — — aM
♀E R R R R — — aM
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(c) . Mitochondrial inheritance of offspring zygotes, offspring sporophytes and offspring gametophytes

The PCR-RFLP band patterns for offspring zygotes and offspring sporophytes using M8 mitochondrial marker and zygote strains (ZCA and ZEB) in group C are shown in figure 2b,c. Note that, in M. angicava, no cell divisions occur in zygotes and sporophytes, both of which are unicellular until zoosporogenesis starts in matured sporophytes ([23], see also electronic supplementary material, figure S3). Only maternal mitochondrial DNA was detected 21 days after fertilization (figure 2b), though both paternal and maternal mitochondrial DNAs remained at 14 days after fertilization (figure 2c). These results were also confirmed with mitochondrial markers (M5, M8, M9, M10, M15 and M17) and all 12 zygote strains that could be used in our analysis (Z13, Z31, Z33, Z34, Z35, Z41, Z43, Z44, Z45, Z53, Z1 and Z2) in groups A and B (electronic supplementary material, table S2). Maternal inheritance of mitochondria was also observed in male and female offspring gametophytes produced by a single offspring sporophyte through meiosis (two sporophytes of Z41 zygote strain with 10 gametophytes examined in each sporophyte; one sporophyte of Z31 zygote strain with 11 gametophytes) (see figure 2d–f). This explains how some of the male and female gametophytes have the same mitochondria haplotype (table 2). In all 10 zygote strains that could be used in our analysis (Z13, Z31, Z33, Z34, Z35, Z41, Z43, Z44, Z45 and Z53) in group A, it was confirmed that the nucleotide at SNP positions of mitochondria in offspring sporophytes was the same as that of the maternal mitochondria in the parental gametophytes (electronic supplementary material, table S3, n = 47).

4. Discussion

Genetic markers are useful tools to track the fate of organelles. However, in most green algae including ulvophyceans, cytoplasmic inheritance has never been studied with such genetic methods [28]. This is mainly because little information on organelle DNA sequence differences between the sexes is available in most species. Instead, many previous studies are based on cytological observations using light, fluorescence and electron microscopy [29–32]. However, cytological data are usually not as strong as genetic data [32]. Our genetic method is free from the problems encountered with most cytological methods.

Mitochondrial inheritance in this slightly anisogamous species helps us understand whether uniparental inheritance is enforced by eliminating paternal mitochondrial DNA in the zygote or by minimizing male gamete size, preventing the transmission of male mitochondria at fertilization, as the nuclear–cytoplasmic conflict hypothesis predicts. We have demonstrated that mitochondria are maternally inherited in M. angicava: grown offspring sporophytes and offspring gametophytes contain only maternal mitochondria, however, zygotes soon after fertilization also contain paternal mitochondria for many days after fusion (figure 2b–d). The process of paternal mitochondria elimination occurs long after fertilization, not through reduced male gamete size. Uniparental inheritance therefore appears to have evolved independently of the evolution of anisogamy, contrary to the nuclear–cytoplasmic conflict hypothesis (note that no conflict between male mitochondria and maternal nuclear genomes may exist).

Several other phenomena that are inconsistent with the nuclear–cytoplasmic conflict hypothesis have been observed at both ends of the evolutionary transition from isogamy to anisogamy in some other biological groups, e.g. uniparental mitochondrial inheritance in an isogamous chlorophycean freshwater green alga, Chlamydomonas reinhardtii (note that mitochondria and chloroplasts are inherited from a different mating type) [33]), and biparental inheritance of mitochondria through doubly uniparental inheritance (DUI) in oogamous bivalves in which two mitochondrial genomes are inherited, one through eggs, the other through sperm [e.g. 34]. By contrast, in ulvophycean marine green algae, the evolution of anisogamy seems to be accompanied by a transition to uniparental organelle inheritance even at a first stage of the evolution of anisogamy. While gamete size might well be related to organelle inheritance pattern (e.g. the smaller size of male gametes in M. angicava may possibly result in their containing fewer mitochondria than female gametes), we however suggest that uniparental inheritance is enforced later, by a mechanism (i.e. eliminating paternal mitochondrial DNA in the zygote) that is quite different from that assumed by the nuclear–cytoplasmic conflict hypothesis (i.e. decreasing male gamete size to a minimum). Although the nuclear–cytoplasmic conflict hypothesis is not completely ruled out, cytoplasmic inheritance is unlikely to drive the evolution of anisogamy in ulvophyceans.

Acknowledgements

We are most grateful to the reviewers and editor whose comments have greatly improved this paper. We also thank K. Yoshida for his technical assistance, and the staff of the Muroran Marine Station of the Field Science Center for Northern Biosphere, Hokkaido University, for their support.

Ethics

This work did not require ethical approval from a human subject or animal welfare committee.

Data accessibility

The data are provided in the electronic supplementary material [35].

Declaration of AI use

We have not used AI-assisted technologies in creating this article.

Authors' contributions

T.T.: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, software, supervision, validation, visualization, writing—original draft, writing—review and editing; G.A.P.: project administration, supervision, writing—review and editing; Y.H.: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, software, supervision, validation, visualization, writing—original draft, writing—review and editing.

All authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration

We declare we have no competing interests.

Funding

This work was supported by grants-in-aid from the Japan Society for the Promotion of Science (grant nos 16H04839, 22K20644 and 23K14260) and Fujiwara Natural History Public Interest Incorporated Foundation.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. Togashi T, Parker GA, Horinouchi Y. 2023. Mitochondrial uniparental inheritance achieved after fertilization challenges the nuclear–cytoplasmic conflict hypothesis for anisogamy evolution. Figshare. ( 10.6084/m9.figshare.c.6837178) [DOI] [PMC free article] [PubMed]

Data Availability Statement

The data are provided in the electronic supplementary material [35].

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