SEXUALITY AND UNIPARENTAL INHERITANCE OF CHLOROPLAST DNA IN THE ISOGAMOUS GREEN ALGA ULVA COMPRESSA (ULVOPHYCEAE)¹

Abstract

Ulva compressa L. is a heterothallic macroalga considered to be in the early evolutionary stage between isogamy and anisogamy. Two genetic lines of this species, each consisting of gametophytes with opposite mating types, were collected on the coasts of Ehime and Iwate prefectures: MGEC-1 (mt(+) ) and MGEC-2 (mt(-) ) from Ehime, and MGEC-5 (mt(+) ) and MGEC-6 (mt(-) ) from Iwate. Their relative gamete sizes (i.e., cell volumes) do not correspond to their mating types: MGEC-6 (19.8 μm(3) ) > MGEC-1 (18.6 μm(3) ) > MGEC-5 (17.0 μm(3) ) > MGEC-2 (10.1 μm(3) ). The pattern of organelle inheritance is an important sexual characteristic in many eukaryotes. We therefore investigated the relationship between gamete size and the inheritance of chloroplast DNA (cpDNA). Polymorphisms between the cpDNA of the two lines were used as markers. We found a 24 bp insertion between psbF and psbL, and the substitution of a StyI site (from CCAAGG to TCAAGG) in the intergenic region between petD and accD. Two interline crosses (MGEC-1 × MGEC-6 and MGEC-2 × MGEC-5) produced 42 and 38 zygotes, respectively. PCR and PCR-RFLP analyses showed that the cpDNA of the mt(+) gametes was consistently inherited in both crosses. The cpDNA is inherited from one parent only, and it depends not on gamete size but on being mt(+) . The cpDNA was observed during crossing and in the zygotes 6 h after mating. In 6% of the zygotes, the cpDNA derived from the mt(-) gametes disappeared 3-4 h after mating. Preferential digestion of the cpDNA in the zygote's mt(-) gamete may form the basis for uniparental inheritance of cpDNA.

Origins of Eukaryotic Sexual Reproduction

“…Although there is as yet no information on the molecules that exert mating-type UP control in most systems, the selective destruction of one set of organelle genomes has been shown in several disparate radiations, including the chlorophytes Gonium (Setohigashi et al 2011) and Bryopsis (Kuroiwa and Hori 1986), the ulvophyte Ulva (Kagami et al 2008), brown algae (Motomura et al 2010), the slime mold Physarum (Moriyama and Kawano 2010), Drosophila (DeLuca and O'Farrell 2012), the fish Orizias (Nishimura et al 2006), and the mouse (Kaneda et al 1995;Kuroiwa 2010;Sato and Sato 2013). Notably, in the vertebrate examples, the sperm organelles enter the egg but are quickly and selectively eliminated in the zygote in a species-specific fashion (Kaneda et al 1995).…”

HAP2/GCS1 Is Involved in the Sexual Reproduction System of the Marine Macroalga Ulva compressa (Ulvales, Chlorophyta)

“…A pair of mt and mt + cultures of U. compressa (MGEC-2 and MGEC-1, respectively) was collected from the Konokawa Coast, Iyo, Ehime, Japan (33 42′N, 132 39′E) (Kagami et al 2005, Kagami et al 2008a, Kagami et al 2008b, Mogi et al 2008. The strains are maintained in the culture collection of Nagasaki University (Nagasaki, Japan).…”

“…Its thallus-shaped gametophytes produce gametes moving with two flagella; the gametophyte morphologies of the two mating types are indistinguishable (Tatewaki 1994, Kagami et al 2005. However, the cell sizes of the mt + and mt gametes in U. compressa are not uniform, suggesting that this species is situated at an intermediate evolutionary stage regarding sexual differentiation of gametes from isogamy to anisogamy (Kagami et al 2008b). Interestingly, a potential mating structure of the mt + gamete in U. compressa is located on the same cellular side as the eyespot, whereas that of the mt gamete is on the side opposite the eyespot, suggesting an asymmetry of mating structures between mt and mt + gametes (Mogi et al 2008).…”

<i>Ulva partita</i> sp. nov., a Novel <i>Enteromorpha</i>-Like <i>Ulva</i> Species from Japanese Coastal Areas

“…In this study, we describe one Enteromorpha-like Ulva species collected from the seashore in Japan, which was previously identified as U. compressa L. based on morphological features (Kagami et al 2005, 2008a, 2008b, Mogi et al 2008). Previous reports have described the genome size (Kagami et al 2005), uncovered the maternal inheritance of chloroplasts using cpDNA markers (Kagami et al 2008b), investigated differences in mating structures between female and male gametes using FE-SEM (Mogi et al 2008), and developed the method of inducing gamete formation (Kuwano et al 2012) in this species.…”

“…Previous reports have described the genome size (Kagami et al 2005), uncovered the maternal inheritance of chloroplasts using cpDNA markers (Kagami et al 2008b), investigated differences in mating structures between female and male gametes using FE-SEM (Mogi et al 2008), and developed the method of inducing gamete formation (Kuwano et al 2012) in this species. Additionally matured thalli can be cryopreserved in liquid nitrogen, and gametes and thalli can be easily prepared (Kuwano et al 2012).…”