Light and Electron Microscopic Observations of Preferential Destruction of Chloroplast and Mitochondrial Dna at Early Male Gametogenesis of the Anisogamous Green Alga Derbesia Tenuissima (Chlorophyta)1

Abstract

Gametogenesis in male and female gametophytes was studied by light microscopy and EM in the dioecious multinucleate green alga Derbesia tenuissima (Moris & De Notaris) P. Crouan & H. Crouan, where male and female gametes differ in size. Gametogenesis was divided into five stages: 32 h (stage 1), 24 h (stage 2), 16 h (stage 3), 8 h (stage 4), and 0.5 h (stage 5) before gamete release. At stage 1, the first sign of gametogenesis observed was the aggregation of gametophyte protoplasm to form putative gametangia. At stage 2, gametangia were separated from the vegetative protoplasm of gametophytes. Morphological changes of nuclei and organelles occurred at this early stage of male gametogenesis, and organelle DNA degenerated. At stage 3, male organelle DNA had completely degenerated, whereas in female gametangia, organelle DNA continued to exist in both chloroplasts and mitochondria. Gametogenesis was almost completed at stage 4 and fully at stage 5. Small male gametes had a DNA-containing nucleus and a large mitochondrion and one or several degenerated chloroplasts. The mitochondria and plastids were devoid of DNA. The large female gametes had a nucleus and multiple organelles, all of which contained their own DNA. Thus, degeneration of chloroplast DNA along with morphological changes of organelles occurred at male gametogenesis in anisogamous green algae ( Bryopsis and D. tenuissima ), in contrast with previous studies in isogamous green algae ( Chlamydomonas , Acetabularia caliculus , and Dictyosphaeria cavernosa ) in which degeneration of chloroplast DNA occurred after zygote formation.

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

“…However, in anisogamous green algae, such as Bryopsis (Kuroiwa and Hori 1986, Ogawa 1988, Kuroiwa et al. 1991) and Derbesia tenuissima (Lee et al. 2002), and in the oogamous alga Chara corallina (Sun et al.…”

Cytoplasmic inheritance in green algae: patterns, mechanisms and relation to sex type

“…The first mechanism is mainly deduced from the data using fluorescence microscopy with DAPI staining, so that it is difficult to deny the possibility that the dispersal of DNA molecules, presumably caused by the digestion or relaxation of the proteins that form the nucleoids, engenders the disappearance of DNA fluorescence. However, the accuracy of the data has been confirmed in C. reinhardtii (Nishimura et al 1999), Volvox carteri (Adams et al 1990), B. maxima , and D. tenuissima (Lee et al 2002) using molecular or biochemical methods or immunoelectron microscopy. Consequently, the disappearance of DNA fluorescence is suggested to be a result of the digestion of DNA molecules by nuclease.…”

“…In contrast, the preferential disappearance of organelle DNA occurs during male gametogenesis in anisogamous species belonging to Bryopsidales, such as the siphonous green algae, Bryopsis maxima (Kuroiwa and Hori 1986;Kuroiwa et al 1991), B. plumosa (Ogawa 1988), Derbesia tenuissima (Lee et al 2002), and Caulerpa (Miyamura and Hori 1997;Miyamura and Nagumo 2007). Kuroiwa et al (1991) studied details of this process in B. maxima, and showed that the size of the chloroplast and the number of nucleoids per chloroplast in male and female gametangia decreased markedly during gametogenesis as a result of continuous chloroplast division; then the chloroplast DNA disappeared in the male gametangia.…”

“…Ulva compressa cross 2 f Kuroiwa and Hori (1986); 9, Kuroiwa and Hori (1990); 10, Kuroiwa et al (1991); 11, Lee et al (2002); 12, Sun et al (1988) the oogamous colonial green alga Volvox carteri f. nagariensis, RFLP analysis of the progenies of crosses between two geographically distant strains indicates that both plastid and mitochondrial genomes are transmitted maternally to the progeny (Adams et al 1990). Coleman and Maguire (1982) and Kuroiwa et al (1993a) investigated the fate of plastid DNA during spermatogenesis and fertilization of V. carteri using fluorescence microscopy with DAPI (4 0 ,6-diamidino-2-phenylindole) staining.…”

“…Sexual reproduction is known to occur in Ulvophyceae, Trebouxiophyceae, Chlorophyceae (UTC clade), and Sager (1954); 2, Cavalier- Smith (1970); 3, Kuroiwa et al (1982); 4, Lee et al (1990); 5, Coleman and Maguire (1983);6, Hamaji et al (2008);7, Stein (1958); 8, Adams et al (1990); 9, Coleman and Maguire (1982); 10, Kuroiwa et al (1993a); 11, Kuroiwa et al (1993b); 12, Kuroiwa et al (1985); 13, Kagami et al (2008); 14, Kawano (2008); 15, Mogi et al (2009);16, Bråten(1971);17, Fjeld (1971); 18, Bråten (1973); 19, Kuroiwa and Hori (1986); 20, Kuroiwa and Hori (1990); 21, Kuroiwa et al (1991);22, Ogawa (1988); 23, Lee et al (2002); 24, Miyamura and Nagumo (2007); 25, …”