Skip to main content
SpringerLink
Log in

Cytoplasmic inheritance of mitochondria and chloroplasts in the anisogamous brown alga Mutimo cylindricus (Phaeophyceae)

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Based on the morphology of gametes, sexual reproduction in brown algae is usually classified into three types: isogamy, anisogamy, and oogamy. In isogamy, chloroplasts and chloroplast DNA (chlDNA) in the sporophyte cells are inherited biparentally, while mitochondria (or mitochondrial DNA, mtDNA) is inherited maternally. In oogamy, chloroplasts and mitochondria are inherited maternally. However, the patterns of mitochondrial and chloroplast inheritance in anisogamy have not been clarified. Here, we examined derivation of mtDNA and chlDNA in the zygotes through strain-specific PCR analysis using primers based on single nucleotide polymorphism in the anisogamous brown alga Mutimo cylindricus. In 20-day-old sporophytes after fertilization, mtDNA and chlDNA derived from female gametes were detected, thus confirming the maternal inheritance of both organelles. Additionally, the behavior of mitochondria and chloroplasts in the zygotes was analyzed by examining the consecutive serial sections using transmission electron microscopy. Male mitochondria were isolated or compartmentalized by a double-membrane and then completely digested into a multivesicular structure 2 h after fertilization. Meanwhile, male chloroplasts with eyespots were observed even in 4-day-old, seven-celled sporophytes. The final fate of male chloroplasts could not be traced. Organelle DNA copy number was also examined in female and male gametes. The DNA copy number per chloroplast and mitochondria in male gametes was lower compared with female organelles. The degree of difference is bigger in mtDNA. Thus, changes in different morphology and DNA amount indicate that maternal inheritance of mitochondria and chloroplasts in this species may be based on different processes and timing after fertilization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adams CR, Stamer KA, Miller JK, McNally JG, Kirk MM, Kirk DL (1990) Patterns of organellar and nuclear inheritance among progeny of two geographically isolated strains of Volvox carteri. Curr Genet 18:141–153

    CAS  PubMed  Google Scholar 

  • Al-Rawi S, Louvet-Vallée S, Djeddi A, Sachse M, Culetto E, Hajjar C et al (2011) Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 334:1144–1147

    CAS  PubMed  Google Scholar 

  • Aoyama H, Hagiwara Y, Misumi O, Kuroiwa T, Nakamura S (2006) Complete elimination of maternal mitochondrial DNA during meiosis resulting in the paternal inheritance of the mitochondrial genome in Chlamydomonas species. Protoplasma 228:231–242

    CAS  PubMed  Google Scholar 

  • Baur E (1909) Das Wesen und die Erblichkeitsverhältnisse der ‘arietates albomarginatae hort’ von Pelargonium zonale. Z Indukt Abstammungs-Vererbungsl 1:330–351

    Google Scholar 

  • Boynton JE, Harris EH, Burkhart BD, Lamerson PM, Gillham NW (1987) Transmission of mitochondrial and chloroplast genomes in crosses of Chlamydomonas. Proc Natl Acad Sci U S A 84:2391–2395

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cavalier-Smith T (1970) Electron microscopic evidence for chloroplast fusion in zygotes of Chlamydomonos reinhardii. Nature 228:333–335

    CAS  PubMed  Google Scholar 

  • Choi SJ, Park EJ, Endo H, Kitade Y, Saga N (2008) Inheritance pattern of chloroplast and mitochondrial genomes in artificial hybrids of Porphyra yezoensis (Rhodophyta). Fish Sci 74:822–829

    CAS  Google Scholar 

  • Correns C (1909) Vererbungsversuche mit blass (gelb) grünen und buntblättrigen Sippen bei Mirabilis jalap, Urtica pilulifera und Lumaria annua. Z Indukt Abstammungs-Vererbungsl 1:291–329

    Google Scholar 

  • Coyer JA, Peters AF, Hoarau G, Stam WT, Olsen JL (2002) Inheritance patterns of ITS1, chloroplasts and mitochondria in artificial hybrids of the seaweeds Fucus serratus and F. evanescens (Phaeophyceae). Eur J Phycol 37:173–178

    Google Scholar 

  • Gomes LC, Scorrano L (2013) Mitochondrial morphology in mitophagy and macroautophagy. BBA Mol Cell Res 1833:205–212

    CAS  Google Scholar 

  • Graham LE, Wilcox LW (2000) Algae. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Green DR, Levine B (2014) To be or not to be? How selective autophagy and cell death govern cell fate. Cell 157:65–75

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi K, Hashimoto N, Daigen M, Ashikawa I (2004) Development of PCR-based SNP markers for rice blast resistance genes at the Piz locus. Theor Appl Genet 108:1212–1220

    CAS  PubMed  Google Scholar 

  • Henry EC, Cole KM (1982) Ultrastructure of swarmers in the Laminariales (Phaeophyceae) II Sperm. J Phycol 18:570–579

    Google Scholar 

  • Hommersand MH, Fredericq S (1990) Sexual reproduction and cystocarp development. In: Cole KM, Sheath RG (eds) Biology of the red algae. Cambridge University Press, New York, pp 305–345

    Google Scholar 

  • Kajikawa M, Yamauchi M, Shinkawa H, Tanaka M, Hatano K, Nishimura Y, Kato M, Fukuzawa H (2019) Isolation and characterization of Chlamydomonas autophagy-related mutants in nutrient-deficient conditions. Plant Cell Physiol 60:126–138

    CAS  PubMed  Google Scholar 

  • Kato Y, Kogame K, Nagasato C, Motomura T (2006) Inheritance of mitochondrial and chloroplast genomes in the isogamous brown alga Scytosiphon lomentaria (Phaeophyceae). Phycol Res 54:65–71

    CAS  Google Scholar 

  • Kawai H, Kogishi K, Hanyuda T, Kitayama T (2012) Taxonomic revision of the genus Cutleria proposing a new genus Mutimo to accommodate M. cylindricus (Cutleriaceae, Phaeophyceae). Phycol Res 60:241–248

    Google Scholar 

  • Kimura K, Nagasato C, Kogame K, Motomura T (2010a) Disappearance of male mitochondrial DNA after the four-cell stage in sporophytes in sporophytes of the isogamous brown alga Scytosiphon Lomentaria (Scytosiphonaceae, Phaeophyceae). J Phycol 46:143–152

    CAS  Google Scholar 

  • Kimura K, Nagasato C, Uwai S, Motomura T (2010b) Sperm mitochondrial DNA elimination in the zygote of the oogamous brown alga Undaria pinnatifida (Laminariales, Phaeophyceae). Cytologia 75:353–361

    CAS  Google Scholar 

  • Kitayama T, Kawai H, Yoshida T (1992) Dominance of female gametophytes in field populations of Cutleria cylindrica (Cutleriales, Phaeophyceae) in the Tsugaru Strait, Japan. Phycologia 31:449–461

    Google Scholar 

  • Kraan S, Guiry MD (2000) Molecular and morphological character inheritance in hybrids of Alaria esculenta and A. praelonga (Alariaceae, Phaeophyceae). Phycologia 39:554–559

    Google Scholar 

  • Kuroiwa T (2010) 100 years since the discovery of non-Mendelian plastid phenotypes. J Plant Res 123:125–129

    PubMed  Google Scholar 

  • Kuroiwa T, Hori T (1986) Preferential digestion of male chloroplast nuclei and mitochondrial nuclei during gametogenesis of Bryopsis maxima Okamura. Protoplasma 133:85–87

    Google Scholar 

  • Kuroiwa T, Kawano S, Watanabe M, Hori T (1991) Preferential digestion of chloroplast DNA in male gametangia during the late stage of gametogenesis in the anisogamous alga Bryopsis maxima. Protoplasma 163:102–113

    CAS  Google Scholar 

  • Lee SH, Motomura T, Ichimura T (2002) 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). J Phycol 38:534–542

    Google Scholar 

  • Luo SM, Ge ZJ, Wang ZW, Jiang ZZ, Wang ZB, Ouyang YC, Hou Y, Schatten H, Sun QY (2013) Unique insights into maternal mitochondrial inheritance in mice. Proc Natl Acad Sci U S A 110:13038–13043

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luo SM, Sun QY (2013) Autophagy is not involved in the degradation of sperm mitochondria after fertilization in mice. Autophagy 9:2156–2157

    CAS  PubMed  Google Scholar 

  • Miyamura S (2010) Cytoplasmic inheritance in green algae: patterns, mechanisms and relation to sex type. J Plant Res 123:171–184

    PubMed  Google Scholar 

  • Motomura T (1990) Ultrastructure of fertilization in Laminaria angustata (Phaeophyta, Laminariales) with emphasis on the behavior of centrioles, mitochondria and chloroplasts of the sperm. J Phycol 26:80–89

    Google Scholar 

  • Motomura T, Nagasato C, Kimura K (2010) Cytoplasmic inheritance of organelles in brown algae. J Plant Res 123:185–192

    PubMed  Google Scholar 

  • Nagasato C, Motomura T (2002) Ultrastructural study on mitosis and cytokinesis in Scytosiphon lomentaria zygotes (Scytosiphonales, Phaeophyceae) by freeze-substitution. Protoplasma 219:140–149

    CAS  PubMed  Google Scholar 

  • Nagasato C, Motomura T, Ichimura T (1998) Selective disappearance of maternal centrioles after fertilization in the anisogamous brown alga Cutleria cylindrica (Cutleriales, Phaeophyceae): paternal inheritance of centrioles is universal in the brown algae. Phychol Res 46:191–198

    Google Scholar 

  • Nagasato C, Motomura T, Ichimura T (2000) Spindle formation in karyogamy-blocked zygotes of the isogamous brown alga Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). Eur J Phycol 35:339–347

    Google Scholar 

  • Nishimura Y, Misumi O, Kato K, Inada N, Higashiyama T, Momoyama Y, Kuroiwa T (2002) An mt+ gamete-specific nuclease that targets mt− chloroplasts during sexual reproduction in C. reinhardtii. Genes Dev 16:1116–1128

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura Y, Shikanai T, Kawamoto S, Toh-e A (2020) Step-wise elimination of α-mitochondrial nucleoids and mitochondrial structure as a basis for the strict uniparental inheritance in Cryptococcus neoformans. Sci Rep 10:1–11

    Google Scholar 

  • Nishimura Y, Yoshinari T, Naruse K, Yamada T, Sumi K, Mitani H, Higashiyama T, Kuroiwa T (2006) Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc Natl Acad Sci U S A 103:1382–1387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peters AF, Scornet D, Müller DG, Kloareg B, Cock JM (2004) Inheritance of organelles in artificial hybrids of the isogamous multicellular chromist alga Ectocarpus siliculosus (Phaeophyceae). Eur J Phycol 39:235–242

    Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Culture and collections of algae (Proc jap Conf Hakone, 1966). Japanese Society of Plant Physiology, Tokyo, pp 63–75

    Google Scholar 

  • Redmann M, Dodson M, Boyer-Guittaut M, Darley-Usmar V, Zhang J (2014) Mitophagy mechanisms and role in human diseases. Int J Biochem Cell Biol 53:127–133

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sager R, Lane D (1972) Molecular basis of maternal inheritance. Proc Natl Acad Sci 69:2410–2413

    CAS  PubMed  Google Scholar 

  • Sato M, Sato K (2011) Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 334:1141–1144

    CAS  PubMed  Google Scholar 

  • Sun GH, Uyeda TQ, Kuroiwa T (1988) Destruction of organelle nuclei during spermatogenesis in Chara corallina examined by staining with DAPI and anti-DNA antibody. Protoplasma 144:185–188

    Google Scholar 

  • Uwai S, Kogame K, Masuda M (2001) A taxonomic study of the Elachista taeniaeformis complex and E. vellosa from the western Pacific (Elachistaceae, Phaeophyceae). Phycologia 40:67–77

    Google Scholar 

  • Wagner-Vogel G, Lämmer F, Kämper J, Basse CW (2015) Uniparental mitochondrial DNA inheritance is not affected in Ustilago maydis Δatg11 mutants blocked in mitophagy. BMC Microbiol 15:23

    PubMed  PubMed Central  Google Scholar 

  • Whelan JA, Russell NB, Whelan MA (2003) A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 278:261–269

    CAS  PubMed  Google Scholar 

  • Wynne MJ, Loiseaux S (1976) Recent advances in life history studies of the Phaeophyta. Phycologia 15:435–452

    Google Scholar 

  • Xin Z, Velten JP, Oliver MJ, Burke JJ (2003) High-throughput DNA extraction method suitable for PCR. Biotechniques 34:820–826

    CAS  PubMed  Google Scholar 

  • Yoon HS, Hackett JD, Bhattacharya D (2002) A single origin of the peridinin-and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci 99:11724–11729

    CAS  PubMed  Google Scholar 

  • Zhang Q, Sodmergen (2010) Why does biparental plastid inheritance revive in angiosperms? J Plant Res 123:201–206

    PubMed  Google Scholar 

  • Zhuang X, Jiang L (2019) Chloroplast degradation: multiple routes into the vacuole. Front Plant Sci 10:359

    PubMed  PubMed Central  Google Scholar 

  • Zuccarello GC, Burger G, West JA, King RJ (1999a) A mitochondrial marker for red algal intraspecific relationships. Mol Ecol 8:1443–1447

    CAS  PubMed  Google Scholar 

  • Zuccarello GC, West JA, Kamiya M, King RJ (1999b) A rapid method to score plastid haplotypes in red seaweeds and its use in determining parental inheritance of plastids in the red alga Bostrychia (Ceramiales). Hydrobiogia 401:207–214

    CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. Shigeo Kawaguchi, Faculty of Agriculture, Kyushu University for providing the material, Fukuoka-strain of M. cylindricus.

Funding

This work was supported by the Sumitomo Foundation (grant number 190311).

Author information

Authors and Affiliations

  1. Graduate School of Environmental Science, Hokkaido University, Sapporo, 060-0810, Japan

    Yuan Shen

  2. Toba Fisheries Science Center, Toba, 517-0005, Japan

    Toyoki Iwao

  3. Muroran Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Muroran, 051-0013, Japan

    Taizo Motomura & Chikako Nagasato

Authors
  1. Yuan Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Toyoki Iwao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Taizo Motomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chikako Nagasato
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yuan Shen and Chikako Nagasato designed the experiment and maintained the strains of M. cylindricus. Toyoki Iwao collected the fresh samples in the field. Taizo Motomura analyzed the data and critically reviewed this manuscript. All authors wrote and edited this manuscript.

Corresponding author

Correspondence to Chikako Nagasato.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Handling Editor: Tsuneyoshi Kuroiwa

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 41 kb)

Fig S1

Gametes and development of a zygote in Mie-strain. a Female gamete. b Male gamete. c-g Development of a single zygote. c Six-hour-old zygote, where two eyespots (arrowheads) can be detected in the zygote. d Two-day-old sporophyte, two eyespots (arrowheads) exist in each daughter cell. e Four-day-old sporophyte, two eyespots (arrowheads) can still be detected. f Eight-day-old sporophyte, only one eyespot (arrowhead) is observed. g 20-day-old crustose sporophyte. AF, anterior flagellum; PF, posterior flagellum. Scale bars: 10 μm (a-f); 20 μm (g). (PNG 215 kb)

High Resolution Image (TIF 1738 kb)

Fig S2

Ultrastructure of mitochondria and chloroplasts in female and male gametes a A female gamete. b A male gamete. c The enlarged view of mitochondrion (m1 in a). d The enlarged view of mitochondrion (m2 in b). The black linear material (arrowhead) is found in tubular cristae of mitochondrion in c and d. e The enlarged view of a chloroplast (c1 in a) with an eyespot (es). f The enlarged view of a chloroplast (c2 in b) with an eyespot (es). Arrow and arrowhead in chloroplast of e and f indicate the girdle lamella and the thylakoid lamellae, respectively. es, eyespot; n, nucleus. Scale bars: 1 μm (a, e); 500 nm (b, c, d, f). (PNG 1311 kb)

High Resolution Image (TIF 10222 kb)

Fig. S3

Ultrastructure of a zygote at two hours after fertilization. a-l Zygote nucleus just after karyogamy. Twenty-seven mitochondria are numbered, and nine chloroplasts are indicated by serial number with C. Mitochondrion numbered as 21 is excluded to show in m-p with high magnification. g-j A female gamete chloroplast with eyespots (c7) is seen. h Male nuclear part with an enriched heterochromatin region that is found in the right side of nucleus. Besides the male nucleus, a chloroplast (c9) of male gamete with eyespots exists. m-p Degrading mitochondrion (numbered as 21) near a male chloroplast (c9). C, centriole; es, eyespot; n, nucleus. Scale bars: 500 nm. (PNG 1729 kb)

High resolution image (TIF 16541 kb)

Fig. S4

Digestion of male mitochondria in a two-hour-old zygote before karyogamy. a Whole cell image. Female nucleus (Fn) and male nucleus (Mn) before karyogamy are observed. b-h Partial serial sections of a magnified view from the white rectangular region in a. Mitochondria labeled with m1-m3 are isolated by double-membranes and inside different destruction degrees of mitochondria can be observed. e, f Male chloroplast with eyespot tightly attaches with male nucleus. Scale bars: 1 μm (a); 200 nm (b-h). (PNG 1819 kb)

High resolution image (TIF 11691 kb)

Fig S5

(PNG 1.66 mb)

High Resolution Image (TIF 12449 kb)

Fig. S6

Ultrastructure of zygote at six hours after fertilization. a-l Twenty-nine mitochondria numbered, and ten chloroplasts are numbered with C. a, b Male chloroplast with eyespots (c5). d-h Female chloroplast with an eyespot (c7). es, eyespot; n, nucleus. Scale bars: 500 nm. (TIF 3877 kb) (PNG 645 kb)

High Resolution Image (TIF 3877 kb)

Fig. S7

Ultrastructure of a seven-celled crustose sporophyte. a, b The whole image of a 7-celled crustose sporophyte in two different sections. c The enlarged view from the white rectangular region in a. d The enlarged view from the white rectangular region in b. Note that the size of eyespots is diminished (c1 and c2). es, eyespot; m, mitochondrion; n, nucleus; v, vacuole. Scale bars: 2 μm (a, b); 500 nm (c, d). ((PNG 184 kb)

High Resolution Image (TIF 11661 kb)

Fig S8

Diagrams of primer locations in the PCR assay. a Primer location of nrDNA ITS1 region. b mtDNA cox1 gene. c chlDNA psaA gene. Predicted sizes are shown between the primer pairs. (PNG 127 kb)

High Resolution Image (TIF 11686 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shen, Y., Iwao, T., Motomura, T. et al. Cytoplasmic inheritance of mitochondria and chloroplasts in the anisogamous brown alga Mutimo cylindricus (Phaeophyceae). Protoplasma 258, 19–32 (2021). https://doi.org/10.1007/s00709-020-01540-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-020-01540-x

Keywords

Search

Navigation