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

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ORIGINAL ARTICLE

Cytoplasmic inheritance of mitochondria and chloroplasts in the anisogamous brown alga Mutimo cylindricus (Phaeophyceae) Yuan Shen 1 & Toyoki Iwao 2 & Taizo Motomura 3 & Chikako Nagasato 3 Received: 11 May 2020 / Accepted: 28 July 2020 # Springer-Verlag GmbH Austria, part of Springer Nature 2020

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. Keywords Anisogamy . Brown algae . Cytoplasmic inheritance . Organelle DNA copy number . Strain specific PCR . Ultrastructure

Introduction In 1909, the non-Mendelian inheritance was firstly discovered in the higher plants Mirabilis jalapa and Pelargonium zonale (Baur 1909; Correns 1909). Interestingly, these discoveries Handling Editor: Handling Editor: Tsuneyoshi Kuroiwa Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00709-020-01540-x) contains supplementary material, which is available to authorized users. * Chikako Nagasato [email protected] 1

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

2

Toba Fisheries Science Center, Toba 517-0005, Japan

3

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

were two entirely different patterns in inheritance of leaf phenotypes. The o