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Morphogenesis and spontaneous chromosome doubling during the parthenogenetic development of haploid female gametophytes in Pyropia haitanensis (Bangiales, Rhodophyta)

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Abstract

Pyropia haitanensis is one of the most economically important seaweeds growing in the coastal regions of south China. Previous studies revealed that parthenogenesis could emerge in P. haitanensis under certain culture conditions. In the present study, detailed cytological observations were made of morphogenesis and chromosomal behaviors of female gametophytes of P. haitanensis during parthenogenesis. Unisexual cultures of female gametophytes, derived from isolated somatic cells of wild gametophytes or obtained from cloned sporophytes, ultimately led to their development into parthenosporophytes. Based on the changes in shape and color of the cellular chromatophore, as well as the metamorphosis and condition of the released cells, the parthenogenesis of P. haitanensis was divided into six developmental stages: vegetative cells (VCs) with multiple stellate chromatophores, carpogonium-like cells (CLCs) with dispersed chromatophores, carpogonium-like protoplasts (CLPs) released post-cell wall dissolution, carpospore-like cells (CCs) with regenerated cell wall, carpospore-like germlings (CGs), and parthenosporophytes. Chromosomal observations showed that VCs were haploid (n = 5), small proportions of CLCs, and CLPs and CCs were diploid (2n = 10), while all the CGs, filamentous conchocelis cells, and conchosporangial branch cells of parthenosporophytes were diploid (2n = 10). Haploid, aneuploid, and polyploidy were not observed in the latter group of cells. Spontaneous chromosome doubling occurred during the parthenogenesis of P. haitanensis, first in highly differentiated CLCs. Furthermore, pit connections could be seen throughout the parthenosporophyte development process similar to that in heterozygous sporophytes. The chromosomes were seen undergoing meiosis during the germination of conchospores released from mature parthenosporophytes, leading to the generation of tetrad cells, which developed into haploid female gametophytes. These results provide evidence for better understanding the mechanism underlying parthenogenesis in Pyropia.

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Acknowledgements

The authors would like to acknowledge Prof. Qi Lin (Fisheries Research Institute of Fujian Province, China) for reading the manuscript.

Funding

The study was supported in part by the National Key Research and Development Program of China (2018YFD0900606), National Natural Science Foundation of China (31072208), Major Science and Technology Specific Program of Zhejiang Province (2016C02055-6), and Science and Tecnology Planning Project of Jiangsu Province, China (BE2018335).

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Authors and Affiliations

  1. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai, China

    Chenhui Zhong & Xinghong Yan

  2. Provincial Key Laboratory of Cultivation and High–Value Utilization of Marine Organisms, Fisheries Research Institute of Fujian Province, Xiamen, Fujian, China

    Chenhui Zhong

  3. Nishikamata 2-4-21, Ota-ku, Tokyo, Japan

    Yusho Aruga

  4. National Demonstration Center for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai, China

    Xinghong Yan

  5. Shanghai Engineering Research Center of Aquaculture, Shanghai, China

    Xinghong Yan

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  1. Chenhui Zhong
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  2. Yusho Aruga
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Correspondence to Xinghong Yan.

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Zhong, C., Aruga, Y. & Yan, X. Morphogenesis and spontaneous chromosome doubling during the parthenogenetic development of haploid female gametophytes in Pyropia haitanensis (Bangiales, Rhodophyta). J Appl Phycol 31, 2729–2741 (2019). https://doi.org/10.1007/s10811-019-01769-x

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  • DOI: https://doi.org/10.1007/s10811-019-01769-x

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