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Rare maternal and biparental transmission of the cucumber mitochondrial DNA reveals sorting of polymorphisms among progenies

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Abstract

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We used a mitochondrial (mt) mutant of cucumber to document rare maternal transmission of mt polymorphisms and demonstrate that polymorphisms can become more prevalent and sort to progenies to increase mt DNA diversity.

Abstract

The mitochondrial (mt) DNAs of most angiosperms show maternal inheritance, although relatively rare biparental or paternal transmission has been documented. The mt DNAs of plants in the genus Cucumis (family Cucurbitaceae) are paternally transmitted in intra- and interspecific crosses. MSC16 is an inbred line of cucumber (Cucumis sativus) with a mitochondrially associated mosaic (MSC) phenotype. MSC16 was crossed as the male parent to wild-type cultivar Calypso, and hybrid progenies were evaluated for the wild-type phenotype in order to screen for rare maternal or biparental transmission of the mt DNA. We then used standard and droplet digital (dd) PCR to study the transmission of polymorphic mt markers across three generations. We observed evidence for occasional maternal and biparental transmission of the mt DNA in cucumber. The transmission of specific regions of the maternal mt DNA could be as high as 17.8%, although the amounts of these maternal regions were often much lower relative to paternally transmitted regions. Different combinations of maternal and paternal mt polymorphisms were detected in progenies across generations, indicating that relatively rare maternal regions can be transmitted to progenies and become predominant to increase mt DNA diversity over generations.

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Acknowledgments

We gratefully acknowledge the support of Nanjing (China) Agricultural University and Zhejiang Academy of Agricultural Sciences to JS (31601764; 31572134; 2017C32004; 2016C02051-4-4) and Grant 2011-51181-30661 from the USDA Specialty Crops Research Initiative (USA).

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Authors and Affiliations

  1. Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, China

    Jia Shen, Weisong Shou & Yuejian Zhang

  2. College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Jia Shen, Gaoya Yuan, Yu Zhao & Jinfeng Chen

  3. USDA-ARS and Department of Horticulture, University of Wisconsin, Madison, WI, 53706, USA

    Michael J. Havey

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  1. Jia Shen
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  2. Weisong Shou
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  3. Yuejian Zhang
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  4. Gaoya Yuan
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  5. Yu Zhao
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  6. Jinfeng Chen
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  7. Michael J. Havey
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Correspondence to Michael J. Havey.

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Communicated by Amnon Levi.

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Shen, J., Shou, W., Zhang, Y. et al. Rare maternal and biparental transmission of the cucumber mitochondrial DNA reveals sorting of polymorphisms among progenies. Theor Appl Genet 132, 1223–1233 (2019). https://doi.org/10.1007/s00122-018-03274-0

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