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Two male sterility-inducing cytoplasms of beet (Beta vulgaris) are genetically distinct but have closely related mitochondrial genomes: implication of a substoichiometric mitochondrial DNA molecule in their evolution

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Abstract

I-12CMS(2) and I-12CMS(3) are sugar beet lines with different sources of cytoplasmic male sterility (CMS) derived from wild beets in Turkey and Pakistan, respectively. We established that I-12CMS(2) has a genetically distinct cytoplasm, but its mitochondrial genome is very similar to I-12CMS(3). Male fertility was assessed in F1 hybrids produced with a common pollen parent. Fertility in the F1's carrying the I-12CMS(3) cytoplasm exceeded that of the F1's with the I-12CMS(2) cytoplasm. Organization of the I-12CMS(2) and I-12CMS(3) mitochondrial genomes were compared based on their physical maps. Mitochondrial genomes of the two strains were largely collinear, except for a large deletion in the noncoding region of I-12CMS(2). Because a mitochondrial orf129 in the I-12CMS(3) cytoplasm is associated with a male sterility phenotype and preservation of orf129 was evident in I-12CMS(2), I-12CMS(2) orf129 was investigated in detail. I-12CMS(2) plants contained three to five times more ORF129 protein than did I-12CMS(3) plants. A single nucleotide substitution, present in the putative promoter region of orf129, appeared to be responsible for the differential accumulation of orf129 transcript. A long N-terminal extension of atp6 is a common feature of some beet CMSs and is found in I-12CMS(2), but the amino acid sequence is unique. I-12CMS(3) mitochondria, but not I-12CMS(2) mitochondria, were found to be heteroplasmic. This heteroplasmy is characterized by a substoichiometric DNA molecule(s) that has at least two I-12CMS(2)-type mitochondrial loci, suggesting the possibility that the I-12CMS(2) mitochondrial genome might have evolved from such a substoichiometric DNA molecule in I-12CMS(3) mitochondria.

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Acknowledgments

Part of this work was conducted at the Center for Genome Dynamics, Faculty of Science, Hokkaido University. This work was supported in part by JSPS KAKENHI Grant Number 25292001.

Conflict of interest

The authors declare that they have no conflict of interest.

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Author notes

  1. Masayuki P. Yamamoto

    Present address: Department of Biology, Faculty of Science, University of Toyama, Toyama, 930-8555, Japan

  2. Kazuyoshi Kitazaki

    Present address: Lowland Farming and Horticulture Research Division, Kyushu Okinawa Agricultural Research Center, National Agriculture and Food Research Organization, Kurume, Fukuoka, 839-8503, Japan

  3. Shigehiko Ebe

    Present address: Tokachi Agricultural Experiment Station, Agriculture Research Department, Hokkaido Research Organization, Memuro, Hokkaido, 082-0081, Japan

Authors and Affiliations

  1. Laboratory of Genetic Engineering, Research Faculty of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan

    Yasuyuki Onodera, Takumi Arakawa, Rika Yui-Kurino, Masayuki P. Yamamoto, Kazuyoshi Kitazaki, Muneyuki Matsunaga, Shiko Yamashita, Tomoyuki Sakai, Tetsuo Mikami & Tomohiko Kubo

  2. Plant Breeding Institute, Research Faculty of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan

    Shigehiko Ebe & Toshiro Kinoshita

  3. Hokkaido Agricultural Research Center, National Agriculture and Food Research Organization, Memuro, Hokkaido, 082-0081, Japan

    Kazunori Taguchi & Yosuke Kuroda

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  1. Yasuyuki Onodera
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Correspondence to Tomohiko Kubo.

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Onodera, Y., Arakawa, T., Yui-Kurino, R. et al. Two male sterility-inducing cytoplasms of beet (Beta vulgaris) are genetically distinct but have closely related mitochondrial genomes: implication of a substoichiometric mitochondrial DNA molecule in their evolution. Euphytica 206, 365–379 (2015). https://doi.org/10.1007/s10681-015-1484-2

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