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A recombination-derived mitochondrial genome retained stoichiometrically only among Solanum verrucosum Schltdl. and Mexican polyploid wild potato species

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Abstract

We previously found a specific DNA fragment, designated Band 1, in the cytoplasm of a Mexican hexaploid wild potato species, Solanum demissum, and varieties with the S. demissum cytoplasm. In this study, we show that Band 1 also occurs substoichiometrically in various species and varieties. The S. demissum DNA sequence harboring Band 1 was extended by genome walking to 7,040 bp, and whole-genome sequencing of the S. verrucosum genome generated a 10,794-bp contig with the corresponding sequence. Their 3′-terminal end sequences had 100 % homology with segment 2 of the S. tuberosum mitochondrial genome, proving that Band 1 originated from a recombination-derived mitochondrial genome. Both normal and recombination-derived mitochondrial genomes co-existed in Band 1 carriers. The presence or absence of Band 1 was surveyed for four accessions of tomato and wild relatives and 172 accessions of 38 Solanum species or potato and tuber-bearing wild relatives, mostly from Mexican species. Together, with the results of our previous survey (mostly for South American species), we conclude that Band 1 is retained stoichiometrically only among S. verrucosum and Mexican polyploid species, supporting S. verrucosum as a maternal ancestor for all Mexican polyploid species. The presence or absence of Band 1 was not uniform within these species and was not associated with ploidy, geographical distribution, or latitude. Several evolutionary hypotheses to explain intraspecific variation were discussed.

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References

  • Abdalla MMF, Hermsen JGTh (1971) The plasmon-genic basis of pollen lobedness and tetrad sterility in Solanum verrucosum hybrids and duplicate linkage groups. Genetica 42:261–270

    Article  Google Scholar 

  • Abdalla MMF, Hermsen JGTh (1973) An evaluation of Solanum verrucosum Schlechtd. for its possible use in potato breeding. Euphytica 22:19–27

    Article  Google Scholar 

  • Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci USA 100:5968–5973

    Article  PubMed  CAS  Google Scholar 

  • Ames M, Spooner DM (2010) Phylogeny of Solanum series Piurana and related species in Solanum section Petota based on five conserved ortholog sequences. Taxon 59:1091–1104

    Google Scholar 

  • Ames M, Salas A, Spooner DM (2007) The discovery and phylogenetic implications of a novel 41 bp plastid DNA deletion in wild potatoes. Plant Syst Evol 268:159–175

    Article  CAS  Google Scholar 

  • Arrieta-Montiel M, Lyznik A, Woloszynska M, Janska H, Tohme J, Mackenzie S (2001) Tracing evolutionary and developmental implications of mitochondrial stoichiometric shifting in the common bean. Genetics 158:851–864

    PubMed  CAS  Google Scholar 

  • Cai D, Rodríguez F, Teng Y, Ané C, Bonierbale M, Mueller LA, Spooner DM (2012) Single copy nuclear gene analysis of polyploidy in wild potatoes (Solanum section Petota). BMC Evol Biol 12:70

    Article  PubMed  CAS  Google Scholar 

  • Chen J, Guan R, Chang S, Du T, Zhang H, Xing H (2011) Substoichiometrically different mitotypes coexist in mitochondrial genomes of Brassica napus L. PLoS One 6:e17662

    Article  PubMed  CAS  Google Scholar 

  • Cipar MS, Peloquin SJ, Hougas RW (1964) Inheritance of incompatibility in hybrids between Solanum tuberosum haploids and diploid species. Euphytica 13:163–172

    Google Scholar 

  • Dionne LA (1961) Cytoplasmic sterility in derivatives of Solanum demissum. Am Potato J 38:117–120

    Article  Google Scholar 

  • Fajardo D, Spooner DM (2011) Phylogenetic relationships of Solanum series Conicibaccata and related species in Solanum section Petota inferred from five conserved ortholog sequences. Syst Bot 36:163–170

    Article  Google Scholar 

  • Feng X, Kaur AP, Mackenzie SA, Dweikat IM (2009) Substoichiometric shifting in the fertility reversion of cytoplasmic male sterile pearl millet. Theor Appl Genet 118:1361–1370

    Article  PubMed  CAS  Google Scholar 

  • Green MR, Sambrook J (2012) Molecular cloning: a laboratory manual, 4th edn: three-volume set. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Grun P, Aubertin M, Radlow A (1962) Multiple differentiation of plasmons of diploid species of Solanum. Genetics 47:1321–1333

    PubMed  CAS  Google Scholar 

  • Hawkes JG (1990) The potato—evolution, biodiversity and genetic resources. Belhaven Press, London

    Google Scholar 

  • Hijmans RJ, Guarino L, Cruz M, Rojas E (2001) Computer tools for spatial analysis of plant genetic resources data: 1 DIVA-GIS. Plant Genet Resour Newsl 127:15–19

  • Hosaka K (2002) Distribution of the 241 bp deletion of chloroplast DNA in wild potato species. Am J Potato Res 79:119–123

    Article  CAS  Google Scholar 

  • Hosaka K, Hanneman RE Jr (1998) Genetics of self-compatibility in a self-incompatible wild diploid potato species Solanum chacoense. 2. Localization of an S locus inhibitor (Sli) gene on the potato genome using DNA markers. Euphytica 103:265–271

    Article  CAS  Google Scholar 

  • Hosaka K, Sanetomo R (2012) Development of a rapid identification method for potato cytoplasm and its use for evaluating Japanese collections. Theor Appl Genet 125:1237–1251

    Article  PubMed  CAS  Google Scholar 

  • Hosaka K, Ogihara Y, Matsubayashi M, Tsunewaki K (1984) Phylogenetic relationship between the tuberous Solanum species as revealed by restriction endonuclease analysis of chloroplast DNA. Jpn J Genet 59:349–369

    Article  CAS  Google Scholar 

  • Janska H, Sarria R, Woloszynska M, Arrieta-Montiel M, Mackenzie S (1998) Stoichiometric shifts in the common bean mitochondrial genome leading to male sterility and spontaneous reversion to fertility. Plant Cell 10:1163–1180

    PubMed  CAS  Google Scholar 

  • Jansky SH, Hamernik AJ (2009) The use of Solanum verrucosum as a bridge species. Genet Resour Crop Evol 56:1107–1115

    Article  Google Scholar 

  • Kanazawa A, Tsutsumi N, Hirai A (1994) Reversible changes in the composition of the population of mtDNAs during dedifferentiation and regeneration in tobacco. Genetics 138:865–870

    PubMed  CAS  Google Scholar 

  • Kardolus JP, van Eck HJ, van den Berg RG (1998) The potential of AFLPs in biosystematics: a first application in Solanum taxonomy (Solanaceae). Plant Syst Evol 210:87–103

    Article  Google Scholar 

  • Kim DH, Kim BD (2006) The organization of mitochondrial atp6 gene region in male fertile and CMS lines of pepper (Capsicum annuum L.). Curr Genet 49:59–67

    Article  PubMed  CAS  Google Scholar 

  • Kim S, Lim H, Park S, Cho KH, Sung SK, Oh DG, Kim KT (2007) Identification of a novel mitochondrial genome type and development of molecular markers for cytoplasm classification in radish (Raphanus sativus L.). Theor Appl Genet 115:1137–1145

    Article  PubMed  CAS  Google Scholar 

  • L’Homme Y, Brown GG (1993) Organizational differences between cytoplasmic male sterile and male fertile Brassica mitochondrial genomes are confined to a single transposed locus. Nucleic Acids Res 21:1903–1909

    Article  PubMed  Google Scholar 

  • Mackenzie SA, Chase CD (1990) Fertility restoration is associated with loss of a portion of the mitochondrial genome in cytoplasmic male-sterile common bean. Plant Cell 2:905–912

    PubMed  CAS  Google Scholar 

  • Martínez-Zapater JM, Gil P, Capel J, Somerville CR (1992) Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell 4:889–899

    PubMed  Google Scholar 

  • Matsubayashi M (1991) Phylogenetic relationships in the potato and its related species. In: Tsuchiya T, Gupta PK (eds) Chromosome engineering in plants: genetics, breeding, evolution Part B. Elsevier, Amsterdam, pp 93–118

    Google Scholar 

  • Nakagawa K, Hosaka K (2002) Species relationships between a wild tetraploid potato species, Solanum acaule Bitter, and its related species as revealed by RFLPs of chloroplast and nuclear DNA. Am J Potato Res 79:85–98

    Article  CAS  Google Scholar 

  • Pandey KK (1962) Interspecific incompatibility in Solanum species. Am J Bot 49:874–882

    Article  Google Scholar 

  • Pendinen G, Gavrilenko T, Jiang J, Spooner DM (2008) Allopolyploid speciation of the tetraploid Mexican potato species S. stoloniferum and S. hjertingii revealed by genomic in situ hybridization. Genome 51:714–720

    Article  PubMed  CAS  Google Scholar 

  • Pendinen G, Spooner DM, Jiang J, Gavrilenko T (2012) Genomic in situ hybridization (GISH) reveals both autopolyploid and allopolyploid origins of different North and Central American hexaploid potato (Solanum section Petota) species. Genome 55:407–415

    Article  PubMed  CAS  Google Scholar 

  • Peralta IE, Spooner DM, Knapp S (2008) The taxonomy of tomatoes: a revision of wild tomatoes (Solanum section Lycopersicon) and their outgroup relatives in sections Juglandifolium and Lycopersicoides. Syst Bot Monogr 84:1–186

    Google Scholar 

  • Plaisted RL, Hoopes RW (1989) The past record and future prospects for the use of exotic potato germplasm. Am Potato J 66:603–627

    Article  Google Scholar 

  • Pushkarnath (1942) Studies on sterility in potatoes. 1. The genetics of self- and cross-incompatibilities. Indian J Genet Plant Breed 2:11–36

    Google Scholar 

  • Rodríguez F, Spooner DM (2009) Nitrate reductase phylogeny of potato (Solanum sect. Petota) genomes with emphasis on the origins of the polyploid species. Syst Bot 34:207–219

    Article  Google Scholar 

  • Ross H (1986) Potato breeding—problems and perspectives. Verlag Paul Parey, Berlin and Hamburg

    Google Scholar 

  • Sanetomo R, Hosaka K (2011a) Reciprocal differences in DNA sequence and methylation status of the pollen DNA between F1 hybrids of Solanum tuberosum × S. demissum. Euphytica 182:219–229

    Article  CAS  Google Scholar 

  • Sanetomo R, Hosaka K (2011b) A maternally inherited DNA marker, descended from Solanum demissum (2n = 6x = 72) to S. tuberosum (2n = 4x = 48). Breed Sci 61:426–434

    Article  PubMed  CAS  Google Scholar 

  • Sanetomo R, Ono S, Hosaka K (2011) Characterization of crossability in the crosses between Solanum demissum and S. tuberosum, and the F1 and BC1 progenies. Am J Potato Res 88:500–510

    Article  Google Scholar 

  • Scotti N, Maréchal-Drouard L, Cardi T (2004) The rpl5-rps14 mitochondrial region: a hot spot for DNA rearrangements in Solanum spp. somatic hybrids. Curr Genet 45:378–382

    Article  PubMed  CAS  Google Scholar 

  • Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19:1251–1264

    Article  PubMed  CAS  Google Scholar 

  • Singh M, Brown GG (1991) Suppression of cytoplasmic male sterility by nuclear genes alters expression of a novel mitochondrial gene region. Plant Cell 3:1349–1362

    PubMed  CAS  Google Scholar 

  • Small ID, Isaac PG, Leaver CJ (1987) Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J 6:865–869

    PubMed  CAS  Google Scholar 

  • Spooner DM, Castillo RT (1997) Reexamination of series relationships of South American wild potatoes (Solanaceae: Solanum sect. Petota): evidence from chloroplast DNA restriction site variation. Am J Bot 84:671–685

    Article  PubMed  CAS  Google Scholar 

  • Spooner DM, Hijmans RJ (2001) Potato systematics and germplasm collecting, 1989–2000. Am J Potato Res 78:237–268, 395

    Article  Google Scholar 

  • Spooner DM, van den Berg RG, Bamberg JB (1995) Examination of species boundaries of Solanum series Demissa and potentially related species in series Acaulia and series Tuberosa (sect. Petota). Syst Bot 20:295–314

    Article  Google Scholar 

  • Spooner DM, van den Berg RG, Rodríguez A, Bamberg J, Hijmans RJ, Lara-Cabrera SI (2004) Wild potatoes (Solanum section Petota) of North and Central America. Syst Bot Monogr 68:1–209

    Article  Google Scholar 

  • Spooner DM, Rodríguez F, Polgár Z, Ballard HE Jr, Jansky SH (2008) Genomic origins of potato polyploids: GBSSI gene sequencing data. Plant Genome Suppl Crop Sci 48(S1):S27–S36

    CAS  Google Scholar 

  • Spooner DM, Ames M, Fajardo D, Rodríguez F (2009) Species boundaries and interrelationships of Solanum sect. Petota (wild and cultivated potatoes) are drastically altered as a result of PBI-funded research, ASA-CSSA-SSSA Annual Meeting Abstracts. Paper No 54478

    Google Scholar 

  • Takeuchi T, Sasaki J, Suzuki T, Horita H, Hiura S, Iketani S, Fujita R, Senda K (2009) DNA markers for efficient selection of disease and pests resistance genes in potato. Hokkaido Nogyo-Shiken-Kaigi-Shiryo 2008:1–26

    Google Scholar 

  • The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

    Article  Google Scholar 

  • Thompson RD, Kirch HH (1992) The S locus of flowering plants: when self-rejection is self-interest. Trends Genet 8:381–387

    PubMed  CAS  Google Scholar 

  • Zaegel V, Guermann B, Le Ret M, Andrés C, Meyer D, Erhardt M, Canaday J, Gualberto JM, Imbault P (2006) The plant-specific ssDNA binding protein OSB1 is involved in the stoichiometric transmission of mitochondrial DNA in Arabidopsis. Plant Cell 18:3548–3563

    Article  PubMed  CAS  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the US Potato Genebank (NRSP-6), Sturgeon Bay, Wisconsin, for providing the Solanum seeds used in this study, and Dr. David M. Spooner for kindly checking taxonomic identities with his updated taxonomy and reviewing the manuscript. We also thank Dr. Itsuro Sugimura and Naoyuki Sugimoto, Hokkaido System Science Co. Ltd., for initial handling of Illumina data, and Shizuka Souma for technical assistance. This study was supported by Calbee, Inc. and Calbee Potato, Inc.

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Correspondence to Kazuyoshi Hosaka.

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Sanetomo, R., Hosaka, K. A recombination-derived mitochondrial genome retained stoichiometrically only among Solanum verrucosum Schltdl. and Mexican polyploid wild potato species. Genet Resour Crop Evol 60, 2391–2404 (2013). https://doi.org/10.1007/s10722-013-0007-z

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