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Genetic mapping of paternal sorting of mitochondria in cucumber

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Abstract

Mitochondria are organelles that have their own DNA; serve as the powerhouses of eukaryotic cells; play important roles in stress responses, programmed cell death, and ageing; and in the vast majority of eukaryotes, are maternally transmitted. Strict maternal transmission of mitochondria makes it difficult to select for better-performing mitochondria, or against deleterious mutations in the mitochondrial DNA. Cucumber is a useful plant for organellar genetics because its mitochondria are paternally transmitted and it possesses one of the largest mitochondrial genomes among all eukaryotes. Recombination among repetitive motifs in the cucumber mitochondrial DNA produces rearrangements associated with strongly mosaic (MSC) phenotypes. We previously reported nuclear control of sorting among paternally transmitted mitochondrial DNAs. The goal of this project was to map paternal sorting of mitochondria as a step towards its eventual cloning. We crossed single plants from plant introduction (PI) 401734 and Cucumis sativus var. hardwickii and produced an F2 family. A total of 425 F2 plants were genotyped for molecular markers and testcrossed as the female with MSC16. Testcross families were scored for frequencies of wild-type versus MSC progenies. Discrete segregations for percent wild-type progenies were not observed and paternal sorting of mitochondria was therefore analyzed as a quantitative trait. A major quantitative trait locus (QTL; LOD >23) was mapped between two simple sequence repeats encompassing a 459-kb region on chromosome 3. Nuclear genes previously shown to affect the prevalence of mitochondrial DNAs (MSH1, OSB1, and RECA homologs) were not located near this major QTL on chromosome 3. Sequencing of this region from PI 401734, together with improved annotation of the cucumber genome, should result in the eventual cloning of paternal sorting of mitochondria and provide insights about nuclear control of organellar-DNA sorting.

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References

  • 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  CAS  Google Scholar 

  • Al-Faifi S, Meyer J, Garcia-Mas J, Monforte A, Havey M (2008) Exploiting synteny in Cucumis for mapping of Psm: a unique locus controlling paternal mitochondrial sorting. Theor Appl Genet 117:523–529

    Article  PubMed  CAS  Google Scholar 

  • Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD (2011) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23:2499–2513

    Article  PubMed  CAS  Google Scholar 

  • Arrieta-Montiel MP, Shedge V, Davila J, Christensen AC, Mackenzie SA (2009) Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 183:1261–1268

    Article  PubMed  CAS  Google Scholar 

  • Bartoszewski G, Malepszy S, Havey MJ (2004) Mosaic (MSC) cucumbers regenerated from independent cell cultures possess different mitochondrial rearrangements. Curr Genet 45:45–53

    Article  PubMed  CAS  Google Scholar 

  • Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl. Springer, New York

    Book  Google Scholar 

  • Castelo AT, Martins W, Gao GR (2002) TROLL-tandem repeat occurrence locator. Bioinformatics 18:634–636

    Article  PubMed  CAS  Google Scholar 

  • Chat J, Chalak L, Petit RJ (1999) Strict paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in interspecific crosses of kiwifruit. Theor Appl Genet 99:314–322

    Article  Google Scholar 

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed  CAS  Google Scholar 

  • Dijkhuizen A, Kennard WC, Havey MJ, Staub JE (1996) RFLP variation and genetic relationships in cultivated cucumber. Euphytica 90:79–87

    Google Scholar 

  • Fauré S, Noyer J-L, Carreel F, Horry J-P, Bakry F, Lanaud C (1994) Maternal inheritance of chloroplast genome and paternal inheritance of mitochondrial genome in bananas (Musa acuminata). Curr Genet 25:265–269

    Article  PubMed  Google Scholar 

  • Fauron CM-R, Moore B, Casper M (1995) Maize as a model of higher plant mitochondrial genome plasticity. Plant Sci 112:11–32

    Article  CAS  Google Scholar 

  • Fujii S, Toriyama K (2008) Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility. Plant Cell Physiol 49:1484–1494

    Article  PubMed  CAS  Google Scholar 

  • Gillham NW (1994) Organelle genes and genomes. Oxford University Press, New York

    Google Scholar 

  • Havey MJ (1997) Predominant paternal transmission of the mitochondrial genome in cucumber. J Hered 88:232–235

    Article  Google Scholar 

  • Havey MJ, McCreight JD, Rhodes B, Taurick G (1998) Differential transmission of the Cucumis organellar genomes. Theor Appl Genet 97:122–128

    Article  CAS  Google Scholar 

  • Havey MJ, Park YH, Bartoszewski G (2004) The Psm locus controls paternal sorting of the cucumber mitochondrial genome. J Hered 95:492–497

    Article  PubMed  CAS  Google Scholar 

  • Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P, Ren Y, Zhu H, Li J, Lin K, Jin W, Fei Z, Li G, Staub J, Kilian A, van der Vossen EAG, Wu Y, Guo J, He J, Jia Z, Ren Y, Tian G, Lu Y, Ruan J, Qian W, Wang M, Huang Q, Li B, Xuan Z, Cao J, Asan WuZ, Zhang J, Cai Q, Bai Y, Zhao B, Han Y, Li Y, Li X, Wang S, Shi Q, Liu S, Cho WK, Kim J-Y, Xu Y, Heller-Uszynska K, Miao H, Cheng Z, Zhang S, Wu J, Yang Y, Kang H, Li M, Liang H, Ren X, Shi Z, Wen M, Jian M, Yang H, Zhang G, Yang Z, Chen R, Liu S, Li J, Ma L, Liu H, Zhou Y, Zhao J, Fang X, Li G, Fang L, Li Y, Liu D, Zheng H, Zhang Y, Qin N, Li Z, Yang G, Yang S, Bolund L, Kristiansen K, Zheng H, Li S, Zhang X, Yang H, Wang J, Sun R, Zhang B, Jiang S, Wang J, Du Y, Li S (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281

    Article  PubMed  CAS  Google Scholar 

  • Jiang C, Zeng ZB (1995) Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics 140:1111–1127

    PubMed  CAS  Google Scholar 

  • Krysan P (2004) Ice-Cap. A high-throughput method for capturing plant tissue samples for genotype analysis. Plant Physiol 135:1162–1169

    Article  PubMed  CAS  Google Scholar 

  • Lilly J, Havey M (2001) Small, repetitive DNAs contribute significantly to the expanded mitochondrial genome of cucumber. Genetics 159:317–328

    PubMed  CAS  Google Scholar 

  • Lilly J, Bartoszewski G, Malepszy S, Havey M (2001) A major deletion in the cucumber mitochondrial genome sorts with the MSC phenotype. Curr Genet 40:144–151

    Article  PubMed  CAS  Google Scholar 

  • Lower RL, Edwards MD (1986) Cucumber breeding. In: Basset MJ (ed) Breeding vegetable crops. AVI Publishing, Westport, pp 173–207

    Google Scholar 

  • Mader E, Lukas B, Novak J (2008) A strategy to setup codominant microsatellite analysis for high-resolution-melting-curve-analysis (HRM). BMC Genet 9:69

    Article  PubMed  Google Scholar 

  • Malepszy S, Burza W, Smiech M (1996) Characterization of a cucumber (Cucumis sativus L.) somaclonal variant with paternal inheritance. J Appl Genet 37:65–78

    Google Scholar 

  • Manly KF, Olson JM (1999) Overview of QTL mapping software and introduction to map manager QT. Mamm Genome 10:327–334

    Article  PubMed  CAS  Google Scholar 

  • Manly KF, Cudmore RH Jr, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mamm Genome 12:930–932

    Article  PubMed  CAS  Google Scholar 

  • Maréchal A, Brisson N (2010) Recombination and the maintenance of plant organelle genome stability. New Phytol 186:299–317

    Article  PubMed  Google Scholar 

  • Martinez-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

    Article  PubMed  CAS  Google Scholar 

  • McCauley DE, Bailey MF, Sherman NA, Darnell MZ (2005) Evidence for paternal transmission and heteroplasmy in the mitochondrial genome of Silene vulgaris, a gynodioecious plant. Heredity 95:50–58

    Article  PubMed  CAS  Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci (USA) 88:9828–9832

    Article  CAS  Google Scholar 

  • Neale DB, Sederoff RR (1989) Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theor Appl Genet 77:212–216

    Article  Google Scholar 

  • Neale DB, Marshall KA, Sederoff RR (1989) Chloroplast and mitochondrial DNA are paternally inherited in Sequoia sempervirens D. Don Endl. Proc Natl Acad Sci 86:9347–9349

    Article  PubMed  CAS  Google Scholar 

  • Newton KJ (1995) Aberrant growth phenotypes associated with mitochondrial genome rearrangements in higher plants. In: Levings CS III, Vasil IK (eds) The molecular biology of plant mitochondria. Kluwer, Boston, pp 585–596

    Chapter  Google Scholar 

  • Odahara M, Kuroiwa H, Kuroiwa T, Sekine Y (2009) Suppression of repeat-mediated gross mitochondrial genome rearrangements by RecA in the moss Physcomitrella patens. Plant Cell 21:1182–1194

    Article  PubMed  CAS  Google Scholar 

  • Pierce LK, Wehner TC (1990) Review of genes and linkage groups in cucumber. HortScience 25:605–615

    CAS  Google Scholar 

  • Reboud X, Zeyl C (1994) Organelle inheritance in plants. Heredity 72:132–140

    Article  Google Scholar 

  • Ren Y, Zhang Z, Liu J, Staub JE, Han Y, Cheng Z, Li X, Lu J, Miao H, Kang H, Xie B, Gu X, Wang X, Du Y, Jin W, Huang S (2009) An integrated genetic and cytogenetic map of the cucumber genome. PLoS one 4:e5795

    Article  PubMed  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 

  • Smith SE (1989) Biparental inheritance of organelles and its implications in crop improvement. Plant Breed Rev 6:361–393

    Google Scholar 

  • Staub JE, Chung SM, Fazio G (2005) Conformity and genetic relatedness estimation in crop species having a narrow genetic base: the case of cucumber (Cucumis sativus L.). Plant Breeding 124:44–53

    Article  CAS  Google Scholar 

  • Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61

    Article  PubMed  CAS  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2010) Windows QTL Cartographer 2.5, Department of Statistics, North Carolina State University, Raleigh, NC

  • Ward B, Anderson R, Bendich A (1981) The mitochondrial genome is large and variable in a family of plants (Cucurbitaceae). Cell 25:793–803

    Article  PubMed  CAS  Google Scholar 

  • Weihe A, Apitz J, Pohlheim F, Salinas-Hartwig A, Börner T (2009) Biparental inheritance of plastidial and mitochondrial DNA and hybrid variegation in Pelargonium. Mol Genet Genomics 282:587–593

    Article  PubMed  CAS  Google Scholar 

  • Xu Y-Z, Arrieta-Montiel M, Virdi K, Paula W, Widhaim J, Basset G, Davila J, Elthon T, Elowsky C, Sato S, Clemente T, MacKenzie S (2011) MutS homolog1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. Plant Cell 23:3426–3441

    Article  Google Scholar 

  • Zaegel V, Guermann B, Le Ret M, Andres 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 

  • Zeng Z-B (1993) Theoretical basis for separation of multiple linked gene effects in mapping quantitative trait loci. Proc Natl Acad Sci 90:10972–10976

    Article  PubMed  CAS  Google Scholar 

  • Zeng ZB (1994) Precision mapping of quantitative trait loci. Genetics 136:1457–1468

    PubMed  CAS  Google Scholar 

  • Zhang Q, Sodmergen (2003) Cytological evidence for preservation of mitochondrial and plastid DNA in the mature generative cells of Chlorophytum spp. (Liliaceae). Protoplasma 221:211–216

    PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the USDA-ARS and the Ruth Dickie Scholarship from the University of Wisconsin

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Correspondence to Michael J. Havey.

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Communicated by C. Quiros.

Names are necessary to report factually on available data; however, the US Department of Agriculture (USDA) neither guarantees nor warrants the standard of the product, and the use of the name by USDA implies no approval of the product to the exclusion of others that may also be suitable.

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Calderon, C.I., Yandell, B.S. & Havey, M.J. Genetic mapping of paternal sorting of mitochondria in cucumber. Theor Appl Genet 125, 11–18 (2012). https://doi.org/10.1007/s00122-012-1812-z

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