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Exploiting synteny in Cucumis for mapping of Psm: a unique locus controlling paternal mitochondrial sorting

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Abstract

The three genomes of cucumber show different modes of transmission, nuclear DNA bi-parentally, plastid DNA maternally, and mitochondrial DNA paternally. The mosaic (MSC) phenotype of cucumber is associated with mitochondrial DNA rearrangements and is a valuable tool for studying mitochondrial transmission. A nuclear locus (Psm) has been identified in cucumber that controls sorting of paternally transmitted mitochondrial DNA. Comparative sequencing and mapping of cucumber and melon revealed extensive synteny on the recombinational and sequence levels near Psm and placed this locus on linkage group R of cucumber and G10 of melon. However, the cucumber genomic region near Psm was surprisingly monomorphic with an average of one SNP every 25 kb, requiring that a family from a more diverse cross is produced for fine mapping and eventual cloning of Psm. The cucumber ortholog of Arabidopsis mismatch repair (MSH1) was cloned and it segregated independently of Psm, revealing that this candidate gene is not Psm.

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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 

  • Abdelnoor R, Christensen A, Mohammed S, Munoz-Castillo B, Moriyama H, Mackenzie S (2006) Mitochondrial genome dynamics in plants and animals: convergent gene fusions of a MutS homologue. J Mol Evol 63:165–173

    Article  PubMed  CAS  Google Scholar 

  • Al-Faifi S (2007) Genetic analyses of mitochondrial transmission in cucumber. PhD Thesis, University of Wisconsin, Madison, pp. 102

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

    Article  PubMed  CAS  Google Scholar 

  • Bonierbale MW, Plaisted RL, Tanksley SD (1988) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103

    PubMed  Google Scholar 

  • Bradeen JM, Staub JE, Wye C, Antonise R, Peleman J (2001) Towards an expanded and integrated linkage map of cucumber (Cucumis sativus L.). Genome 44:111–119

    Article  PubMed  CAS  Google Scholar 

  • Cannon SB, Sterck L, Rombauts S, Sato S, Cheung F, Gouzy J, Wang X, Mudge J, Vasdewani J, Schiex T (2006) Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc Natl Acad Sci (USA) 103:14959–14964

    Article  CAS  Google Scholar 

  • Conley CA, Hanson MR (1995) How do alterations in plant mitochondrial genomes disrupt pollen development? J Bioenerg Biomemb 27:447–457

    Article  CAS  Google Scholar 

  • Danin-Poleg Y, Reis N, Baudracco-Arnas S, Pitrat M, Staub JE, Oliver M, Arus P, deVicente CM, Katzir N (2000) Simple sequence repeats in Cucumis mapping and map merging. Genome 43:963–974

    Google Scholar 

  • Devos KM, Gale MD (1997) Comparative genetics in the grasses. Plant Mol Biol 35:3–15

    Article  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 

  • Dirlewanger E, Cosson P, Howad W, Capdeville G, Bosselut N, Claverie M, Voisin R, Poizat C, Lafargue B, Baron O, Laigret F, Kleinhentz M, Arús P, Esmenjaud D (2004) Microsatellite genetic linkage maps of myrobalan plum and an almond-peach hybrid—location of root-knot nematode resistance genes. Theor Appl Genet 109:827–838

    Article  PubMed  CAS  Google Scholar 

  • Dominguez I, Graziano E, Gebhardt C, Barakat A, Berry S, Arus P, Delseny M, Barnes S (2003) Plant genome archaeology: evidence for conserved ancestral chromosome segments in dicotyledonous plant species. Plant Biotech J 1:91–99

    Article  CAS  Google Scholar 

  • Gonzalez-Ibeas D, Blanca J, Roig C, González-To M, Picó B, Truniger V, Gómez P, Deleu W, Caño-Delgado A, Arús A, Nuez F, Garcia-Mas J, Puigdomènech P, Aranda MA (2007) MELOGEN: an EST database for melon functional genomics. BMC Genomics 8:306

    Article  PubMed  Google Scholar 

  • Gonzalo M, Oliver M, Garcia-Mas J, Monfort A, Dolcet-Sanjuan R, Katzir N, Arús P, Monforte A (2005) Simple-sequence repeat markers used in merging linkage maps of melon (Cucumis melo L.). Theor Appl Genet 110:802–811

    Article  PubMed  CAS  Google Scholar 

  • Hanson MR (1991) Plant mitochondrial mutations and male sterility. Ann Rev Genet 25:461–486

    Article  PubMed  CAS  Google Scholar 

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

    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 

  • Howad W, Yamamoto T, Dirlewanger E, Testolin R, Cosson P, Cipriani G, Monforte AJ, Georgi L, Abbott AG, Arús P (2005) Mapping with a few plants: using selective mapping for microsatellite saturation of the Prunus reference map. Genetics 171:1305–1309

    Article  PubMed  CAS  Google Scholar 

  • Katzir N, Danin-Poleg Y, Tzuri G, Karchi Z, Lavi U, Cregan PB (1996) Length polymorphism and homologies of microsatellites in several Cucurbitaceae species. Theor Appl Genet 93:1282–1290

    Article  CAS  Google Scholar 

  • Kennard WC, Poetter K, Dijkhuizen A, Meglic V, Staub JE, Havey MJ (1994) Linkages among RFLP, RAPD, isozyme, disease resistance, and morphological markers in narrow and wide crosses of cucumber. Theor Appl Genet 89:42–48

    CAS  Google Scholar 

  • Ku HM, Liu J, Doganlar S, Tanksley SD (2001) Exploitation of Arabidopsis-tomato synteny to construct a high-resolution map of the ovate-containing region in tomato chromosome 2. Genome 44:470–475

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lorieux M, Perrier X, Goffinet B, Lanaud C, Gonzalez de Leon D (1995) Maximum-likelihood models for mapping genetic markers showing segregation distortion. 2. F2 populations. Theor Appl Genet 90:81–89

    Google Scholar 

  • Luo M, Wang Y-H, Frisch D, Joobeur T, Wing RA, Dean RA (2001) Melon bacterial artificial chromosome (BAC) library construction using improved methods and identification of clones linked to the locus conferring resistance to melon Fusarium wilt (Fom–2). Genome 44:154–162

    Article  PubMed  CAS  Google Scholar 

  • Lyttle TW (1991) Segregation distorters. Ann Rev Genet 25:511–557

    Article  PubMed  CAS  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, Cudmore JRH, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mammal Genome 12:930–932

    Article  CAS  Google Scholar 

  • Martin W, McCallum J, Shigyo M, Jakse J, Kuhl JC, Yamane N, Sink KC, Town CD, Havey MJ (2005) Genetic mapping of expressed sequences in onion and in silico comparisons show scant colinearity with rice. Mol Genet Genomics 274:197–204

    Article  PubMed  CAS  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 

  • Matsuura S (1995) Paternal inheritance of mitochondrial DNA in cucumber (Cucumis sativus L.). Rep Cucurbit Genet Coop 18:31–33

    Google Scholar 

  • Meyer JD, Deleu W, Garcia-Mas J, Havey MJ (2008) Construction of a fosmid library of cucumber (Cucumis sativus) and comparative analyses of the eIF4E and eIF(iso) 4E regions from cucumber and melon (Cucumis melo). Mol Genet Genomics 279:473–480

    Article  PubMed  CAS  Google Scholar 

  • Neuhausen SL (1992) Evaluation of restriction length polymorphism in Cucumis melo. Theor Appl Genet 83:379–384

    Article  Google Scholar 

  • Newton KJ, Coe EH (1986) Mitochondrial DNA changes in abnormal growth (nonchromosomal Stripe) mutants of maize. Proc Natl Acad Sci (USA) 83:7363–7366

    Article  CAS  Google Scholar 

  • Park YH, Sensoy S, Wye C, Antonise R, Peleman J, Havey MJ (2000) A genetic map of cucumber composed of RAPDs, RFLPs, AFLPs, and loci conditioning resistance to papaya ringspot and zucchini yellow mosaic viruses. Genome 43:1003–1010

    Article  PubMed  CAS  Google Scholar 

  • Park Y, Katzir N, Brotman Y, King J, Bertrand F, Havey M (2004) Comparative mapping of ZYMV resistances in cucumber (Cucumis sativus L.) and melon (Cucumis melo L.). Theor Appl Genet 109:707–712

    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 

  • Sakamoto W, Kondo H, Murata M, Motoyoshi F (1996) Altered mitochondrial gene expression in a maternal distorted leaf mutant of Arabidopsis induced by chloroplast mutator. Plant Cell 8:1377–1390

    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 

  • Yamato K, Newton K (1999) Heteroplasmy and homoplasmy for maize mitochondrial mutants: a rare homoplasmic nad4 deletion mutant plant. J Hered 90:369–373

    Article  Google Scholar 

  • Zamir D, Tadmor Y (1986) Unequal segregation of nuclear genes in plants. Bot Gaz 147:355–358

    Article  Google Scholar 

Download references

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Authors and Affiliations

  1. Department of Horticulture, University of Wisconsin, Madison, WI, 53706, USA

    Sulieman Al-Faifi & Jenelle D. F. Meyer

  2. Department of Plant Production, College of Food Sciences and Agriculture, King Saud University, PO Box 2460, Riyadh, 11451, Saudi Arabia

    Sulieman Al-Faifi

  3. Centre de Recerca en Agrigenòmica CSIC-IRTA-UAB, IRTA, Carretera de Cabrils Km 2, 08348, Cabrils (Barcelona), Spain

    Jordi Garcia-Mas & Antonio J. Monforte

  4. USDA/ARS, Department of Horticulture, University of Wisconsin, Madison, WI, 53706, USA

    Michael J. Havey

Authors
  1. Sulieman Al-Faifi
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  2. Jenelle D. F. Meyer
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  3. Jordi Garcia-Mas
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  4. Antonio J. Monforte
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  5. Michael J. Havey
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Corresponding author

Correspondence to Michael J. Havey.

Additional information

Communicated by R. Hagemann.

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. This work was supported by USDA-ARS and a graduate fellowship from King Saud University to SAF.

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Al-Faifi, S., Meyer, J.D.F., Garcia-Mas, J. et al. Exploiting synteny in Cucumis for mapping of Psm: a unique locus controlling paternal mitochondrial sorting. Theor Appl Genet 117, 523–529 (2008). https://doi.org/10.1007/s00122-008-0796-1

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  • DOI: https://doi.org/10.1007/s00122-008-0796-1

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