Theoretical and Applied Genetics

, Volume 117, Issue 4, pp 523–529 | Cite as

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

  • Sulieman Al-Faifi
  • Jenelle D. F. Meyer
  • Jordi Garcia-Mas
  • Antonio J. Monforte
  • Michael J. HaveyEmail author
Original Paper


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.


Single Nucleotide Polymorphism Linkage Group Melon Simple Sequence Repeat Marker Plant Introduction 
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  1. 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) 100:5968–5973CrossRefGoogle Scholar
  2. 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 63:165–173PubMedCrossRefGoogle Scholar
  3. Al-Faifi S (2007) Genetic analyses of mitochondrial transmission in cucumber. PhD Thesis, University of Wisconsin, Madison, pp. 102Google Scholar
  4. Bartoszewski G, Malepszy S, Havey M (2004) Mosaic (MSC) cucumbers regenerated from independent cell cultures possess different mitochondrial rearrangements. Curr Genet 45:45–53PubMedCrossRefGoogle Scholar
  5. 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 120:1095–1103PubMedGoogle Scholar
  6. Bradeen JM, Staub JE, Wye C, Antonise R, Peleman J (2001) Towards an expanded and integrated linkage map of cucumber (Cucumis sativus L.). Genome 44:111–119PubMedCrossRefGoogle Scholar
  7. 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) 103:14959–14964CrossRefGoogle Scholar
  8. Conley CA, Hanson MR (1995) How do alterations in plant mitochondrial genomes disrupt pollen development? J Bioenerg Biomemb 27:447–457CrossRefGoogle Scholar
  9. 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 43:963–974Google Scholar
  10. Devos KM, Gale MD (1997) Comparative genetics in the grasses. Plant Mol Biol 35:3–15PubMedCrossRefGoogle Scholar
  11. Dijkhuizen A, Kennard WC, Havey MJ, Staub JE (1996) RFLP variation and genetic relationships in cultivated cucumber. Euphytica 90:79–87Google Scholar
  12. 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 109:827–838PubMedCrossRefGoogle Scholar
  13. 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 1:91–99CrossRefGoogle Scholar
  14. 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 8:306PubMedCrossRefGoogle Scholar
  15. 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 110:802–811PubMedCrossRefGoogle Scholar
  16. Hanson MR (1991) Plant mitochondrial mutations and male sterility. Ann Rev Genet 25:461–486PubMedCrossRefGoogle Scholar
  17. Havey MJ (1997) Predominant paternal transmission of the mitochondrial genome in cucumber. J Hered 88:232–235Google Scholar
  18. Havey MJ, Park YH, Bartoszewski G (2004) The Psm locus controls paternal sorting of the cucumber mitochondrial genome. J Hered 95:492–497PubMedCrossRefGoogle Scholar
  19. 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 171:1305–1309PubMedCrossRefGoogle Scholar
  20. 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 93:1282–1290CrossRefGoogle Scholar
  21. 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 89:42–48Google Scholar
  22. 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 44:470–475PubMedCrossRefGoogle Scholar
  23. Lilly JW, Bartoszewski G, Malepszy S, Havey MJ (2001) A major deletion in the cucumber mitochondrial genome sorts with the MSC phenotype. Curr Genet 40:144–151PubMedCrossRefGoogle Scholar
  24. 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 90:81–89Google Scholar
  25. 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 44:154–162PubMedCrossRefGoogle Scholar
  26. Lyttle TW (1991) Segregation distorters. Ann Rev Genet 25:511–557PubMedCrossRefGoogle Scholar
  27. Malepszy S, Burza W, Smiech M (1996) Characterization of a cucumber (Cucumis sativus L.) somaclonal variant with paternal inheritance. J Appl Genet 37:65–78Google Scholar
  28. Manly KF, Cudmore JRH, Meer JM (2001) Map Manager QTX, cross-platform software for genetic mapping. Mammal Genome 12:930–932CrossRefGoogle Scholar
  29. 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 274:197–204PubMedCrossRefGoogle Scholar
  30. Martinez-Zapater JM, Gil P, Capel J, Somerville CR (1992) Mutations at the Arabidopsis CHM locus promote rearrangements of the mitochondrial genome. Plant Cell 4:889–899PubMedCrossRefGoogle Scholar
  31. Matsuura S (1995) Paternal inheritance of mitochondrial DNA in cucumber (Cucumis sativus L.). Rep Cucurbit Genet Coop 18:31–33Google Scholar
  32. 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 279:473–480PubMedCrossRefGoogle Scholar
  33. Neuhausen SL (1992) Evaluation of restriction length polymorphism in Cucumis melo. Theor Appl Genet 83:379–384CrossRefGoogle Scholar
  34. Newton KJ, Coe EH (1986) Mitochondrial DNA changes in abnormal growth (nonchromosomal Stripe) mutants of maize. Proc Natl Acad Sci (USA) 83:7363–7366CrossRefGoogle Scholar
  35. 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 43:1003–1010PubMedCrossRefGoogle Scholar
  36. 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 109:707–712PubMedCrossRefGoogle Scholar
  37. Pierce LK, Wehner TC (1990) Review of genes and linkage groups in cucumber. HortScience 25:605–615Google Scholar
  38. 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 8:1377–1390PubMedCrossRefGoogle Scholar
  39. Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19:1251–1264PubMedCrossRefGoogle Scholar
  40. Yamato K, Newton K (1999) Heteroplasmy and homoplasmy for maize mitochondrial mutants: a rare homoplasmic nad4 deletion mutant plant. J Hered 90:369–373CrossRefGoogle Scholar
  41. Zamir D, Tadmor Y (1986) Unequal segregation of nuclear genes in plants. Bot Gaz 147:355–358CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Sulieman Al-Faifi
    • 1
    • 2
  • Jenelle D. F. Meyer
    • 1
  • Jordi Garcia-Mas
    • 3
  • Antonio J. Monforte
    • 3
  • Michael J. Havey
    • 4
    Email author
  1. 1.Department of HorticultureUniversity of WisconsinMadisonUSA
  2. 2.Department of Plant ProductionCollege of Food Sciences and Agriculture, King Saud UniversityRiyadhSaudi Arabia
  3. 3.Centre de Recerca en Agrigenòmica CSIC-IRTA-UABIRTACabrils (Barcelona)Spain
  4. 4.USDA/ARS, Department of HorticultureUniversity of WisconsinMadisonUSA

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