Journal of Plant Research

, Volume 126, Issue 4, pp 469–482 | Cite as

Transmission ratio distortion of molecular markers in a doubled haploid population originated from a natural hybrid between Osmunda japonica and O. lancea

  • Yoko Yatabe-KakugawaEmail author
  • Chie Tsutsumi
  • Yumiko Hirayama
  • Shizuka Tsuneki
  • Noriaki Murakami
  • Masahiro Kato
Regular paper


In ferns, intra-gametophytic selfing occurs as a mode of reproduction where two gametes from the same gametophyte form a completely homozygous sporophyte. Intra-gametophytic selfing is considered to be prevented by lethal or deleterious recessive genes in several diploid species. In order to investigate the modes and tempo of selection acting different developmental stages, doubled haploids obtained from intra-gametophytic selfing within isolated gametophytes of a putative F1 hybrid between Osmunda japonica and O. lancea were analyzed with EST_derived molecular markers, and the distribution pattern of transmission ratio distortion (TRD) along linkage map was clarified. As the results, the markers with skewness were clustered in two linkage groups. For the two highly distorted regions, gametophytes and F2 population were also examined. The markers skewed towards O. japonica on a linkage group (LG_2) showed skewness also in gametophytes, and the TRD was generated in the process of spore formation or growth of gametophytes. Also, selection appeared to be operating in the gametophytic stage. The markers on other linkage group (LG_11) showed highest skewness towards O. lancea in doubled haploids, and it was suggested that the segregation of LG_11 were influenced by zygotic lethality or genotypic evaluation and that some deleterious recessive genes exist in LG_11 and reduce the viability of homozygotes with O. japonica alleles. It is very likely that a region of LG_11were responsible for the low frequencies of intra-gametophytic selfing in O. japonica.


Intra-gametophytic selfing Inbreeding depression Doubled haploid Osmunda Transmission ratio distortion 



We thank S. Matsumoto and W. Shinohara for assistance with the cultivation of materials. This study was supported by Grants-in-Aid number 20247006 to M.K. from the Japan Society for the Promotion of Science, research grant to Y.Y. from the Asahi Glass Foundation and that from the New Technology Development Foundation.

Supplementary material

10265_2012_540_MOESM1_ESM.docx (68 kb)
Supplementary material 1 (DOCX 74 kb)


  1. Altshul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z (1997) Gapped Blast and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefGoogle Scholar
  2. Barzen E, Mechelke W, Ritter E, Schultekappert E, Salamini F (1995) An extended map of the sugar-beet genome containing RFLP and RAPD loci. Theor Appl Genet 90:189–193CrossRefGoogle Scholar
  3. Berry ST, Leon AJ, Hanfrey CC, Challis P, Burkholz A, Barnes SR, Rufener GK, Lee M, Caligari PDS (1995) Molecular marker analysis of Helianthus annuus L. 2. Construction of an RFLP linkage map for cultivated sunflower. Theor Appl Genet 91:195–199CrossRefGoogle Scholar
  4. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268CrossRefGoogle Scholar
  5. Charlesworth DMT, Morgan MT, Charlesworth B (1990) Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multi-locus system with no linkage. Evolution 44:1469–1489CrossRefGoogle Scholar
  6. Cheng X, Zhang SZ (2010) Index to chromosome numbers of Chinese Pteridophyta (1969–2009). J Fairylake Bot Gard 9:1–58CrossRefGoogle Scholar
  7. Cheng Y, Geng JF, Zhang JY, Wang Q, Ban QY, Hou X (2009) The construction of a genetic linkage map of non-heading Chinese cabbage (Brassica campestris ssp chinensis Makino). J Genet Genomics 36:501–508PubMedCrossRefGoogle Scholar
  8. Cousens MI, Lacey DG, Kelly EM (1985) Life history studies of ferns: a consideration of perspective. Proc Roy Soc Edinburgh 86B:371–380Google Scholar
  9. Crist KC, Farrar DR (1983) Ganetic load and long distance dispersal in Asplenium platyneuron. Can J Bot 61:1809–1814CrossRefGoogle Scholar
  10. Cryder CM, Corgan JN, Urquhart NS, Clason D (1991) Isozyme analysis of progeny derived from (Allium fistulosum × Allium cepa) × Allium cepa. Theor Appl Genet 82:337–345CrossRefGoogle Scholar
  11. Devaux P, Kilian A, Kleinhofs A (1995) Comparative mapping of the barley genome with male and female recombination-derived, doubled haploid populations. Mol Gen Genet 249:600–608PubMedCrossRefGoogle Scholar
  12. Dobzhansky T (1936) Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21:113–135PubMedGoogle Scholar
  13. Fisherman L, Kelly AJ, Morgan E, Willis JH (2001) A genetic map in the Mimulus guttatus species complex reveals transmission ration distortion due to heterospecific interactions. Genetics 159:1701–1716Google Scholar
  14. Flinn KM (2006) Reproductive biology of three fern species may contribute of differential colonization success in post-agricultural forests. Am J Bot 93:1289–1294PubMedCrossRefGoogle Scholar
  15. Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schachtschabel U, Kaufmann H, Thompson RD, Bonierbale MW, Ganal MW, Tanksley SD, Salamini F (1991) RFLP maps of potato and their alignment with the homoeologous tomato genome. Theor Appl Genet 83:49–57CrossRefGoogle Scholar
  16. Graner A, Jahoor A, Schondelmaier J, Siedler H, Pillen K, Fischbeck G, Wenzel G, Hermann RG (1991) Construction of an RFLP map of barley. Theor Appl Genet 83:250–256CrossRefGoogle Scholar
  17. Gubler M, Park SM, Jetten M, Stephanopoulos G, Sinskey AJ (1994) Effects of phosphoenol pyruvate-carboxylase deficiency on metabolism and lysine productionin corynebacterium-glutamicum. Appl Microbial Biotechnol 6:857–863CrossRefGoogle Scholar
  18. Hall MC, Willis JH (2005) Transmission ratio distortion in intraspecific hybrids of Mimulus guttatus: implications for genomic divergence. Genetics 170:375–386PubMedCrossRefGoogle Scholar
  19. Helentjaris T, Slocum M, Wright S, Schaefer A, Nienhuis J (1986) Construction of genetic-linkage maps in maize and tomato using restriction-fragment-length-polymorphism. Theor Appl Genet 72:761–769CrossRefGoogle Scholar
  20. Heun M, Kennedy AE, Anderson JA, Lapitan NLV, Sorrells ME, Tanksley SD (1991) A construction of a restriction-fragment-length-polymorphism map for barley (Hordeum vulgare). Genome 34:437–447CrossRefGoogle Scholar
  21. Hirabayashi H (1963) Chromosome numbers in Japanese Osmunda. J Jap Bot 38:332–333Google Scholar
  22. Iwatsuki K (1992) Ferns and fern allies of Japan. Heibonsha, TokyoGoogle Scholar
  23. Jenczewski E, Gherardi M, Bonnin I, Prosperi JJ, Olivieri I, Huguet T (1997) Insight on segregation distortions in two intraspecific crosses between annual species of Medicago (Leguminosae). Theor Appl Genet 94:682–691CrossRefGoogle Scholar
  24. Klekowski EJ Jr (1968) Reproductive biology of the Pteridophyta. II. Theoretical considerations. Bot J Lin Soc 62:347–359CrossRefGoogle Scholar
  25. Klekowski EJ Jr (1969) Reproductive biology of the Pteridophyta. II. Theoretical considerations. Bot J Linn Soc 62:347–359CrossRefGoogle Scholar
  26. Klekowski EJ Jr (1970a) Reproductive biology of the Pteridophyta IV. An experimental study of mating system in Ceratopteris thalictroides (L.) Brongn. Bot J Linn Soc 63:153–169CrossRefGoogle Scholar
  27. Klekowski EJ Jr (1970b) Evidence against self-incompatibility and for genetic lethas in the fern Stenochalaena tenuifolia (Desv.) Moore. Bot J Linn Soc 63:171–176CrossRefGoogle Scholar
  28. Klekowski EJ Jr (1970c) Populational and genetic studies of a homosporous fern-Osmunda regalis. Am J Bot 57:1122–1138CrossRefGoogle Scholar
  29. Klekowski EJ Jr (1972) Evidence against genetic self-incompatibility in the homosporous fern Pteridium aquilinum. Evolution 26:66–73CrossRefGoogle Scholar
  30. Klekowski EJ Jr (1973) Genetic load in Osmunda regalis populations. Am J Bot 60:146–154CrossRefGoogle Scholar
  31. Knobloch IW (1976) Pteridophyte hybrids. Publ Mus Michigan State Univ Biol Ser 5:273–352Google Scholar
  32. Kosambi DD (1944) The estimation of map distances recombination values. Ann Eugen 12:172–175Google Scholar
  33. Kurita S (1963) Cytotaxonomical studies on some leptosporangiate ferns. J Coll Arts Sci Chiba Univ 4:43–52Google Scholar
  34. Ky CL, Barre P, Lorieux M, Trouslot P, Akaffou S, Louarn J, Charrier A, Hamon S, Noirot M (2000) Interspecific genetic linkage map, segregation distortion and genetic conversion in coffee (Coffea sp.). Theor Appl Genet 101:669–676CrossRefGoogle Scholar
  35. Lacape JM, Jacobs J, Arioli T, Derijcker R, Forestier-Chiron N, Llewellyn D, Jean J, Thomas E, Viot C (2009) A new interspecific, Gossypium hirsutum × G. barbadense, RIL population: towards a unified consensus linkage map of tetraploid cotton. Theor Appl Genet 119:281–292PubMedCrossRefGoogle Scholar
  36. Lander ES, Greene P, Abrahamson J, Barrow A, Dally MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedCrossRefGoogle Scholar
  37. Lavery P, James SH (1986) Complex hybridity in Isotoma petraea. VI. Distorted segregation, gametic lethal systems and population divergence. Heredity 58:401–408CrossRefGoogle Scholar
  38. Lefebvre V, Palloix A, Caranta C, Pochard E (1995) Construction of an intraspecific integrated linkage map of pepper using molecular markers and doubled-haploid progenies. Genome 38:112–121PubMedCrossRefGoogle Scholar
  39. Liedl BE, Anderson NO (1993) Reproductive barriers: identification, uses, and circumvention. Plant Breed Rev 11:11–154Google Scholar
  40. Lin SY, Ikebashi H, Yanagihara S, Kawashima A (1992) Segregation distortion via male gametes in hybrids between Indica and Japonica or wide-compatibilities of rice (Oryza sativa L). Theor Appl Genet 84:812–818Google Scholar
  41. Lloyd RM (1974) Mating systems and genetic load in pioneer and non-pioneer Hawaiian Pteridophyta. Bot J Linn Soc 69:23–35CrossRefGoogle Scholar
  42. Lorieux M, Ndjiondjop MN, Ghesquiere A (2000) A first interspecific O. sativa × O. glaberrima microsatellite genetic linkage map. Theor Appl Genet 100:593–601Google Scholar
  43. Lott MS, Volin JC, Pemberton RW, Austin DF (2003) The reproductive biology of the invasive ferns Lygodium microphyllum and L. japonicum (Schizaeaceae): implications for invasive potential. Am J Bot 90:1144–1152PubMedCrossRefGoogle Scholar
  44. Lövis JD (1977) Evolutionary patterns and processes in ferns. In: Preston RD, Woolhouse HW (eds) Advances in botanical research. Academic Press, London, pp 229–415Google Scholar
  45. Maekawa M, Kita F (1985) New gametophyte genes located in the third linkage group (Chromosome 3) of rice. Jpn J Breed 35:25–31Google Scholar
  46. Mangelsdorf PC, Jones DF (1926) The expression of mendelian factors in the gametophyte of maize. Genetics 11:423–455PubMedGoogle Scholar
  47. Menancio-Hautea D, Fatokun CA, Kumar L, Danesh D, Young ND (1993) Comparative genome analysis of mungbean (Vigna radiata L. Wilczek) and cowpea (V. unguiculata L. Walpers) using RFLP mapping data. Theor Appl Genet 86:797–810CrossRefGoogle Scholar
  48. Mitui K (1968) Chromosomes and speciation in fern. Sci Rep Tokyo Kyoiku Daigaku Sec B 13:285–333Google Scholar
  49. Muller HJ (1939) Reversibility in evolution considered from the standpoint of genetics. Biol Rev 14:261–280CrossRefGoogle Scholar
  50. Nakazato T, Jung M, Housworth EA, Rieseberg LH, Gastony GJ (2007) A genomewide study of reproductive barriers between allopatric populations of a homosporous fern, Ceratopteris richardii. Genetics 177:1141–1150PubMedCrossRefGoogle Scholar
  51. Nitsch JP (1951) Growth and development in vitro of excised ovaries. Am J Bot 38:566–576CrossRefGoogle Scholar
  52. Ottaviano E, Gorla MS, Pe E (1982) Male gametophytic selection in maize. Theor Appl Genet 63:249–254CrossRefGoogle Scholar
  53. Pakull B, Groppe K, Meyer M, Markussen T, Fladung M (2009) Genetic linkage mapping in aspen (Populus tremula L. and Populus tremuloides Michx.). Tree Genet Genomes 5:505–515CrossRefGoogle Scholar
  54. Pfahler PL (1967) Fertilization ability of maize pollen grains. II. Pollen genotype, female sporophyte and pollen storage interactions. Genetics 57:513–521PubMedGoogle Scholar
  55. Pfahler PL (1975) Factors affecting male transmission in maize (Zea mays L.). In: Mulcahy DL (ed) Gamete competition in plants and animals. Elsevier, New York, pp 115–124Google Scholar
  56. Philipp U, Wehling P, Wricke G (1994) A linkage map of rye. Theor Appl Genet 88:243–248CrossRefGoogle Scholar
  57. Quillet MC, Madjidian N, Griveau Y, Serieys H, Tersac M, Lorieux M, Bervillé A (1995) Mapping genetic factors controlling pollen viability in an interspecific cross in Helianthus sect. Helianthus. Theor Appl Genet 91:1195–1202CrossRefGoogle Scholar
  58. Ranker TA, Gemmill CEC, Trapp PG, Hambleton A, Ha K (1996) Population genetics and reproductive biology of lava-flow colonizing species of Hawaiian Sadleria (Blechnaceae). In: Camus JM, Gibby M, John RJ (eds) Pteriodology in perspecitive. Royal Botanic Gardens, Kew, pp 581–598Google Scholar
  59. Remington DL, O’malley DM (2000) Whole-genome characterization of embryonic stage inbreeding depression in a selfed loblolly pine family. Genetics 155:337–348PubMedGoogle Scholar
  60. Sprague GF (1933) Pollen tube establishment and the deficiency of waxy seeds in certain maize crosses. Proc Natl Acad Sci USA 19:838–841PubMedCrossRefGoogle Scholar
  61. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, SunderlandGoogle Scholar
  62. Takamiya M (1996) Index to chromosomes of Japanese Pteridophyta (1910–1996). Japan Pteridological Society, TokyoGoogle Scholar
  63. Tanhuanpaa P, Kalendar R, Schulman AH, Kiviharju E (2008) The first doubled haploid linkage map for cultivated oat. Genome 51:560–569PubMedCrossRefGoogle Scholar
  64. Tani N, Takahashi T, Iwata H, Mukai Y, Ujino-Ihara T (2003) A consensus linkage map for sugi (Cryptomeria japonica) from two pedigrees, based on microsatellites and expressed sequence tags. Genetics 165:1551–1568PubMedGoogle Scholar
  65. Tsutsumi C, Matsumoto S, Yatabe-Kakugawa Y, Hirayama Y, Kato M (2011) A new allotetraploid species of Osmunda (Osmundaceae). Syst Bot 36:836–844CrossRefGoogle Scholar
  66. Tunio SA, Oldfield NJ, Ala’Aldeen DA, Wooldridge KG, Turner DPJ (2010) The role of glyceraldehyde 3-phosphate dehydrogenase (GapA-1) in Neisseria meningitides adherence to human cells. BMC Microbiol 10:280PubMedCrossRefGoogle Scholar
  67. Virk PS, Ford-Lloyd BV, Newbury HJ (1998) Mapping AFLP markers associated with subspecific differentiation of Oryza sativa (rice) and an investigation of segregation distortion. Heredity 81:613–620CrossRefGoogle Scholar
  68. Watano Y (1986) Genetic life history of the homosporous fern Osmunda lancea. In: Iwatsuki K, Raven PH, Bock WJ (eds) Modern aspects of species. Univ Tokyo Press, Tokyo, pp 211–219Google Scholar
  69. Watano Y (1988) High levels of genetic divergence among populations in a weedy fern, Pteris multifida Poir. Plant Species Biol 3:109–115CrossRefGoogle Scholar
  70. Xu Y, Zhu L, Xiao J, Huang N, McCouch SR (1997) Chromosomal regions associated with segregation distortion of molecular markers in F2, backcross, doubled haploid, and recombinant inbred populations in rice (Oryza sativa L.). Mol Gen Genet 253:535–545Google Scholar
  71. Yamagishi M, Yano M, Fukuta Y, Fukui K, Otani M, Shimada T (1996) Distorted segregation of RFLP markers in regenerated plants derived from anther culture of an F1 hybrid of rice. Genes Genet Syst 71:31–41CrossRefGoogle Scholar
  72. Yatabe Y, Tsutsumi C, Hirayama Y, Mori K, Murakami N, Kato M (2009) Genetic population structure of Osmunda japonica, rheophilous Osmunda lancea and their hybrids. J Plant Res 122:585–595PubMedCrossRefGoogle Scholar
  73. Yatabe Y, Yamamoto K, Tsutsumi C, Shinohara W, Murakami N, Kato M (2010) Fertility and precocity of Osmunda × intermedia offspring in culture. J Plant Res 124:265–268PubMedCrossRefGoogle Scholar
  74. Yin TM, DiFazio SP, Gunter LE, Riemenschneider D, Tuskan GA (2004) Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor Appl Genet 109:451–463PubMedCrossRefGoogle Scholar
  75. Zamir D, Tanksley SD, Jones RA (1982) Haploid selection for low temperature tolerance of tomato pollen. Genetics 101:129–137PubMedGoogle Scholar
  76. Zivy M, Devaux P, Blaisonneau J, Jean R, Thiellement H (1992) Segregation distortion and linkage studies in microspore-derived double haploid lines of Hordeum vulgare L. Theor Appl Genet 83:919–924Google Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2012

Authors and Affiliations

  • Yoko Yatabe-Kakugawa
    • 1
    Email author
  • Chie Tsutsumi
    • 2
  • Yumiko Hirayama
    • 2
  • Shizuka Tsuneki
    • 3
  • Noriaki Murakami
    • 3
  • Masahiro Kato
    • 2
  1. 1.Botanical Gardens, Graduate School of ScienceThe University of TokyoTokyoJapan
  2. 2.Department of BotanyNational Museum of Nature and ScienceTsukubaJapan
  3. 3.Makino Herbarium, Tokyo Metropolitan UniversityHachiojiJapan

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