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

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Abstract

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.

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References

  • 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 25:3389–3402

    Article  Google Scholar 

  • 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 90:189–193

    Article  CAS  Google Scholar 

  • 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 91:195–199

    Article  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • 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 44:1469–1489

    Article  Google Scholar 

  • Cheng X, Zhang SZ (2010) Index to chromosome numbers of Chinese Pteridophyta (1969–2009). J Fairylake Bot Gard 9:1–58

    Article  Google Scholar 

  • 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 36:501–508

    Article  PubMed  CAS  Google Scholar 

  • Cousens MI, Lacey DG, Kelly EM (1985) Life history studies of ferns: a consideration of perspective. Proc Roy Soc Edinburgh 86B:371–380

    Google Scholar 

  • Crist KC, Farrar DR (1983) Ganetic load and long distance dispersal in Asplenium platyneuron. Can J Bot 61:1809–1814

    Article  Google Scholar 

  • Cryder CM, Corgan JN, Urquhart NS, Clason D (1991) Isozyme analysis of progeny derived from (Allium fistulosum × Allium cepa) × Allium cepa. Theor Appl Genet 82:337–345

    Article  Google Scholar 

  • 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 249:600–608

    Article  PubMed  CAS  Google Scholar 

  • Dobzhansky T (1936) Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21:113–135

    PubMed  CAS  Google Scholar 

  • 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 159:1701–1716

    Google Scholar 

  • Flinn KM (2006) Reproductive biology of three fern species may contribute of differential colonization success in post-agricultural forests. Am J Bot 93:1289–1294

    Article  PubMed  Google Scholar 

  • 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 83:49–57

    Article  Google Scholar 

  • 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 83:250–256

    Article  Google Scholar 

  • 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 6:857–863

    Article  Google Scholar 

  • Hall MC, Willis JH (2005) Transmission ratio distortion in intraspecific hybrids of Mimulus guttatus: implications for genomic divergence. Genetics 170:375–386

    Article  PubMed  CAS  Google Scholar 

  • 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 72:761–769

    Article  CAS  Google Scholar 

  • 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 34:437–447

    Article  Google Scholar 

  • Hirabayashi H (1963) Chromosome numbers in Japanese Osmunda. J Jap Bot 38:332–333

    Google Scholar 

  • Iwatsuki K (1992) Ferns and fern allies of Japan. Heibonsha, Tokyo

    Google Scholar 

  • 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 94:682–691

    Article  Google Scholar 

  • Klekowski EJ Jr (1968) Reproductive biology of the Pteridophyta. II. Theoretical considerations. Bot J Lin Soc 62:347–359

    Article  Google Scholar 

  • Klekowski EJ Jr (1969) Reproductive biology of the Pteridophyta. II. Theoretical considerations. Bot J Linn Soc 62:347–359

    Article  Google Scholar 

  • 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 63:153–169

    Article  Google Scholar 

  • Klekowski EJ Jr (1970b) Evidence against self-incompatibility and for genetic lethas in the fern Stenochalaena tenuifolia (Desv.) Moore. Bot J Linn Soc 63:171–176

    Article  Google Scholar 

  • Klekowski EJ Jr (1970c) Populational and genetic studies of a homosporous fern-Osmunda regalis. Am J Bot 57:1122–1138

    Article  Google Scholar 

  • Klekowski EJ Jr (1972) Evidence against genetic self-incompatibility in the homosporous fern Pteridium aquilinum. Evolution 26:66–73

    Article  Google Scholar 

  • Klekowski EJ Jr (1973) Genetic load in Osmunda regalis populations. Am J Bot 60:146–154

    Article  Google Scholar 

  • Knobloch IW (1976) Pteridophyte hybrids. Publ Mus Michigan State Univ Biol Ser 5:273–352

    Google Scholar 

  • Kosambi DD (1944) The estimation of map distances recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Kurita S (1963) Cytotaxonomical studies on some leptosporangiate ferns. J Coll Arts Sci Chiba Univ 4:43–52

    Google Scholar 

  • 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 101:669–676

    Article  CAS  Google Scholar 

  • 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 119:281–292

    Article  PubMed  CAS  Google Scholar 

  • 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 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Lavery P, James SH (1986) Complex hybridity in Isotoma petraea. VI. Distorted segregation, gametic lethal systems and population divergence. Heredity 58:401–408

    Article  Google Scholar 

  • 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 38:112–121

    Article  PubMed  CAS  Google Scholar 

  • Liedl BE, Anderson NO (1993) Reproductive barriers: identification, uses, and circumvention. Plant Breed Rev 11:11–154

    Google Scholar 

  • 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 84:812–818

    Google Scholar 

  • Lloyd RM (1974) Mating systems and genetic load in pioneer and non-pioneer Hawaiian Pteridophyta. Bot J Linn Soc 69:23–35

    Article  Google Scholar 

  • Lorieux M, Ndjiondjop MN, Ghesquiere A (2000) A first interspecific O. sativa × O. glaberrima microsatellite genetic linkage map. Theor Appl Genet 100:593–601

    CAS  Google Scholar 

  • 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 90:1144–1152

    Article  PubMed  Google Scholar 

  • Lövis JD (1977) Evolutionary patterns and processes in ferns. In: Preston RD, Woolhouse HW (eds) Advances in botanical research. Academic Press, London, pp 229–415

    Google Scholar 

  • Maekawa M, Kita F (1985) New gametophyte genes located in the third linkage group (Chromosome 3) of rice. Jpn J Breed 35:25–31

    Google Scholar 

  • Mangelsdorf PC, Jones DF (1926) The expression of mendelian factors in the gametophyte of maize. Genetics 11:423–455

    PubMed  CAS  Google Scholar 

  • 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 86:797–810

    Article  CAS  Google Scholar 

  • Mitui K (1968) Chromosomes and speciation in fern. Sci Rep Tokyo Kyoiku Daigaku Sec B 13:285–333

    Google Scholar 

  • Muller HJ (1939) Reversibility in evolution considered from the standpoint of genetics. Biol Rev 14:261–280

    Article  Google Scholar 

  • 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 177:1141–1150

    Article  PubMed  Google Scholar 

  • Nitsch JP (1951) Growth and development in vitro of excised ovaries. Am J Bot 38:566–576

    Article  CAS  Google Scholar 

  • Ottaviano E, Gorla MS, Pe E (1982) Male gametophytic selection in maize. Theor Appl Genet 63:249–254

    Article  Google Scholar 

  • 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 5:505–515

    Article  Google Scholar 

  • Pfahler PL (1967) Fertilization ability of maize pollen grains. II. Pollen genotype, female sporophyte and pollen storage interactions. Genetics 57:513–521

    PubMed  CAS  Google Scholar 

  • 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 115–124

    Google Scholar 

  • Philipp U, Wehling P, Wricke G (1994) A linkage map of rye. Theor Appl Genet 88:243–248

    Article  CAS  Google Scholar 

  • 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 91:1195–1202

    Article  CAS  Google Scholar 

  • 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 581–598

    Google Scholar 

  • Remington DL, O’malley DM (2000) Whole-genome characterization of embryonic stage inbreeding depression in a selfed loblolly pine family. Genetics 155:337–348

    PubMed  CAS  Google Scholar 

  • Sprague GF (1933) Pollen tube establishment and the deficiency of waxy seeds in certain maize crosses. Proc Natl Acad Sci USA 19:838–841

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

  • Takamiya M (1996) Index to chromosomes of Japanese Pteridophyta (1910–1996). Japan Pteridological Society, Tokyo

    Google Scholar 

  • Tanhuanpaa P, Kalendar R, Schulman AH, Kiviharju E (2008) The first doubled haploid linkage map for cultivated oat. Genome 51:560–569

    Article  PubMed  CAS  Google Scholar 

  • 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 165:1551–1568

    PubMed  CAS  Google Scholar 

  • Tsutsumi C, Matsumoto S, Yatabe-Kakugawa Y, Hirayama Y, Kato M (2011) A new allotetraploid species of Osmunda (Osmundaceae). Syst Bot 36:836–844

    Article  Google Scholar 

  • 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 10:280

    Article  PubMed  Google Scholar 

  • 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 81:613–620

    Article  CAS  Google Scholar 

  • 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 211–219

    Google Scholar 

  • Watano Y (1988) High levels of genetic divergence among populations in a weedy fern, Pteris multifida Poir. Plant Species Biol 3:109–115

    Article  Google Scholar 

  • 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 253:535–545

    Google Scholar 

  • 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 71:31–41

    Article  Google Scholar 

  • 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 122:585–595

    Article  PubMed  CAS  Google Scholar 

  • 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 124:265–268

    Article  PubMed  Google Scholar 

  • 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 109:451–463

    Article  PubMed  CAS  Google Scholar 

  • Zamir D, Tanksley SD, Jones RA (1982) Haploid selection for low temperature tolerance of tomato pollen. Genetics 101:129–137

    PubMed  CAS  Google Scholar 

  • 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 83:919–924

    Google Scholar 

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Acknowledgments

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.

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Correspondence to Yoko Yatabe-Kakugawa.

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Y. Yatabe-Kakugawa is the recipient of the BSJ Award for Young Scientist, 2011.

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Yatabe-Kakugawa, Y., Tsutsumi, C., Hirayama, Y. et al. Transmission ratio distortion of molecular markers in a doubled haploid population originated from a natural hybrid between Osmunda japonica and O. lancea . J Plant Res 126, 469–482 (2013). https://doi.org/10.1007/s10265-012-0540-4

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