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Molecular phylogeny of the genus Asparagus (Asparagaceae) explains interspecific crossability between the garden asparagus (A. officinalis) and other Asparagus species

Abstract

The genus Asparagus comprises approximately 200 species, some of which are commercially cultivated, such as the garden asparagus (A. officinalis). Many Asparagus species, including A. officinalis, are dioecious and have been grouped into a subgenus distinct from that of hermaphroditic species. Although many interspecific crossings have been attempted to introduce useful traits into A. officinalis, only some of the dioecious species were found to be cross-compatible with A. officinalis. Here, molecular phylogenetic analyses were conducted to determine whether interspecific crossability is proportional to the genetic distance between the crossing pairs and to further clarify the evolutionary history of the Asparagus genus. A clade with all cross-compatible species and no cross-incompatible species was recovered in the phylogenetic tree based on analyses of non-coding cpDNA regions. In addition, a sex-linked marker developed for A. officinalis amplified a male-specific region in all cross-compatible species. The phylogenetic analyses also provided some insights about the evolutionary history of Asparagus; for example, by indicating that the genus had its origin in southern Africa, subsequently spreading throughout the old world through intensive speciation and dispersal. The results also suggest that dioecious species were derived from a single evolutionary transition from hermaphroditism in Asparagus. These findings not only contribute towards the understanding of the evolutionary history of the genus but may also facilitate future interspecific hybridization programs involving Asparagus species.

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References

  • Ahmad M, McNeil DL (1996) Comparison of crossability, RAPD, SDS-PAGE and morphological markers for revealing genetic relationships within and among Lens species. Theor Appl Genet 93:788–793

    Article  CAS  Google Scholar 

  • Alberti P, Casali PE, Barbaglio E et al (2004) Interspecific hybridization for Asparagus breeding. In: Proceedings of the XLVIII Italian Society of Agricultural Genetics–SIFV-SIGA Joint Meeting. Lecce, Italy

  • APG III (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121

    Article  Google Scholar 

  • Barnea A, Yom-Tov Y, Friedman J (1991) Does ingestion by birds affect seed germination? Funct Ecol 5:394–402

    Article  Google Scholar 

  • Barrett SCH (2002) Evolution of sex: the evolution of plant sexual diversity. Nat Rev Genet 3:274–284

    PubMed  Article  CAS  Google Scholar 

  • Bawa KS (1980) Evolution of dioecy in flowering plants. Ann Rev Ecol Syst 11:15–39

    Article  Google Scholar 

  • Bracale M, Caporali E, Galli MG et al (1991) Sex determination and differentiation in Asparagus officinalis L. Plant Sci 80:67–77

    Article  CAS  Google Scholar 

  • Burk LG (1967) An interspecific bridge-cross: Nicotiana repanda through N. sylvestris to N. tabacum. J Hered 58:215–218

    Google Scholar 

  • Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997

    Article  Google Scholar 

  • Chen L, Zhou Z-X, Yang Y-J (2007) Genetic improvement and breeding of tea plant (Camellia sinensis) in China: from individual selection to hybridization and molecular breeding. Euphytica 154:239–248

    Article  CAS  Google Scholar 

  • Clifford HT, Conran JG (1987) Asparagaceae. In: George AS (ed) Flora of Australia. Australian Government Publishing Service, Canberra, pp 140–142

    Google Scholar 

  • Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381

    Article  Google Scholar 

  • Coyne JA, Orr HA (1996) “Patterns of speciation in Drosophila” revised. Evolution 51:295–303

    Article  Google Scholar 

  • Crow JF (1998) 90 years ago: the beginning of hybrid maize. Genetics 148:923–928

    PubMed  CAS  Google Scholar 

  • Dahlgren RMT, Clifford HT, Yeo PF (1985) The families of the monocotyledons. Springer, Heidelberg

    Book  Google Scholar 

  • Darwin C (1877) Different forms of flowers on plants of the same species. John Murray, London

    Book  Google Scholar 

  • Dehgan B (1984) Phylogenetic significance of interspecific hybridization in Jatropha (Euphorbiaceae). Syst Bot 9:467–478

    Article  Google Scholar 

  • Desfeux C, Maurice S, Henry J-P et al (1996) Evolution of reproductive systems in the genus Silene. Proc R Soc Lond B 263:409–414

    Article  CAS  Google Scholar 

  • Ernst M, Krug H (1998) Seasonal growth and development of asparagus (Asparagus officinalis L.). III. The effect of temperature and water stress on carbohydrate content in storage roots and rhizome buds. Gartenbauwissenschaft 63:202–208

    CAS  Google Scholar 

  • Fukuda T, Ashizawa H, Suzuki R et al (2005) Molecular phylogeny of the genus Asparagus (Asparagaceae) inferred from plastic petB intron and petD-rpoA intergenic spacer sequences. Plant Species Biol 20:121–132

    Article  Google Scholar 

  • Galli MG, Bracale M, Falavigna A et al (1993) Different kinds of male flowers in the dioecious plant Asparagus officinalis L. Sex Plant Reprod 6:16–21

    Article  Google Scholar 

  • Gill GP, Harvey CF, Gardner RC et al (1998) Development of sex-linked PCR markers for gender identification in Actinidia. Theor Appl Genet 97:439–445

    Article  CAS  Google Scholar 

  • Guindon S, Dufayard J-F, Lefort V et al (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    PubMed  Article  CAS  Google Scholar 

  • He CY, Hsiang T, Wolyn DJ (2002) Induction of systemic disease resistance and pathogen defence responses in Asparagus officinalis inoculated with nonpathogenic strains of Fusarium oxysporum. Plant Pathol 51:225–230

    Article  Google Scholar 

  • Ito T, Suzuki G, Ochiai T et al (2005) Genomic organization of the AODEF gene in Asparagus officinalis L. Genes Genet Syst 80:95–103

    PubMed  Article  CAS  Google Scholar 

  • Ito T, Ochiai T, Ashizawa H et al (2007) Production and analysis of reciprocal hybrids between Asparagus officinalis L. and A. schoberioides Kunth. Genet Resour Crop Evol 54:1063–1071

    Article  Google Scholar 

  • Ito T, Ochiai T, Fukuda T et al (2008) Potential of interspecific hybrids in Asparagaceae. Acta Hortic 776:279–284

    CAS  Google Scholar 

  • Jakse J, Štajner N, Kozjak P et al (2008) Trinucleotide microsatellite repeat is tightly linked to male sex in hop (Humulus lupulus L.). Mol Breed 21:139–148

    Article  CAS  Google Scholar 

  • Jamsari A, Nits I, Reamon-Büttner SM et al (2004) BAC-derived diagnostic markers for sex determination in asparagus. Theor Appl Genet 108:1140–1146

    PubMed  Article  CAS  Google Scholar 

  • Jansky S, Hamernik A (2009) The introgression of 2× 1EBN Solanum species into the cultivated potato using Solanum verrucosum as a bridge. Genet Resour Crop Evol 56:1107–1115

    Article  Google Scholar 

  • Khrustaleva LI, Kik C (1998) Cytogenetical studies in the bridge cross Allium cepa × (A. fistulosum × A. roylei). Theor Appl Genet 96:8–14

    Article  Google Scholar 

  • Kubitzki K, Rudall PJ (1998) Asparagaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 3. Springer, Heidelberg, pp 125–128

    Google Scholar 

  • Kunitake H, Nakashima T, Mori K et al (1996) Production of interspecific somatic hybrid plants between Asparagus officinalis and A. macowanii through electrofusion. Plant Sci 116:213–222

    Article  CAS  Google Scholar 

  • Lawrie SL (2006) The ecology of bridal veil (Asparagus declinatus L.) in South Australia. Plant Prot Q 21:99–100

    Google Scholar 

  • Lee Y-O, Kanno A, Kameya T (1997) Phylogenetic relationships in the genus Asparagus based on the restriction enzyme analysis of the chloroplast DNA. Breed Sci 47:375–378

    CAS  Google Scholar 

  • Liu Y, Chen H, Zhuang D et al (2010) Characterization of a DRE-binding transcription factor from asparagus (Asparagus officinalis L.) and its overexpression in Arabidopsis resulting in salt- and drought-resistant transgenic plants. Int J Plant Sci 171:12–23

    Article  CAS  Google Scholar 

  • Lloyd DG (1975) The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45:325–339

    Article  Google Scholar 

  • Löptien H (1979) Identification of the sex chromosome pair in asparagus (Asparagus officinalis L.). Z. Pflanzenzüchtg 82:162–173

    Google Scholar 

  • Marcellán ON, Camadro EL (1996) Self- and cross-incompatibility in Asparagus officinalis and Asparagus densiflorus cv. Sprengeri. Can J Bot 74:1621–1625

    Article  Google Scholar 

  • Nakayama H, Ito T, Hayashi Y et al (2006) Development of sex-linked primers in garden asparagus (Asparagus officinalis L.). Breed Sci 56:327–330

    Article  Google Scholar 

  • Nogales M, Padilla DP, Nieves C et al (2007) Secondary seed dispersal systems, frugivorous lizards and predaroty birds in insular volcanic badlands. J Ecol 95:1394–1403

    Article  Google Scholar 

  • Obermeyer AA (1983) Protasparagus Oberm. nom. nov.: new combinations. S Afr J Bot 2:243–244

    Google Scholar 

  • Paolucci I, Gaudet M, Jorge V et al (2010) Genetic linkage maps of Populus alba L. and comparative mapping analysis of sex determination across Populus species. Tree Genet Genomes 6:863–875

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    PubMed  Article  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    PubMed  Article  CAS  Google Scholar 

  • Shaw J, Lickey EB, Beck JT et al (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166

    PubMed  Article  CAS  Google Scholar 

  • Shaw J, Lickey EB, Schilling EE et al (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288

    PubMed  Article  CAS  Google Scholar 

  • Singh AK (1986) Utilization of wild relatives in the genetic improvement of Arachis hypogaea L. 8. Synthetic amphidiploids and their importance in interspecific breeding. Theor Appl Genet 72:433–439

    Article  Google Scholar 

  • Smith J, Putnam A, Nair M (1990) In vitro control of Fusarium diseases of Asparagus officinalis L. with a Streptomyces or its polyene antibiotic, Faeriefungin. J Agric Food Chem 38:1729–1733

    Article  Google Scholar 

  • Štajner N, Bohanec B, Javornik B (2002) Genetic variability of economically important Asparagus species as revealed by genome size analysis and rDNA ITS polymorphisms. Plant Sci 162:931–937

    Article  Google Scholar 

  • Stansbury CD (2001) Dispersal of the environmental weed bridal creeper, Asparagus asparagoides by silvereyes, Zosterops lateralis, in south-western Australia. Emu 101:39–45

    Article  Google Scholar 

  • Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. BioTechniques 14:748–750

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M et al (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    PubMed  Article  CAS  Google Scholar 

  • Traveset A, Riera N, Mas RE (2001) Passage through bird guts causes interspecific differences in seed germination characteristics. Funct Ecol 15:669–675

    Article  Google Scholar 

  • Turelli M, Barton NH, Coyne JA (2001) Theory and speciation. Trends Ecol Evol 16:330–343

    PubMed  Article  Google Scholar 

  • Turner PJ, Scott JK, Spafford H (2008) The ecological barriers to the recovery of bridal creeper (Asparagus asparagoides (L.) Druce) infested sites: Impacts on vegetation and the potential increase in other exotic species. Austral Ecol 33:713–722

    Article  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F et al (1997) The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882

    Article  Google Scholar 

  • Weiblen GD, Oyama RK, Donoghue MJ (2000) Phylogenetic analysis of dioecy in Monocotyledons. Am Nat 155:46–58

    PubMed  Article  Google Scholar 

  • Williams PA (2006) The role of blackbirds (Turdus merula) in weed invasion in New Zealand. N Z J Ecol 30:285–291

    Google Scholar 

  • Zhou JS, Zhan FX, Tang YP et al (2009) Interspecific hybridization between A. officinalis L. and Asparagus dauricus Fisch.ex Link. In: XIIth International Asparagus Symposium. Lima, Peru

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Acknowledgments

We gratefully thank Drs. Y. Ozaki and E. Nishihara for providing seeds of A. kiusianus and A. dauricus, respectively. This study was partly supported by Grant-in-Aid for Scientific Research, Grant-in-Aid for Japan Society for the Promotion of Science (JSPS) Fellows (to S.K.) from the Ministry of Education, Science and Culture of Japan.

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Correspondence to Shosei Kubota.

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Communicated by M. Havey.

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Kubota, S., Konno, I. & Kanno, A. Molecular phylogeny of the genus Asparagus (Asparagaceae) explains interspecific crossability between the garden asparagus (A. officinalis) and other Asparagus species. Theor Appl Genet 124, 345–354 (2012). https://doi.org/10.1007/s00122-011-1709-2

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  • DOI: https://doi.org/10.1007/s00122-011-1709-2

Keywords

  • Dioecious Species
  • trnL Intron
  • Hermaphroditism
  • cpDNA Region
  • Single Polymerase Chain Reaction Product