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.
Similar content being viewed by others
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
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
Barnea A, Yom-Tov Y, Friedman J (1991) Does ingestion by birds affect seed germination? Funct Ecol 5:394–402
Barrett SCH (2002) Evolution of sex: the evolution of plant sexual diversity. Nat Rev Genet 3:274–284
Bawa KS (1980) Evolution of dioecy in flowering plants. Ann Rev Ecol Syst 11:15–39
Bracale M, Caporali E, Galli MG et al (1991) Sex determination and differentiation in Asparagus officinalis L. Plant Sci 80:67–77
Burk LG (1967) An interspecific bridge-cross: Nicotiana repanda through N. sylvestris to N. tabacum. J Hered 58:215–218
Charlesworth B, Charlesworth D (1978) A model for the evolution of dioecy and gynodioecy. Am Nat 112:975–997
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
Clifford HT, Conran JG (1987) Asparagaceae. In: George AS (ed) Flora of Australia. Australian Government Publishing Service, Canberra, pp 140–142
Coyne JA, Orr HA (1989) Patterns of speciation in Drosophila. Evolution 43:362–381
Coyne JA, Orr HA (1996) “Patterns of speciation in Drosophila” revised. Evolution 51:295–303
Crow JF (1998) 90 years ago: the beginning of hybrid maize. Genetics 148:923–928
Dahlgren RMT, Clifford HT, Yeo PF (1985) The families of the monocotyledons. Springer, Heidelberg
Darwin C (1877) Different forms of flowers on plants of the same species. John Murray, London
Dehgan B (1984) Phylogenetic significance of interspecific hybridization in Jatropha (Euphorbiaceae). Syst Bot 9:467–478
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
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
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
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
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
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
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
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
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
Ito T, Ochiai T, Fukuda T et al (2008) Potential of interspecific hybrids in Asparagaceae. Acta Hortic 776:279–284
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
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
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
Khrustaleva LI, Kik C (1998) Cytogenetical studies in the bridge cross Allium cepa × (A. fistulosum × A. roylei). Theor Appl Genet 96:8–14
Kubitzki K, Rudall PJ (1998) Asparagaceae. In: Kubitzki K (ed) The families and genera of vascular plants, vol 3. Springer, Heidelberg, pp 125–128
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
Lawrie SL (2006) The ecology of bridal veil (Asparagus declinatus L.) in South Australia. Plant Prot Q 21:99–100
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
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
Lloyd DG (1975) The maintenance of gynodioecy and androdioecy in angiosperms. Genetica 45:325–339
Löptien H (1979) Identification of the sex chromosome pair in asparagus (Asparagus officinalis L.). Z. Pflanzenzüchtg 82:162–173
Marcellán ON, Camadro EL (1996) Self- and cross-incompatibility in Asparagus officinalis and Asparagus densiflorus cv. Sprengeri. Can J Bot 74:1621–1625
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
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
Obermeyer AA (1983) Protasparagus Oberm. nom. nov.: new combinations. S Afr J Bot 2:243–244
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
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
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
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
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
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
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
Stansbury CD (2001) Dispersal of the environmental weed bridal creeper, Asparagus asparagoides by silvereyes, Zosterops lateralis, in south-western Australia. Emu 101:39–45
Stewart CN Jr, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. BioTechniques 14:748–750
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
Traveset A, Riera N, Mas RE (2001) Passage through bird guts causes interspecific differences in seed germination characteristics. Funct Ecol 15:669–675
Turelli M, Barton NH, Coyne JA (2001) Theory and speciation. Trends Ecol Evol 16:330–343
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
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
Weiblen GD, Oyama RK, Donoghue MJ (2000) Phylogenetic analysis of dioecy in Monocotyledons. Am Nat 155:46–58
Williams PA (2006) The role of blackbirds (Turdus merula) in weed invasion in New Zealand. N Z J Ecol 30:285–291
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
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.
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Havey.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-011-1709-2