Genetic Resources and Crop Evolution

, Volume 64, Issue 8, pp 1873–1887 | Cite as

Evaluation of genetic resources in the genus Asparagus for resistance to Asparagus virus 1 (AV-1)

  • Thomas NothnagelEmail author
  • Holger Budahn
  • Ilona Krämer
  • Edgar Schliephake
  • Edit Lantos
  • Susann Plath
  • Reiner Krämer
Research Article


Forty-four Asparagus officinalis cultivars, gene bank accessions and breeding lines as well as thirty-four accessions of wild relatives of Asparagus were evaluated for resistance to Asparagus virus 1. Three different test strategies were developed for the assessment of individual plants: (1) natural infection under field conditions, or two vector-mediated infection assays using the green peach aphid Myzus persicae (2) in an insect-proof gauze cage or (3) in a climate chamber. The AV-1 infections were verified by DAS-ELISA and RT-PCR approaches. All tested 660 individual plants of A. officinalis germplasm were susceptible to AV-1 infection. In contrast, in 276 plants of 29 Asparagus wild accessions no virus infection could be detected. These resistant accessions comprised of nineteen diploid, tetraploid and hexaploid species of both the Eurasian clade and the African clade of the asparagus germplasm. Data of the AV-1 resistance evaluation are discussed in relation to the genetic distance of the resistance carrier and potential application in breeding.


Asparagus spp. Asparagus virus 1 ELISA Genetic diversity Myzus persicae RT-PCR SSR marker Virus resistance Wild relatives 



The research was supported by the Federal Ministry of Agriculture and Food (BMEL). We wish to thank Barbara Sell, Susanne Kozber, Karla Müller, Elke Zjaba, Ute Fuhrmann, Ilona Renneberg and Anke Dilger for the excellent technical assistance. Furthermore, we thank all breeders and gene banks for allocation of the asparagus material, especially Dr. Ludwig Martins, curator of the collection of the Gruson-Gewächshäuser Magdeburg. The authors are grateful to Dr. Heiko Zibell for his critical review of the manuscript.

Author contribution

Budahn H: SSR analysis, genetic distance; Krämer I: RT-PCR; Krämer R: Resistance tests and ELISA analysis, study design; Lantos E: Resistance tests and ELISA analysis; Nothnagel T: Genetic resources, plant material, study design; Schliephake E: Vector preparation and allocation (M. persicae); Plath S: Chromosome analyses

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest. Furthermore we declare that the experiments comply with the current laws of Germany.

Supplementary material

10722_2016_476_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 24 kb)
10722_2016_476_MOESM2_ESM.docx (24 kb)
Supplementary material 2 (DOCX 24 kb)
10722_2016_476_MOESM3_ESM.docx (26 kb)
Supplementary material 3 (DOCX 25 kb)


  1. Aldenhoff L (2014) Belastung von Spargeljungpflanzen mit ertragsrelevanten Viren. Documents/lraka/Fachinformationen/Garten-Obst-Weinbau/Spargelanbau/Spargeltag2015/Aldenhoff Vortrag Viren Spargeltag Ka 2015.pdf
  2. Baker JG (1875) Revision of the genera and species of Asparagaceae. J Linn Soc Bot 14:508–632. doi: 10.1111/j.1095-8339.1875.tb00349.x CrossRefGoogle Scholar
  3. Bandte M, Grubits E, von Bargen S, Rabenstein F, Weber D, Uwihs F, Büttner C (2008) Eine Feldstudie zum Auftreten von Virusinfektionen in Spargel (Asparagus officinalis L.) in norddeutschen Ertragsanlagen. ALVA-Tagung Raumberg-Gumpenstein 63:97–99. ISSN 1811-7317Google Scholar
  4. Blockus S, Lesker T, Maiss E (2014) Complete genome sequences of two biologically distinct isolates of Asparagus virus 1. Arch Virol 160:569–572. doi: 10.1007/s00705-014-2227-8 CrossRefPubMedGoogle Scholar
  5. Boiteux LS, Nagata T, Dutra WP, Fonseca ME (1993) Sources of resistance to tomato spotted wilt virus (TSWV) in cultivated and wild species of Capsicum. Euphytica 67:89–94. doi: 10.1007/BF00022729 CrossRefGoogle Scholar
  6. Boonen P (2001) Spargel von der Heilpflanze zur Delikatesse. NUGI 601 730. ISBN 90-805609-3-6Google Scholar
  7. Castro P, Gil J, Cabrera A, Moreno R (2013) Assessment of genetic diversity and phylogenetic relationships in Asparagus species related to Asparagus officinalis. Genet Resour Crop Evol 60:1275–1288. doi: 10.1007/s10722-012-9918-3 CrossRefGoogle Scholar
  8. Chen JF, Luo XD, Qian ChT, Molly MJ, Staub JE, Zhuang FY, Lou QF, Ren G (2004) Cucumis monosomic alien addition lines: morphological, cytological, and genotypic analyses. Theor Appl Genet 108:1343–1348. doi: 10.1007/s00122-003-1546-z CrossRefPubMedGoogle Scholar
  9. Chen JF, Zhou XH (2011) Cucumis. In: C. Kole (ed) Wild crop relatives: genomics and breeding resources—vegetables. Springer, Berlin, pp 67–90. doi: 10.1007/978-3-642-20450-0_6
  10. Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for detection of plant viruses. J Gen Virol 34:475–483. doi: 10.1099/0022-1317-34-3-475 CrossRefPubMedGoogle Scholar
  11. Clifford HT, Conran JG (1987) Asparagaceae. In: George AS (ed) Flora of Australia. Australian Government of Public Service, Canberra, Australia, pp 159–164. ISBN-13:978 0 644 05214 6Google Scholar
  12. Conroy RJ (1975) Asparagus decline and replant deaths. Agric Gaz NSW 86:23Google Scholar
  13. De Vries-Paterson RM, Evans TA, Stephens CT (1992) The effect of asparagus virus- infection on asparagus tissue culture. Plant Cell Tiss Org 31:31–35. ISSN:0167-6857Google Scholar
  14. Eenink AH, Dieleman FL, Groenwold R (1981) Resistance of lettuce (Lactuca) to the leaf aphid Nasonovia ribis nigri. 1. Transfer of resistance from L. virosa to L. sativa by interspecific crosses and selection of resistant breeding lines. Euphytica 31:291–300. doi: 10.1007/BF00021643 CrossRefGoogle Scholar
  15. Elmer WH, Johnson DA, Mink GI (1996) Epidemiology and management of the diseases causal to asparagus decline. Plant Dis 80:117–125. ISSN:0191-2917Google Scholar
  16. Evans TA, DeVries RM, Wacker TL, Stephens CT (1990) Epidemiology of asparagus viruses in Michigan asparagus. Acta Hortic 271:285–290. doi: 10.17660/ActaHortic.1990.271.41 CrossRefGoogle Scholar
  17. Evans TA, Stephens CT (1984) Virus-fungus inter-relationships in a Fusarium root and crown rot complex in asparagus. Phytopathology 74:860–861Google Scholar
  18. Falavigna A, Alberti P, Casali PE, Toppino L, Huaisong W, Menella G (2008) Interspecific hybridization for asparagus breeding in Italy. Acta Hortic 776:291–297. doi: 10.17660/ActaHortic.2008.776.37 CrossRefGoogle Scholar
  19. Fraser RSS (1990) The genetics of resistance to plant viruses. Annu Rev Phytopathol 28:179–200. doi: 10.1146/ CrossRefGoogle Scholar
  20. Fujisawa I, Goto T, Tsuchizaki T, Iizuka N (1983) Host range and some properties of Asparagus Virus 1 isolated from Asparagus officinalis in Japan. Ann Phytopathol Soc Jpn 49:299–307. doi: 10.3186/jjphytopath.49.299 CrossRefGoogle Scholar
  21. Gibson RW, Jones MGK, Fish N (1988) Resistance to potato leaf roll virus and potato virus Y in somatic hybrids between dihaploid Solanum tuberosum and S. brevides. Theor Appl Genet 76:113–117. doi: 10.1007/BF00288840 CrossRefPubMedGoogle Scholar
  22. Gonzalez-Castanon ML, Falavigna A (2008) Asparagus germplasm and interspecific hybridization. Acta Hortic 776:319–326. doi: 10.17660/ActaHortic.2008.776.41 CrossRefGoogle Scholar
  23. Grandillo S, Chetelat R, Knapp S, Spooner D, Peralta I, Cammareri M, Prerz O, Termolino P, Tripodi P, Chiusano ML, Ercolano MR, Frusciante L, Monti L, Pignone D (2011) Chapter 9 Solanum sect. Lycopersicon. In: C. Kole (ed) Wild crop relatives: genomic and breeding resources, vegetables, Springer, Berlin, pp 129–246. doi: 10.1007/978-3-642-20450-0-9
  24. Greiner HD (1980) Untersuchungen über Virus und Fusarium an Spargel (Asparagus officinalis L.) im nordbadischen Anbaugebiet unter besonderer Berücksichtigung einer Virus-Pilz-Wechselwirkung. Dissertation Universität HohenheimGoogle Scholar
  25. Hayes RJ, Ryder EJ (2007) Introgression of novel alleles for partial resistance to big vein disease from Lactuca virosa into the cultivated lettuce. HortScience 42:35–39. ISSN:2327-9834Google Scholar
  26. Hein A (1963) Virosen an Spargel. Mitt. Biol. Bundesanstalt Land- und Forstwirtschaft Berlin-Dahlem 108:70–74Google Scholar
  27. Howell WE (1985) Properties of Asparagus Virus 1 isolated from Washington State Asparagus. Plant Dis 69:1044–1046. doi: 10.1094/PD-69-1044 CrossRefGoogle Scholar
  28. Index to Plant Chromosome Numbers (IPCN) ICPN- Accessed 14 June 2016
  29. Ito T, Ochiai T, Ashizawa H, Shimodate T, Sonoda T, Fukuda T, Yokoyama J, Kameya T, Kanno A (2007) Production and analysis of reciprocal hybrids between Asparagus officinalis L. and A. schoberioides Kunth. Genet Resour Crop Evol 54:1063–1071. doi: 10.1007/s10722-006-9186-1 CrossRefGoogle Scholar
  30. Jessop JP (1966) The genus Asparagus in Southern Africa. Bothalia 9:31–96CrossRefGoogle Scholar
  31. Kakeda K, Fukui K, Yamagata H (1991) Heterochromatic differentiation in barley chromosomes revealed by C-and N-banding techniques. Theor Appl Genet 81:144–150. doi: 10.1007/BF00215715 CrossRefPubMedGoogle Scholar
  32. Kalyani G, Reddy AS, Lava Kumar P, Prasada Rao RDVJ, Aruna R, Waliyar F, Nigam SN (2007) Sources of resistance to Tobacco streak virus in Wild Arachis (Fabaceaea: Papilionoidae) Germplasm. Plant Dis 91:1585–1590. doi: 10.1094/PDIS-91-12-1585 CrossRefGoogle Scholar
  33. Kang BC, Yean I, Jahn MM (2005) Genetics of plant virus resistance. Ann Rev Phytopathol 43:581–621. doi: 10.1146/annurev.phyto.43.011205.141140 CrossRefGoogle Scholar
  34. Kanno A, Yokoyama J (2011) Asparagus. In: C. Kole (ed) Wild crop relatives: genomic and breeding resources, vegetables. Springer, Berlin, pp 23–42. doi: 10.1007/978-3-642-20450-0_3
  35. Kay QON, Davies EW, Rich TCG (2001) Taxonomy of the western European endemic Asparagus prostratus (A.officinalis subsp. prostratus (Asparagaceae). Bot J Linn Soc 137:127–137. doi: 10.1006/bojl.2001.0458 Google Scholar
  36. Kegler H, Schmidt HB, Woltersdorff B, Reinhardt I, Weber I, Proll I (1991) Spread of viruses in asparagus fields. Arch Phytopathol PFL 27:251–258. ISSN:0323-5408 (Print); ISSN:1477-2906 (Online)Google Scholar
  37. Kegler H, Schwarz S, Kecke S, Gottwald J, Arndt H, Schubert J (1999) A contribution to virus testing of Asparagus plants. Arch Phytopathol PFL 32:193–203. ISSN:0323-5408 (Print); ISSN:1477-2906 (Online)Google Scholar
  38. Knaflewski M, Fiedorow Z, Pawlowski A (2008) Viral diseases and their impact on Asparagus performance and yield. Acta Hortic 776:191–197. doi: 10.17660/ActaHortic.2008.776.23 CrossRefGoogle Scholar
  39. Krämer R, Lantos E, Aldenhoff L, Nothnagel T (2016) Virusbefall in Spargelanbau-Regionen Deutschlands, Europas und Nordamerikas. 48. Jahrestreffen des Arbeitskreises “Viruskrankheiten der Pflanzen“07. und 08. März 2016, Hannover,
  40. Kubota S, Konno I, Kanno A (2012) 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. doi: 10.1007/s00122-011-1709-2 CrossRefPubMedGoogle Scholar
  41. Lambourne C, McPherson M, Wright K, Goodson M (2012) Asparagus—screening UK crops for virus infection. Report FV384a, Stockbridge Technology Centre Ltd., Agriculture and Horticulture Development BoardGoogle Scholar
  42. Maule DP, Caranta C, Boulton MI (2007) Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8:223–231. doi: 10.1111/j.1364-3703.2007.00386.x CrossRefPubMedGoogle Scholar
  43. McCollum GD (1988) Asparagus densiflorus cultivars Sprengeri and Myers cross-pollination with A. officinalis and other species. Asparagus Newsl 61:1–10Google Scholar
  44. Mercati F, Riccardi P, Leebens-Mack J, Abenavoli MR, Falavigna A, Sunseri F (2013) Single nucleotide polymorphism isolated from a novel EST dataset in garden asparagus (Asparagus officinalis L.). Plant Sci 203–204:115–123. doi: 10.1016/j.plantsci.2013.01.002 CrossRefPubMedGoogle Scholar
  45. Moffett P (2009) Mechanisms of recognition in dominant R gene mediated resistance. Adv Virus Res 75:1–33. doi: 10.1016/S0065-3527/(09)07501-0 CrossRefPubMedGoogle Scholar
  46. Moreno R, Espejo JA, Cabrera A, Gil J (2008a) Origin of tetraploid cultivated asparagus landraces inferred from nuclear ribosomal DNA internal transcribed spacer’ polymorphisms. Ann Appl Biol 153:233–241. doi: 10.1111/j.1744-7348.2008.00254.x Google Scholar
  47. Moreno R, Espejo JA, Moreno MT, Gil J (2008b) Collection and conservation of ‘Morado de Huetor’ Spanish tetraploid asparagus landrace. Genet Resour Crop Evol 55:773–777. doi: 10.1007/s10722-008-9358-2 CrossRefGoogle Scholar
  48. Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273. PMC413122Google Scholar
  49. Norup MF, Petersen G, Burrows S, Bouchenak-Khelladi Y, Leebsens-Mack J, Pires JC, Linder HP, Seberg O (2015) Evolution of Asparagus L. (Asparagaceae): OUT-of-South-Africa and multiple origins of sexual dimorphism. Mol Phylogenet Evol 92:25–44. doi: 10.1016/j.ympev.2015.06.002 CrossRefPubMedGoogle Scholar
  50. Nothnagel T, Krämer R, Rabenstein F, Schreyer L (2013) Untersuchungen zum Auftreten von Braunverfärbungen bei Spargel (Asparagus officinalis L.) unter besonderer Berücksichtigung des Befalls mit Fusarium spp. und Viren in Spargelanlagen Sachsen-Anhalts. J Kulturpflanzen 65:50–59. doi: 10.5073/JfK.2013.02.2 Google Scholar
  51. Nothnagel T, Budahn H, Krämer I, Schliephake E, Schreyer L, Krämer R (2014) Resistance to Asparagus virus 1 in the Wild Relative Asparagus amarus. J Phytopathol 162:180–189. doi: 10.1111/jph.12169 CrossRefGoogle Scholar
  52. Nothnagel T, Krämer R, Budahn H, Schrader O, Ulrich D, Schreyer L (2012) Interspecific hybridization of asparagus for the enlargement of the genetic basis concerning resistance to biotic and abiotic stress. Acta Hortic 960:139–146. doi: 10.17660/ActaHortic.2012.960.19 CrossRefGoogle Scholar
  53. Obermeyer AA (1983) Protasparagus Oberm., nom.nov: new combinations. S Afr J Bot 2:1929–1939Google Scholar
  54. Obermeyer AA (1984) Revision of the genus Myrsiphyllum Willd. Bothalia 15:77–88. doi: 10.4102/abc.v15i1/2.1106 Google Scholar
  55. Ochiai T, Sonoda T, Kanno A, Kameya T (2002) Interspecific hybrids between Asparagus schoberioides Kunth and A. officinalis L. Acta Hortic 589:225–229. doi: 10.17660/ActaHortic.2002.589.31 CrossRefGoogle Scholar
  56. Oetting WS, Lee HK, Flanders DJ, Wiesner GL, Sellers TA, King RA (1995) Linkage analysis with multiplexed short tandem repeat polymorphisms using infrared fluorescence and M13 tailed primers. Genomics 30:450–458. doi: 10.1006/geno.1995.1264 CrossRefPubMedGoogle Scholar
  57. Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15:8–15. doi: 10.1007/BF02772108 CrossRefGoogle Scholar
  58. Ruge B, Linz A, Pickering R, Proeseler G, Greif P, Wehling P (2003) Mapping of Rym14Hb, a gene introgressed from Hordeum bulbosum and conferring resistance to BaMMV and BaYMV in barley. Theor Appl Genet 107:965–971. doi: 10.1007/s00122-003-1339-4 CrossRefPubMedGoogle Scholar
  59. Schickel W, Behr HC, Illert S, Baltsch R, Tübben HG (1993) ZMP Bilanz Gemüse `92. Zentrale Markt- und Preisberichtstelle GmbH, Bonn, Germany. ISBN: 0344-9378Google Scholar
  60. Stajner N, Bohance 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. doi: 10.1016/S0168-9452(02)00039-0 CrossRefGoogle Scholar
  61. Subramanya R (1981) Relationship between tolerance and resistance to pepper mottle virus in a cross between Capsicum annum L. × Capsicum chinensis Jacq. Euphytica 31:461–464. doi: 10.1007/BF00021663 CrossRefGoogle Scholar
  62. Tiberini A, Zaccaria A, Tomassoli L (2014) Incidence and genetic variability of asparagus virus 1 in naturally infested asparagus. J Plant Pathol 96:177–182. ISSN:1125-4653Google Scholar
  63. Tomassoli L, Tiberini A, Vetten HJ (2012) Viruses of Asparagus. Adv Virus Res 84:345–365CrossRefPubMedGoogle Scholar
  64. Tomassoli L, Zaccaria A, Tiberini A (2007) Use of one step RT-PCR for detection of Asparagus virus 1. J Plant Pathol 89:413–415. ISSN:1125-4653Google Scholar
  65. Tomassoli L, Zaccaria A, Valentino A, Tamietti G (2008) First investigations on the diseases affecting green asparagus crops in Sicily. Col Prot 37:83–90Google Scholar
  66. Triebe B, Mukai Y, Dhaliwal HS, Martin TJ, Gill BS (1991) Identification of alien chromatin specifying resistance to weak streak mosaic and greenbug in wheat germ plasm by C-banding and in situ hybridization. Theor Appl Genet 81:381–389. doi: 10.1007/BF00228680 CrossRefPubMedGoogle Scholar
  67. Truniger V, Aranda MA (2009) Recessive resistance to plant viruses. Adv Virus Res 75:119–159. doi: 10.1016/S0065-3527(09)07504-6 CrossRefPubMedGoogle Scholar
  68. Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DH, Walter SM, Webb DA (1980) Flora Europaea. Vol. 5: Alismataceae to Orchidaceae (Monocotyledones), Cambrigde University Press, Cambrigde, pp.71–73. ISBN:0-521-20108-xGoogle Scholar
  69. Valente MT, Sabatini E, Casali PE, Ferrari L, Falavigna A (2012) Molecular marker-assisted introgression of wild Asparagus species genome into the cultivated Asparagus officinalis L. Acta Hortic 950:181–186. doi: 10.17660/ActaHortic.2012.950.19 CrossRefGoogle Scholar
  70. Weissenfels M (1973) Virusbefall am Spargel (Asparagus officinalis L.). Archiv Gartenbau 21:235–243Google Scholar
  71. Weissenfels M, Schmelzer K (1976) Untersuchungen über das Schadausmaß durch Viren am Spargel (Asparagus officinalis L.). Arch Phytopathol PFL 12:67–73CrossRefGoogle Scholar
  72. Wilking PW (1987) Transfer of polygenic resistance to ryegrass mosaic lines from perennial to Italian ryegrass by backcrossing. Ann Appl Biol 111:409–413. doi: 10.1111/j.1744-7348.1987.tb01468.x CrossRefGoogle Scholar
  73. Yang HJ (1979) Early effects of viruses on the growth and productivity of asparagus plants. HortScience 14:734–735. ISSN: 0018-5345Google Scholar
  74. Young CC (1984) Auto-intoxication in root exudates of Asparagus officinalis L. Plant Soil 82:247–253. doi: 10.1007/BF02220251 CrossRefGoogle Scholar
  75. Ziebell H (2016) Plant Defence and Viral Interference. In: T. Kleinow (ed) Plant–virus interaction: molecular biology, intra- and intercellular transport. Springer, pp 123–159. doi: 10.1007/978-3-319-25489-0-5

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Institute for Breeding Research on Horticultural CropsJulius Kühn-Institut (JKI), Federal Research Centre for Cultivated PlantsQuedlinburgGermany
  2. 2.Institute for Resistance Research and Stress ToleranceJulius Kühn-Institut (JKI), Federal Research Centre for Cultivated PlantsQuedlinburgGermany

Personalised recommendations