Skip to main content
SpringerLink
Log in

Spinach: better management of downy mildew and white rust through genomics

  • Chapter
The Downy Mildews - Biology, Mechanisms of Resistance and Population Ecology

  • 7 Accesses

Abstract

Spinach (Spinacia oleracea) has become an increasingly important vegetable crop in many parts of the world. Significant changes in production practices, particularly in the U.S. and E.U., have occurred in the past 10–15 years as a result of increased product demand. These changes likely increased the incidence and severity of downy mildew, caused by Peronospora farinosa f. sp. spinaciae. Recently, progress has been made to define the genetics of resistance to this pathogen and the closely related white rust pathogen, Albugo occidentalis. In this chapter, we outline the genetic and genomic resources currently available for spinach, draw parallels between spinach diseases and more thoroughly characterized pathosystems, and describe efforts currently underway to develop new genetic and genomic tools to better understand downy mildew and white rust of spinach. Presently, many crucial tools and resources required to define the molecular underpinnings of disease are unavailable for either spinach or its pathogens. New resources and information for spinach genomics would provide a jumpstart for ongoing efforts to define (and deploy) genetic resistance against downy mildew and white rust.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

Pfs :

Peronospora farinosa f. sp. spinaciae

Ao :

Albugo occidentalis

RPF :

Resistance to Peronospora farinosa

NIL:

Near Isogenic Line

MAS:

Marker Assisted Selection

References

  • Aarts, N., Metz, M., Holub, E., Staskawicz, B. J., Daniels, M. J., & Parker, J. E. (1998). Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proceedings of the National Academy of Sciences USA, 95, 10306–10311.

    Article  CAS  Google Scholar 

  • Allen, R. L., Bittner-Eddy, P. D., Grenville-Briggs, L. J., Meitz, J. C., Rehmany, A. P., Rose, L. E., et al. (2004). Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science, 306, 1957–1960.

    Article  PubMed  CAS  Google Scholar 

  • Arumuganathan, K., & Earle, E. D. (1991). Nuclear DNA content of some important plant species. Plant Molecular Biology Reporter, 9, 208–218.

    Article  CAS  Google Scholar 

  • Baumgarten, A., Cannon, S., Spangler, R., & May, G. (2003). Genome-level evolution of resistance genes in Arabidopsis thaliana. Genetics, 165, 309–319.

    PubMed  CAS  Google Scholar 

  • Bemis, W. P., & Wilson, G. B. (1953). A new hypothesis explaining the genetics of sex determination. Journal of Heredity, 44, 41–45.

    Google Scholar 

  • Bittner-Eddy, P. D., & Beynon, J. L. (2001). RPP13-Nd an Arabidopsis LZ-NBS-LRR-type resistance gene that is salicylic acid-independent and that does not require disease resistance signaling pathways defined by EDS1 or Ndr1. Molecular Plant-Microbe Interactions, 14, 416–421.

    Article  PubMed  CAS  Google Scholar 

  • Bittner-Eddy, P. D., Crute, I. R., Holub, E. B., & Beynon, J. L. (2000). RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica (At). The Plant Journal, 21, 177–188.

    Article  PubMed  CAS  Google Scholar 

  • Botella, M. A., Parker, J. E., Frost, L. N., Bittner-Eddy, P. D., Beynon, J. L., Daniels, M. J., et al. (1998). Three genes of the Arabidopsis RPP1 complex resistance locus recognise distinct Peronospora parasitica (At) avirulence determinants. Plant Cell, 10, 1847–1860.

    Article  PubMed  CAS  Google Scholar 

  • Bowers, J. L., & Goode, M. J. (1980a). Spinach varieties. Proceedings of the Arkansas State Horticultural Society, 101, 64.

    Google Scholar 

  • Bowers, J. L., & Goode, J. J. (1980b). Ozarka and Greenvalley: new disease resistant spinach cultivars. Arkansas Farm Research, 32(2), 6.

    Google Scholar 

  • Brandenberger, L. P., Correll, J. C., & Morelock, T. E. (1991). Identification of and cultivar reactions to a new race (race 4) of Peronospora farinosa f. sp. spinaciae on spinach in the United States. Plant Disease, 75, 630–634.

    Article  Google Scholar 

  • Brandenberger, L. P., Morelock, T. E., & Correll, J. C. (1992). Evaluation of spinach germplasm for resistance to a new race (Race 4) of Peronospora farinosa f. sp. spinaciae. HortScience, 27, 1118–1119.

    Google Scholar 

  • Brandenberger, L. P., Correll, J. C., Morelock, T. E., & McNew, R. W. (1994). Characterization of resistance of spinach to white rust (Albugo occidentalis) and downy mildew (Peronospora farinosa f. sp. spinaciae). Phytopathology, 84, 431–437.

    Article  Google Scholar 

  • Brenner, D. M. (2009). The U.S. spinach germplasm collection. (Paper presented at The T.E. Morelock International Spinach Conference, Fayetteville, AR). From: http://spinach.uark.edu/Spinach Conference 2009 Program.pdf, November.

  • Choi, Y. J., Hong, S. B., & Shin, H. D. (2007). Re-consideration of Peronospora effusa infecting Spinacia oleracea as distinct species, Peronospora effusa. Mycological Research III, 381–391.

    Google Scholar 

  • Correll, J. C. (1998). Review of the biology of Peronospora farinosa f. sp. spinaciae. In: Crop protection Compendium. Wallingford, U.K.: CABI).

    Google Scholar 

  • Correll, J. C., Koike, S. T., Brandenberger, L. P., Black, M. C., & Morelock, T. E. (1990). A new race (Race 4) of downy mildew on spinach. California Agriculture, 44, 14–15.

    Google Scholar 

  • Correll, J. C., Morelock, T. E., Black, M. C., Koike, S. T., Brandenberger, L. P., & Dainello, F. J. (1994). Economically important diseases of spinach. Plant Disease, 78, 653–660.

    Article  Google Scholar 

  • Correll, J. C., Irish, B. M., Koike, S. T., & Morelock, T. E. (2001). Update on downy mildew (Peronospora farinosa f.sp. spinaciae) of spinach in the United States. Paper presented at the National Spinach Conference, Fayetteville, AR USA, November.

    Google Scholar 

  • Correll, J. C., Irish, B. M., Koike, S. T., Shafer, J., & Morelock, T. E. (2003). Update on downy mildew of spinach. Paper presented at the National Spinach Conference, Fayetteville, AR USA, November

    Google Scholar 

  • Correll, J. C., Feng, C., Irish, B. M., Koike, S. T., Morelock, T. E., Bentley, T. C. et al. (2007). Spinach downy mildew: overview of races and the development of molecular markers linked to major resistance genes. In: A. Lebeda, & P. T. N. Spencer-Phillips (Eds.), Advances in downy mildew research, 3 (pp. 135–142).

    Google Scholar 

  • Correll, J. C., Feng, C. Kudrna, D. A., Ammiraju, J., Raju, & Wing, R. A. (2009). Construction of a spinach (Spinacae oleracea) BAC library. Plant and Animal Genomes XVII. p. 604.

    Google Scholar 

  • Daehnfeldt, L. (2007). Danish production of vegetable seed—Is it only spinach? Retrived June 18, 2007 from http://www.daehnfeldt.com/index.asp?NyhedsId=38.

  • Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., et al. (1994). A central role of salicylic acid in plant disease resistance. Science, 266, 1247–1249.

    Article  PubMed  CAS  Google Scholar 

  • Dicoteau, D. R. (2000). Vegetable crops. New Jersey: Prentice Hall.

    Google Scholar 

  • Dong, X. (2004). NPR1, all things considered. Current Opinion in Plant Biology, 7, 547–552.

    Article  PubMed  CAS  Google Scholar 

  • Eenink, A. H. (1974). Linkage in Spinacia oleracea L. between the locus for resistance to Peronospora spinaciae Laub. and the locus for tolerance for cucumber virus 1. Euphytica, 23, 485–487.

    Article  Google Scholar 

  • Eenink, A. H. (1976a). Linkage of Spinacia oleracea L. Of two race-specific genes for resistance to downy mildew Peronospora farinosa f.sp. spinaciae Byford. Euphytica., 25, 713–715.

    Article  Google Scholar 

  • Eenink, A. H. (1976b). Resistance in spinach to downy mildew. In: Proceedings of Eucarpia Meeting. LeafyVegetables, pp. 53–54. Wageningen, Holland.

    Google Scholar 

  • Ellis, J. R., & Janick, J. (1960). The chromosomes of Spinacia oleracea. American Journal of Botany, 47, 210–214.

    Article  Google Scholar 

  • Feng, C., Correll, J. C., & Bluhm, B. H. (2010). A spinach BAC library for marker development, gene discovery, and functional genomics. Phytopathology, 100, S35.

    Google Scholar 

  • Foss, C. R., & Jones, L. J. (2005). Crop profile for spinach seed in Washington. From: http://www.ipmcenters.org/cropprofiles/docs/waspinachseed.html.

  • Goode, M. J., Morelock, T. E., & Bowers, J. L. (1988). ‘Fall Green’ spinach. HortScience, 23(5), 931.

    Google Scholar 

  • Greville, R. K. (1824). Flora Edinensis. Edinburgh: Blackwood & Strand.

    Google Scholar 

  • Groben, R., & Wricke, G. (1998). Occurrence of microsatellites in spinach sequences from computer datebases and development of polymorphic SSR markers. Plant Breeding, 117, 271–274.

    Article  CAS  Google Scholar 

  • Handke, S., Seehaus, H., & Radies, M. (2000). Detection of a linkage group of the four turkestanica. Gartenbauswissenschaft., 65, 73–78.

    Google Scholar 

  • Holub, E. B. (1997). Organization of resistance genes in Arabidopsis. In I. R. Crute & E. B. Holub (Eds.), The gene-for-gene relationship in plant-parasite interactions (pp. 5–26). Wallingford: CABI.

    Google Scholar 

  • Inaba, T., & Morinaka, T. (1984). Heterothallism in Peronospora effusa. Phytopathology, 74, 214–216.

    Article  Google Scholar 

  • Inaba, T., Tkahashi, K., & Morinaka, T. (1983). Seed transmission of spinach downy mildew. Plant Disease, 67, 1139–1141.

    Article  Google Scholar 

  • Irish, B. M. (2004). New races of the downy mildew pathogen of spinach, identification of molecular markers for disease resistance, and molecular diversity of spinach germplasm. Dissertation, University of Arkansas.

    Google Scholar 

  • Irish, B. M., Correll, J. C., Koike, S. T., Schafer, J., & Morelock, T. E. (2003). Identification and cultivar reaction to three new races of the spinach downy mildew pathogen from the United States and Europe. Plant Disease, 87, 567–572.

    Article  Google Scholar 

  • Irish, B. M., Correll, J. C., Raid, R. N., & Morelock, T. E. (2004). First report of Peronospora farinosa f. sp. spinaciae (race 5) of spinach in Florida. Plant Disease, 88, 84.

    Article  Google Scholar 

  • Irish, B. M., Correll, J. C., Koike, S. T., & Morelock, T. E. (2007). Three new races of the spinach downy mildew pathogen identified by a modified set of spinach differentials. Plant Disease, 91, 1392–1396.

    Article  Google Scholar 

  • Irish, B. M., Correll, J. C., Feng, C., Bentley, T., & de los Reyes, B. G. (2008). Characterization of a resistance locus (Pfs-1) to the spinach downy mildew pathogen (Peronospora farinosa f. sp. spinaciae) & development of a molecular marker linked to Pfs-1. Phytopathology, 98, 894–900.

    Article  PubMed  CAS  Google Scholar 

  • Ito, M., Ohmido, N., Akiyama, Y., Fukui, K., & Koba, T. (2000). Characterization of spinach chromosomes by condensation patterns and physical mapping of 5S and 45S rDNAs by FISH. Journal of the American Society for Horticultural Science, 125(1), 59–62.

    CAS  Google Scholar 

  • Janick, J., & Stevenson, E. C. (1954). A genetic study of the heterogametic nature of the staminate plant in spinach (Spinacia oleracea L.). Proceedings of the American Society for Horticultural Science, 63, 444–446.

    Google Scholar 

  • Khattak, J. Z. K., Torp, A. M., & Andersen, S. B. (2006). A genetic linkage map of spinacia oleracea and localization of a sex determination locus. Euphytica, 148, 311–318.

    Article  CAS  Google Scholar 

  • Lucier, G., & Plummer, C. (2004). Vegetable consumption expected to rise in 2004. Vegetables and melons outlook, Electronic Outlook Report from the Economic Research Service, United States Department of Agriculture VGS-302 April 21, 2004. From http://www.ers.usda.gov/publications/vgs/Apr04/vgs302.pdf.

  • McDowell, J. M., Cuzick, A., Can, C., Beynon, J., Dangl, J. L., & Holub, E. B. (2000). Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant Journal, 22, 523–529.

    Article  PubMed  CAS  Google Scholar 

  • McDowell, J. M., Williams, S. G., Funderburg, N. T., Eulgem, T., & Dangl, J. L. (2005). Genetic analysis of developmentally regulated resistance to downy mildew (Hyaloperonospora parasitica) in Arabidopsis thaliana. Molecular Plant-Microbe Interactions, 18, 1226–1234.

    Article  PubMed  CAS  Google Scholar 

  • Metzger, J. D., & Zeevaart, J. A. D. (1985). Spinacia oleracea. In A. H. Halevy (Ed.), Handbook of flowering, vol. IV (pp. 384–392). Boca Raton: CRC.

    Google Scholar 

  • Meyers, B. C., Kozik, A., Griego, A., Kuang, H., & Michelmore, R. W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell, 15, 809–834.

    Article  PubMed  CAS  Google Scholar 

  • Michelmore, R. W. (2003). The impact zone: genomics and breeding for durable disease resistance. Current Opinion in Plant Biology, 6, 397–404.

    Article  PubMed  Google Scholar 

  • Morelock, T. E. (1999). Spinach: variety test and description. Hortscience, 34(6), 987–988.

    Google Scholar 

  • Morelock, T. E., & Correll, J. C. (2001). Spinach breeding in Arkansas. Paper presented at the National Spinach Conference, Fayetteville, AR USA.

    Google Scholar 

  • Morelock, T. E., & Correll, J. C. (2003). Spinach breeding in the mid-south. Paper presented at the National Spinach Conference, AR USA, November.

    Google Scholar 

  • Morelock, T. E., & Correll, J. C. (2005). Spinach breeding in the mid-south. Paper presented at the National Spinach Conference., Fayetteville, AR USA, November.

    Google Scholar 

  • Morelock, T. E., & Correll, J. C. (2008). Spinach breeding. In J. Prohens & F. Nuez (Eds.), Vegetables I (pp. 183–212). New York: Springer.

    Google Scholar 

  • Noël, L., Moores, T. L., Van der Biezen, E. A., Parniske, M., Daniels, M. J., Parker, J. E., et al. (1999). Pronounced intra specific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell, 11, 2099–2111.

    Article  PubMed  Google Scholar 

  • Nonnicke, I. L. (1989). Vegetable production. Van Nostrand Runhold.

    Google Scholar 

  • Parker, J. E., Holub, E. B., Frost, L. N., Falk, A., Gunn, N. D., & Daniels, M. J. (1996). Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell, 8, 2033–2046.

    Article  PubMed  CAS  Google Scholar 

  • Parker, J. E., Coleman, M. J., Szabò, V., Frost, L. N., Schmidt, R., van der Biezen, E. A., et al. (1997). The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the Toll and interleukin-1 receptors with N and L6. Plant Cell, 9, 879–894.

    Article  PubMed  CAS  Google Scholar 

  • Prior, R. L. (2003).Spinach as a source of antioxidant phytochemicals with potential health effects. Paper presented at the National Spinach Conference, Fayetteville, AR. USA,, November.

    Google Scholar 

  • Rentel, M. C., Leonelli, L., Dahlbeck, D., Zhao, B., & Staskawicz, B. J. (2008). Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proceedings of the National Academy of Sciences USA, 105, 1091–1096.

    Article  CAS  Google Scholar 

  • Ryder, E. J. (1979). Leafy salad vegetables. New York: AVI.

    Google Scholar 

  • Schmitz-Linneweber, C., Maier, R. M., Alcaraz, J., Cottet, A., Herrmann, R Gl, & Mache, R. (2001). The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization. Plant Molecular Biology, 45, 307–315.

    Article  PubMed  CAS  Google Scholar 

  • Slusarenko, A. J., & Schlaich, N. L. (2003). Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Molecular Plant Pathology, 4, 159–170.

    Article  PubMed  Google Scholar 

  • Smith, P. G. (1950). Downy mildew immunity in spinach. Phytopathology, 40, 65–68.

    Google Scholar 

  • Smith, P. G., Webb, R. E., Millett, A. M., & Luhn, C. H. (1961). Downy mildew on spinach. California Agriculture, 15, 5.

    Google Scholar 

  • Smith, P. G., Webb, R. E., & Luhn, C. H. (1962). Immunity to race 2 of spinach downy mildew. Phytopathology, 52, 597–599.

    Google Scholar 

  • Sneep, J. (1958). The present position of spinach breeding. Euphytica, 7, 1–8.

    Article  Google Scholar 

  • Stern, D. B., & Palmer, J. D. (1986). Tripartite mitochondrial genome of spinach: physical structure, mitochondrial gene mapping, and locations of transposed chloroplast DNA sequences. Nucleic Acids Research, 14, 5651–5666.

    Article  PubMed  CAS  Google Scholar 

  • Timmis, J. N., & Scott, N. S. (1983). Sequence homology between spinach nuclear and chloroplast genomes. Nature, 305, 65–67.

    Article  CAS  Google Scholar 

  • United States Department of Agriculture – National Agricultural Statistics Service. (2008). From http://www.nass.usda.gov/QuickStats/index2.jsp

  • Van Damme, M., Andel, A., Huibers, R. P., Panstruga, R., Weisbeek, P. J., et al. (2005). Identification of Arabidopsis loci required for susceptibility to the downy mildew pathogen Hyaloperonospora parasitica. Molecular Plant-Microbe Interactions, 18, 583–592.

    Article  PubMed  Google Scholar 

  • van der Biezen, E. A., Freddie, C. T., Kahn, K., Parker, J. E., & Jones, J. D. (2002). Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signaling components. Plant Journal, 29, 439–451.

    Article  PubMed  Google Scholar 

  • Walker, J. C. (1952). Diseases of vegetable crops. New York: McGraw Hill.

    Google Scholar 

  • Whisson, D. L., & Scott, N. S. (1985). Nuclear and mitochondrial DNA have sequence homology with a chloroplast gene. Plant Molecular Biology, 4, 267–273.

    Article  CAS  Google Scholar 

  • Wiant, J. S. (1937). White rust on Texas spinach. Plant Disease Reporter, 21, 114–115.

    Google Scholar 

  • Wilson, G. W. (1907). Studies in North American Peronosporales. I. The genus Albugo. Torrey Botanical Club Bulletin, 3461–3485.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Pathology, University of Arkansas, Fayetteville, AR, 72701, USA

    J. C. Correll, B. H. Bluhm & C. Feng

  2. Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN, 37996, USA

    K. Lamour

  3. Washington State University, Mount Vernon, WA, 98273-4768, USA

    L. J. du Toit

  4. University of California Cooperative Extension, Salinas, CA, 93901, USA

    S. T. Koike

Authors
  1. J. C. Correll
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. H. Bluhm
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Lamour
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. J. du Toit
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. T. Koike
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. C. Correll .

Editor information

Editors and Affiliations

  1. Palacký University in Olomouc, Olomouc-Holice, Czech Republic

    Aleš Lebeda

  2. Valent USA Corporation, Alex, NC, USA

    Gerald J Holmes

  3. University of Neuchâtel, Neuchâtel, Switzerland

    Brigitte Mauch-Mani

  4. Imperial College London, Ascot, UK

    Michael J. Jeger

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Correll, J.C., Bluhm, B.H., Feng, C., Lamour, K., du Toit, L.J., Koike, S.T. (2010). Spinach: better management of downy mildew and white rust through genomics. In: Lebeda, A., Holmes, G.J., Mauch-Mani, B., Jeger, M.J. (eds) The Downy Mildews - Biology, Mechanisms of Resistance and Population Ecology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1281-2_5

Download citation

  • DOI: https://doi.org/10.1007/978-94-007-1281-2_5

  • Accepted:

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-007-1280-5

  • Online ISBN: 978-94-007-1281-2

  • eBook Packages: Biomedical and Life Sciences (R0)

Publish with us

Policies and ethics

Search

Navigation