Abstract
Downy mildew is an economically important and widespread disease in quinoa (Chenopodium quinoa) growing areas. Although in many studies Peronospora farinosa is most commonly regarded as the causal agent of the disease, identification and classification of the pathogen remain still uncertain due to its taxonomic confusion. Thirty-six Peronospora isolates from quinoa with different geographic origins including Argentina, Bolivia, Denmark, Ecuador, and Peru were morphologically and molecularly compared with Peronospora species from other Chenopodium species. The morphology of three herbarium specimens was similar to that of P. variabilis, which originated from C. album, characterized by flexuous to curved ultimate branchlets and pedicellated conidia. Phylogenetic analysis based on ITS rDNA sequences also placed the quinoa pathogen within the same clade as P. variabilis. Within the ITS rDNA sequences of the quinoa pathogens, two base substitutions were found, which separated the majority of the Danish isolates from isolates from South America, but no sequence difference was found among the isolates from different cultivars of quinoa. The present results indicate that the pathogen responsible for the quinoa downy mildew is identical to Peronospora variabilis and that it should not be lumped with P. farinosa as claimed previously by most studies.
Similar content being viewed by others
References
Galwey NW, Leakey CLA, Price KR, Fenwick GR. Chemical composition and nutritional characteristics of quinoa (Chenopodium quinoa Willd.). Food Sci Nutr. 1990;42F:245–61.
Jacobsen SE, Mujica A, Stolen O. Salt tolerance of quinoa during germination. Agron Trop Maracay. 1998;48:359–66.
Jensen CR, Jacobsen SE, Andersen MN, Nunez N, Andersen SD, Rasmussen L, et al. Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying. Eur J Agron. 2000;13:11–25.
Bhargava A, Shukla S, Ohri D. Chenopodium quinoa—an Indian perspective. Ind Crops Prod. 2006;23:73–87.
Danielsen S, Munk L. Evaluation of disease assessment methods in quinoa for their ability to predict yield losses caused by downy mildew. Crop Prot. 2004;23:219–28.
Kumar A, Bhargava A, Shukla S, Singh HB, Ohri D. Screening of exotic Chenopodium quinoa accessions for downy mildew resistance under mid-eastern conditions of India. Crop Prot. 2006;25:879–89.
Tewari JP, Boyetchko SM. Occurrence of Peronospora farinosa f. sp. chenopodii on quinoa in Canada. Can Plant Dis Surv. 1990;70:127–8.
García-Blázquez G, Constantinescu O, Tellería MT, Martín MP. Preliminary check list of Albuginales and Peronosporales (Chromista) reported from the Iberian Peninsula and Balearic Islands. Mycotaxon. 2006;98:185–8.
Danielsen S, Jacobsen SE, Hockenhull J. First report of downy mildew of quinoa caused by Peronospora farinosa f. sp. chenopodii in Denmark. Plant Dis. 2002;86:1175.
Choi YJ, Hong SB, Shin HD. Re-consideration of Peronospora farinosa infecting Spinacia oleracea as distinct species, Peronospora effusa. Mycol Res. 2007;111:381–91.
Voglmayr H. Phylogenetic relationships of Peronospora and related genera based on nuclear ribosomal ITS sequences. Mycol Res. 2003;107:1132–42.
Choi YJ, Denchev CM, Shin HD. Morphological and molecular analyses support the existence of host-specific Peronospora species infecting Chenopodium. Mycopathologia. 2008;165:155–64.
Thines M, Telle S, Ploch S, Runge F. Identity of the downy mildew pathogens on sage, basil and coleus, with implications for quarantine measures. Mycol Res. 2009;113:532–40.
García-Blázquez G, Göker M, Voglmayr H, Martín MP, Tellería MT, Oberwinkler F. Phylogeny of Peronospora, parasitic on Fabaceae, based on ITS sequences. Mycol Res. 2008;112:502–12.
Holmgren PK, Holmgren NH. Index herbariorum. New York Botanical Garden. http://sciweb.nybg.org/science2/indexHerbariorum.asp, 1998.
Lee SB, Taylor JW. Isolation of DNA from fungal mycelia and single spores. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press; 1990. p. 282–7.
Griffith GW, Shaw DS. Polymorphisms in Phytophthora infestans: Four mitochondrial haplotypes are detected after PCR amplification of DNA from pure cultures or from host lesions. Appl Environ Microb. 1998;64:4007–14.
Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier M. A molecular phylogeny of Phytophthora and related Oomycetes. Fungal Genet Biol. 2000;30:17–32.
White TJ, Bruns T, Lee S, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press; 1990. p. 315–22.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;24:4876–82.
Stamatakis E. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–90.
Ronquist F, Huelsenbeck JP. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.
Posada D, Crandall KA. Modeltest: testing the model of DNA substitution. Bioinformatics. 1998;14:817–8.
Swofford DL. PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4, Sunderland, Massachusetts, USA, Sinauer Associates, 2002.
Danielsen S, Ames T. El mildiu (Peronospora farinosa) de la Quinua (Chenopodium quinoa) en la zona Andina. Manual Práctico para el Estudio de la Enfermedad y del Patógeno. Lima, Peru, International Potato Center, 2000.
Yerkes WD, Shaw CG. Taxonomy of the Peronospora species on Cruciferae and Chenopodiaceae. Phytopathology. 1959;49:499–507.
Danielsen S, Lübeck M. Universally Primed-PCR indicates geographical variation of Peronospora farinosa ex. Chenopodium quinoa. J Basic Microbiol (accepted).
Intelmann F, Spring O. Analysis of total DNA by minisatellite and simple-sequence repeat primers for the use of population studies in Plasmopara halstedii. Can J Microbiol. 2002;48:555–9.
Roeckel-Drevet P, Tourvieille J, Gulya TJ, Charmet G, Nicolas P, Tourvieill de Labrouhe D. Molecular variability of sunflower downy mildew, Plasmopara halstedii, from different continents. Can J Microbiol. 2003;49:492–502.
Spring O, Bachofer M, Thines M, Riethmüller A, Göker M, Oberwinkler F. Intraspecific relationship of Phytophthora halstedii isolates differing in pathogenicity and geographic origin based on ITS sequence data. Eur J Plant Pathol. 2006;114:309–15.
Lindqvist H, Koponen H, Valkonen JPT. Variability of Peronospora sparsa (syn. P. rubi) in Finland as measured by amplified fragment length polymorphism. Eur J Plant Pathol. 2002;108:327–35.
Sukno SA, Taylor AM, Farman ML. Genetic uniformity among isolates of Peronospora tabacina, the tobacco blue mold pathogen. Phytopathology. 2002;92:1236–44.
Constantinescu O. The nomenclature of Plasmopara (Chromista, Peronosporales) parasitic on Geraniaceae. Taxon. 2004;53:523–5.
Voglmayr H, Fatehi J, Constantinescu O. Revision of Plasmopara (Chromista, Peronosporales) parasitic on Geraniaceae. Mycol Res. 2006;110:633–45.
Constantinescu O. Plasmopara orientalis sp. nov. (Chromista, Peronosporales). Sydowia. 2002;54:129–36.
Danielsen S, Mercado VH, Munk L, Ames T. Seed transmission of downy mildew (Peronospora farinosa f. sp. chenopodii) in quinoa and effect of relative humidity on seedling infection. Seed Sci Technol. 2004;32:91–8.
Aragón L, Gutiérrez W. El mildiu en cuatro especies de Chenopodium. Fitopatologia. 1991;27(2):104–9.
Acknowledgments
The authors are grateful to the curator of herbarium BPI for allowing access to specimens in their care.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Choi, YJ., Danielsen, S., Lübeck, M. et al. Morphological and Molecular Characterization of the Causal Agent of Downy Mildew on Quinoa (Chenopodium quinoa). Mycopathologia 169, 403–412 (2010). https://doi.org/10.1007/s11046-010-9272-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11046-010-9272-y