Peronospora variabilis

Author: Maria G. Zambrano, University of Florida

Reviewed by: Jeffrey Rollins, University of Florida

Pathogen

Quinoa (Chenopodium quinoa) is a crop of major importance in the Andean region for its nutritional value. It is also currently produced in North America, Europe, and Asia. The most wide spread disease that affects this crop is quinoa downy mildew, caused by Peronospora variabilis. The disease can cause a loss of crop yield of up to 58% and is the most damaging threat to the crop.

Peronospora variabilis is an oomycete in the Peronosporaceae family. It is a biothophic, obligate parasite with the main host being quinoa. The pathogen has also been reported to infect Chenopodium album and Chenopodium murale; both edible and widespread in Europe and Asia. Although it was initially classified as Peronospora farinosa f. sp. chenopodii, it has now been classified as a different species based on molecular and morphological characteristics.

Peronospora variabilis has pale brown, mostly elipsoidal sporangia (frequently referred to as conidia for their ability to germinate directly). Its sporangiophores (or conidiophores) are colorless and slightly curved, the branches are subdichotomous and the ultimate branches mostly in pairs (2). It is heterothallic. The two mating types necessary for oospore production are present in most of the Andean region, where the sexual spores can be found in the fields (3). The hypae are aseptate and multinucleate.

Symptoms and Signs

Symptoms include the appearance of chlorotic spots or pink discoloration on the upper leaf surface. These spots later turn necrotic. The signs indicating the presence of this pathogen include dense tan or grey sporulation and orange oospores on the lower leaf surface. Leaves densely covered with spores ultimately fall off. When infection is systemic, the plant will show dwarfing and yellowing. Infection during early development of the plant will result in heavier defoliation.

Ecology and Spread

Downy mildews are favored by cold temperatures and high humidity. In the case of P. variabilis, humidity above 80% and temperatures between 13-18 C are conducive for the development of the disease. Sporangia are dispersed by wind and initiate polycyclic sproangium production and infection throughout the season. The sporangium germinates directly and penetrates the plant’s epidermis with an apressorium. The fungus then extends its hyphae through the intercellular spaces. When the mycelium reaches the underside of the leaf, sporangiophores are produced and projected on the lower surface of the leaf. The sporangia can repeat the cycle until the end of the season. Two different mating types can form an oospore, the sexual spore that is also the resting structure of the pathogen. The oospore overwinters on the plant’s seeds, debris, or in the soil. Oospores penetrate the leaf tissue through natural openings such as stomata. Free moisture allows germination of the oospores, initiating the cycle again. In addition to wind dispersal, the disease spreads through oospore-infected seeds (7). The infection in this case is systemic.

Geographic Distribution

Quinoa downy mildew is endemic to Ecuador, Bolivia, Peru, Chile, and Colombia (5). The disease has also been reported in the United States (12), Canada (13), Denmark (6), Portugal (9), Korea (1), and India (10).

Management

The identification and development of resistant cultivars is of prime importance in the prevention of damage caused by P. variabilis. Cultivars La Molina 89, Amarilla de Marangani, and Ingapirca, exhibit good levels of resistance to the pathogen (3). The high diversity of the quinoa crop in the Andean region offers hope for finding new resistant cultivars (8).

Cultural practices are used to manage the disease in the Andean region where most growers are low income and resource limited. These practices include crop rotation, reduction of free moisture in the field, and combining different crops. Reduction of free moisture in the field is the most effective of these practices and is achieved by spacing crop rows and improving water drainage.

Seed testing has been proposed in countries that plan to increase their production of the crop as a measure for management. PCR based methods have also been developed to detect the pathogen (11).

Diagnostic Procedures

Being the only oomycete that infects quinoa, the diagnosis of quinoa powdery mildew is mainly perfomed by visual confirmation of the characteristic sporangia on the lower surface of the leaves.

As the pathogen is an obligate biotroph, samples of P. variabilis can be kept on host tissue. The leaves with sporangia can be refrigerated at 5°C for up to two weeks.

For longer preservation of samples, the infected leaves can be frozen at -20°C for six months or the sporangia alone can be frozen in liquid nitrogen for several years (4).

Resources and References

1. Choi, Y. J., Choi, I. Y., Kim, J. S., and Shin, H. D. 2014. First Report of Quinoa Downy Mildew Caused by Peronospora variabilis in Republic of Korea. Plant Disease, (ja).
2. Choi, Y. J., Danielsen, S., Lübeck, M., Hong, S. B., Delhey, R., and Shin, H. D. 2010. Morphological and molecular characterization of the causal agent of downy mildew on quinoa (Chenopodium quinoa). Mycopathologia, 169(5): 403-412.
3. Danielsen, S. 2001. Heterothallism in Peronospora farinosa f. sp. chenopodii, the causal agent of downy mildew of quinoa (Chenopodium quinoa). Journal of basic microbiology, 41(5): 305-309.
4. Danielsen, S., and Ames, T. 2000. El mildiu (Peronospora farinosa) de la quinua (Chenopodium quinoa) en la zona andina. Centro Internacional de la Papa, Lima, Peru. 32 pp.
5. Danielsen, S., Jacobsen, S.E., Echegaray, J., and Ames T. 1999. Impact of downy mildew on the yield of quinoa. CIP program report, 2000. 397-401.
6. Danielsen, S., Jacobsen, S. E., and Hockenhull, J. 2002. First report of downy mildew of quinoa caused by Peronospora farinosa f. sp. chenopodii in Denmark. Plant Disease, 86(10): 1175-1175.
7. Danielsen, S., Mercado, V. H., Ames, T., and Munk, L. 2004. Seed transmission of downy mildew (Peronospora farinosa f. sp. chenopodii) in quinoa and effect of relative humidity on seedling infection. Seed Science and Technology, 32(1): 91-98.
8. Danielsen, S; L. Munk and R. Nelson. 2000b. AFLP and virulence markers for the characterization of Peronospora farinosa isolates from quinoa. Durable Disease Resistance Symposium, Nov. 28- Dec. 1. Ede, Wageningen. p. 38.
9. Garcia Blasquez, G., Constantinescu, O., Telleria, M.T., and Martin, M.P. 2006. Preliminary chack lists of Albuginales and Peronosporales (Chromista) reported from the Iberian Peninsula and Balearic Islands. Mycotaxon. 98: 185-188.
10. Kumar, A., Bhargava, A., Shukla, S., Singh, H.B., and Ohri, D. 2006. Screening of exotic Chenopodium quinoa accessions for downy mildew resistance under mid-eastern conditions of India. Crop Prot. 25: 879–89.
11. Testen, A. L., Jimenez-Gasco, M. D. M., Ochoa, J. B., and Backman, P. A. 2014. Molecular detection of Peronospora variabilis in quinoa seeds and phylogeny of the quinoa downy mildew pathogen in South America and the United States. Phytopathology, (ja).
12. Testen, A. L., McKemy, J. M., and Backman, P. A. 2012. First Report of Quinoa Downy Mildew Caused by Peronospora variabilis in the United States. Plant Disease. 96(1): 146-146.
13. Tewari, J.P., and Boyetchko, S.M. 1990. Occurrence of Peronospora farinosa f.sp. chenopodii on quinoa in Canada. Canadian Plant Disease Survey. 70: 127–128.

Acknowledgements

• National Institute of Food and Agriculture, U.S. Department of Agriculture, under Agreement No. 2011-41530-30708 as part of "Diagnostic Image Series Development for Supporting IPM in the Southern Region" (USDA-NIFA-RIPM-003351)