Genetic variation for tolerance to the downy mildew pathogen Peronospora variabilis in genetic resources of quinoa (Chenopodium quinoa)

Abstract

Background Quinoa (Chenopodium quinoa Willd.) is an ancient grain crop that is tolerant to abiotic stress and has favorable nutritional properties. Downy mildew is the main disease of quinoa and is caused by infections of the biotrophic oomycete Peronospora variabilis Gaüm. Since the disease causes major yield losses, identifying sources of downy mildew tolerance in genetic resources and understanding its genetic basis are important goals in quinoa breeding. Results We infected 132 South American genotypes, three Danish cultivars and the weedy relative C. album with a single isolate of P. variabilis under greenhouse conditions and observed a large variation in disease traits like severity of infection, which ranged from 5 to 83%. Linear mixed models revealed a significant effect of genotypes on disease traits with high heritabilities (0.72 to 0.81). Factors like altitude at site of origin or seed saponin content did not correlate with mildew tolerance, but stomatal width was weakly correlated with severity of infection. Despite the strong genotypic effects on mildew tolerance, genome-wide association mapping with 88 genotypes failed to identify significant marker-trait associations indicating a polygenic architecture of mildew tolerance. Conclusions The strong genetic effects on mildew tolerance allow to identify genetic resources, which are valuable sources of resistance in future quinoa breeding.

A Review of Chenopodium quinoa (Willd.) Diseases—An Updated Perspective

“…The earliest report of downy mildew infecting quinoa in South America came from Martin Cardenas (1941), who found it infecting quinoa in Cochabamba, Bolivia, and identified it as P. farinosa [ 36 ]. P. variabilis has been documented throughout the world ( Figure 1 ) [ 26 , 29 , 30 , 31 , 32 , 37 , 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 50 , 51 , 52 ] wherever quinoa is cultivated. It is expected to become ubiquitous in all quinoa cropping areas as oospores found in seeds have also been seen in old dried leaves [ 32 , 53 , 54 ].…”

“…Moreover, C. album (known as goosefoot, fat hen, or lamb’s quarters) [ 55 ] is frequently infected by downy mildew throughout Europe because it is conspecific [ 56 ] with the P. variabilis from C. quinoa . Therefore, it is likely to be a reservoir for the pathogen and an alternative host [ 29 , 52 , 56 ]. Other Chenopodium species, such as C. murale L. (nettle leaf goosefoot), C. ambrosoides L. (Indian goosefoot, Mexican tea), C. berlandieri Moq.…”

“…These reports require further investigation to confirm the accurate identity of the pathogen. Cross-infection reported so far is solely that of P. variabilis isolated from C. album and C. quinoa [ 52 ].…”

“…In most downy mildews, the hyphae enter the leaf via stomatal pores [ 58 ] ( Figure 3 C). The formation of an appressorium-like swelling (penetration structures that exert pressure) on histopathological samples was observed under a microscope [ 52 , 59 ]. It penetrated the stomata ( Figure 3 B,D) but did not directly penetrate the cuticle [ 49 , 59 ].…”

“…A hypersensitive response has also been observed ( Figure 4 E,G). The sporulation presence differs considerably, probably due to cultivar responses and the pathogenic capability of the specific isolate [ 52 , 54 , 67 ].…”