Influence of farming practices on the population genetics of the maize pathogen Cercospora zeina in South Africa.

Gray leaf spot (GLS) is an important foliar disease of maize. This disease, caused by Cercospora zeina, is prevalent in both smallholder and commercial maize farms in South Africa. Notably, smallholder practices are geared towards conservation agriculture, planting diverse maize genotypes within a field and avoiding chemical control. This study examined the population genetic structure of 129 C. zeina isolates from three smallholder farm sites in KwaZulu-Natal in South Africa using 13 microsatellite markers. These were analysed, together with 239 isolates previously analysed from four commercial farms in the same province, to determine whether farming systems influence the genetic diversity of C.zeina. In addition, we wanted to determine whether the smallholder farming system harboured a greater diversity of C.zeina haplotypes due to lack of chemical spraying of these crops. Overall, farming systems exhibited partial, but significant, population differentiation, contributing 10% of the genetic variation observed. A 16% genetic variation conferred between KwaNxamalala (smallholder) and Cedara (commercial) areas that are in close proximity, confirmed this. Private alleles accounted for 29% of the 52 alleles observed in smallholder farms. Smallholder farms harboured a higher gene and genotypic diversity, with a clonal fraction of only 13% compared to 32% in commercial farms. Mating type ratios indicative of sexual recombination and lower linkage disequilibrium in most smallholder populations were consistent with higher levels of diversity. This study suggests that commercial farming practices, such as fungicides and monoculture crop planting, may result in a narrower genetic diversity of the pathogen that is then propagated by asexual reproduction. In contrast, management of GLS disease in smallholder farms should consider the greater diversity of pathogen genotypes, especially if future research shows that this equates to a greater diversity of pathogenicity alleles.

Cercospora zeina from Maize in South Africa Exhibits High Genetic Diversity and Lack of Regional Population Differentiation.

South Africa is one of the leading maize-producing countries in sub-Saharan Africa. Since the 1980s, Cercospora zeina, a causal agent of gray leaf spot of maize, has become endemic in South Africa, and is responsible for substantial yield reductions. To assess genetic diversity and population structure of C. zeina in South Africa, 369 isolates were collected from commercial maize farms in three provinces (KwaZulu-Natal, Mpumalanga, and North West). These isolates were evaluated with 14 microsatellite markers and species-specific mating type markers that were designed from draft genome sequences of C. zeina isolates from Africa (CMW 25467) and the United States (USPA-4). Sixty alleles were identified across 14 loci, and gene diversity values within each province ranged from 0.18 to 0.35. High levels of gene flow were observed (Nm = 5.51), and in a few cases, identical multilocus haplotypes were found in different provinces. Overall, 242 unique multilocus haplotypes were identified with a low clonal fraction of 34%. No distinct population clusters were identified using STRUCTURE, principal coordinate analysis, or Weir's theta θ statistic. The lack of population differentiation was supported by analysis of molecular variance tests, which indicated that only 2% of the variation was attributed to variability between populations from each province. Mating type ratios of MAT1-1 and MAT1-2 idiomorphs from 335 isolates were not significantly different from a 1:1 ratio in all provinces, which provided evidence for sexual reproduction. The draft genome of C. zeina CMW 25467 exhibited a complete genomic copy of the MAT1-1 idiomorph as well as exonic fragments of MAT genes from both idiomorphs. The high level of gene diversity, shared haplotypes at different geographical locations within South Africa, and presence of both MAT idiomorphs at all sites indicates widespread dispersal of C. zeina between maize fields in the country as well as evidence for sexual recombination. The outcomes of this genome-enabled study are important for disease management since the high diversity has implications for dispersal of fungicide resistance should it emerge and the need for diversified resistance breeding.