Endemic and panglobal genetic groups, and divergence of host-associated forms in worldwide collections of the wheat leaf rust fungus Puccinia triticina as determined by genotyping by sequencing

Abstract

The wheat leaf rust fungus, Puccinia triticina, is found in the major wheat growing regions of the world and is a leading cause of yield loss in wheat. Populations of P. triticina are highly variable for virulence to resistance genes in wheat and adapt quickly to resistance genes in wheat cultivars. The objectives of this study were to determine the genetic relatedness of worldwide collections of P. triticina using restriction site associated genotyping by sequencing. A total of 558 isolates of P. triticina from wheat producing regions in North America, South America, Europe, the Middle East, Ethiopia, Russia, Pakistan, Central Asia, China, New Zealand, and South Africa were characterized at 6745 single nucleotide loci. Isolates were also tested for virulence to 20 near-isogenic lines that differ for leaf rust resistance genes. Populations that were geographically proximal were also more closely related for genotypes. In addition, groups of isolates within regions that varied for genotype were similar to groups from other regions, which indicated past and recent migration across regions. Isolates from tetraploid durum wheat in five different regions were highly related with distinct genotypes compared to isolates from hexaploid common wheat. Based on a molecular clock, isolates from durum wheat found only in Ethiopia were the first to diverge from a common ancestor form of P. triticina that is found on the wild wheat relative Aegilops speltoides, followed by the divergence of isolates found worldwide that are virulent to durum wheat, and then by isolates found on common wheat.

Fig. 1. Neighbor joining plot of Provesti’s genetic distance of Puccinia triticina genotypes based on 6745 SNP markers of 556 isolates in 11 regional populations.

NA North America; SA South America; EA East Africa; ME Middle East; NZ New Zealand; SAF South Africa; EU Europe; PK Pakistan; CN China; CA Central Asia; RU Russia.

Fig. 2. Average observed (H_o) and average expected (H_e) heterozygosity of 6745 SNP loci in 11 regional populations of Puccinia triticina.

NA North America; SA South America; EU Europe; ME Middle East; EA East Africa; RU Russia; PK Pakistan; CA Central Asia; CN China; New Zealand; SAF South Africa.

Fig. 3. Neighbor joining plots of 556 Puccinia triticina isolates in 40 MLG genotype groups in 11 regional populations.

NA North America; SA South America; EA East Africa; ME Middle East; NZ New Zealand; SAF South Africa; EU Europe; PK Pakistan; CN China; CA Central Asia; RU Russia. a Plot of Prevosti’s genetic distance of isolates in MLG groups based on 6745 SNP markers. Indicated clusters (A-O) of isolate groups have support values over 95% based on 1000 bootstrap samples. All bootstrap support values are indicated in supplemental Fig. 4. b Plot of Prevosti’s genetic distance of virulence to 20 Thatcher wheat lines near-isogenic for leaf rust resistance genes of isolates in 40 MLG genotype groups. Numbers of isolates in each region and MLG group are in Table 1.

Fig. 4. Percentage of Puccinia triticina isolates based on SNP genotype in 15 SNP genotype clusters (A-O) in 11 regional populations.

Numbers of isolates in each region are in Table 1.

Fig. 5. Neighbor joining plot of Puccinia triticina isolates in 40 genotype groups based on nucleotide diversity between and within groups of 6745 SNP markers.

Divergence times between groups were based on branch lengths scaled by 2x the genome-wide mutation rate. AEG isolates collected from Aegilops speltoides; NA North America; SA South America; EA East Africa; ME Middle East; NZ New Zealand; SAF South Africa; EU Europe; PK Pakistan; CN China; CA Central Asia; RU Russia.