Molecular Population Genetic Analysis Differentiates Two Virulence Mechanisms of the Fungal Avirulence Gene NIP1

Abstract

Deletion or alteration of an avirulence gene are two mechanisms that allow pathogens to escape recognition mediated by the corresponding resistance gene in the host. We studied these two mechanisms for the NIP1 avirulence gene in field populations of the fungal barley pathogen Rhynchosporium secalis. The product of the avirulence gene, NIP1, causes leaf necrosis and elicits a defense response on plants with the Rrs1 resistance gene. A high NIP1 deletion frequency (45%) was found among 614 isolates from different geographic populations on four continents. NIP1 was also sequenced for 196 isolates, to identify DNA polymorphisms and corresponding NIP1 types. Positive diversifying selection was found to act on NIP1. A total of 14 NIP1 types were found, 11 of which had not been described previously. The virulence of the NIP1 types was tested on Rrs1 and rrs1 barley lines. Isolates carrying three of these types were virulent on the Rrs1 cultivar. One type each was found in California, Western Europe, and Jordan. Additionally, a field experiment with one pair of near-isogenic lines was conducted to study the selection pressure imposed by Rrs1 on field populations of R. secalis. Deletion of NIP1 was the only mechanism used to infect the Rrs1 cultivar in the field experiment. In this first comprehensive study on the population genetics of a fungal avirulence gene, virulence to Rrs1 in R. secalis was commonly achieved through deletion of the NIP1 avirulence gene but rarely also through point mutations in NIP1.

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

“…A common evolutionary strategy for evading recognition is the loss of an entire avirulence gene (Schürch et al ., 2004; Mackey & McFall, 2006; de Jonge et al ., 2012; Hartmann et al ., 2017). However, loss of Avr3D1 was not observed in any of the 132 global strains, despite its location in a highly plastic genomic region, as shown by presence/absence polymorphisms for neighbouring genes and transposable elements.…”

Fine mapping, physical mapping and development of diagnostic markers for the Rrs2 scald resistance gene in barley

“…Overall, only a few cases are reported in the literature where fungal isolates were shown to break the Rrs2 mediated resistance of cultivar Atlas in Europe. The study of Schürch et al (2004) showed that two isolates (AU2 and RS88CA27) out of 41 tested were able to break the resistance. Lehnackers and Knogge (1990) identified four races which were able to complete the developmental cycle from spore germination to sporulation on Atlas.…”

A Single Binding Site Mediates Resistance- and Disease-Associated Activities of the Effector Protein NIP1 from the Barley Pathogen Rhynchosporium secalis

“…Of the remaining 16 variants, four have been studied in more detail. NIP1 types I and II, which were found in .50% of all NIP1-carrying fungal isolates (Schü rch et al, 2004), are elicitor active on Rrs1 barley, with type II showing somewhat lower activity than type I. In contrast, types III and IV are drastically less active or inactive (Rohe et al, 1995;Fiegen and Knogge, 2002).…”

“…secalis strains virulent on Rrs1 barley plants either lack the NIP1 gene or carry point mutations in the coding sequence that result in single amino acid alterations, which strongly reduce or abolish the biological activity of the gene product (Rohe et al, 1995). Comparison of the deduced amino acid sequences encoded by NIP1 alleles from more than 200 fungal isolates so far led to the classification of 18 NIP1 variants (Rohe et al, 1995;Schü rch et al, 2004), two of which may not be expressed properly due to mutations in the start codon and in the acceptor splice site, respectively. Of the remaining 16 variants, four have been studied in more detail.…”