Genome Analyses of an Aggressive and Invasive Lineage of the Irish Potato Famine Pathogen

Abstract

Pest and pathogen losses jeopardise global food security and ever since the 19th century Irish famine, potato late blight has exemplified this threat. The causal oomycete pathogen, Phytophthora infestans, undergoes major population shifts in agricultural systems via the successive emergence and migration of asexual lineages. The phenotypic and genotypic bases of these selective sweeps are largely unknown but management strategies need to adapt to reflect the changing pathogen population. Here, we used molecular markers to document the emergence of a lineage, termed 13_A2, in the European P. infestans population, and its rapid displacement of other lineages to exceed 75% of the pathogen population across Great Britain in less than three years. We show that isolates of the 13_A2 lineage are among the most aggressive on cultivated potatoes, outcompete other aggressive lineages in the field, and overcome previously effective forms of plant host resistance. Genome analyses of a 13_A2 isolate revealed extensive genetic and expression polymorphisms particularly in effector genes. Copy number variations, gene gains and losses, amino-acid replacements and changes in expression patterns of disease effector genes within the 13_A2 isolate likely contribute to enhanced virulence and aggressiveness to drive this population displacement. Importantly, 13_A2 isolates carry intact and in planta induced Avrblb1, Avrblb2 and Avrvnt1 effector genes that trigger resistance in potato lines carrying the corresponding R immune receptor genes Rpi-blb1, Rpi-blb2, and Rpi-vnt1.1. These findings point towards a strategy for deploying genetic resistance to mitigate the impact of the 13_A2 lineage and illustrate how pathogen population monitoring, combined with genome analysis, informs the management of devastating disease epidemics.

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

“…Effector genes are critical for the invasion, colonization, and reproduction of pathogens on hosts, and the finding of high genetic diversity in the effector gene Avr3a is consistent with the evolutionary hypothesis postulating that genes involving in antagonistic host‐pathogen coevolution have higher evolutionary rates compared to other genes as documented both in P. infestans (Cárdenas et al., 2011; de Vries et al., 2017) and many other species (Allen et al., 2004, 2008; Raffaele, Win, Cano, & Kamoun, 2010). This high evolutionary rate may well contribute to the rapid “breakdown” of many host resistances mediated by major genes (Cooke et al., 2012; Pilet et al., 2005). In previous studies, only two haplotypes formed by three SNPs were detected in 55 isolates of P. infestans (Armstrong et al., 2005) and six haplotypes generated by 12 SNPs were found in a different set of 88 sequences (Cárdenas et al., 2011).…”

“…Sequence analysis indicates that, as for many other effector genes (Cooke et al., 2012; Raffaele & Kamoun, 2012), various types of mutations are responsible for the level of genetic variation detected in Avr3a including point mutation, early termination, frameshift, and defeated start and stop codons (Figure 2a). Although nucleotide substitution was the main mechanism, other types of mutations account for ~15% of haplotype variation observed.…”

“…Functional redundancy encoded by multiple copies of effector genes relaxes selective pressure on one or more of the gene copies, which in turn allows more frequent and abrupt mutations to occur without severe impact on the fitness of the pathogen. Indeed, multiple mutation mechanisms including base substitution, deletion, pseudogenization, and transcriptional silencing have been documented in effector genes (Cooke et al., 2012; Raffaele & Kamoun, 2012). Interaction of these mutation events results in higher genetic variation in effector genes than in the rest of pathogen genome (Karasov, Horton, & Bergelson, 2014; Raffaele & Kamoun, 2012) and enhances response to selection driven by the change in host defense systems.…”

ANTICIPATORY BREEDING: MOLECULAR MARKERS AS A TOOL IN DEVELOPING DONORS OF POTATO (Solanum tuberosum L.) LATE BLIGHT RESISTANCE FROM COMPLEX INTERSPECIFIC HYBRIDS

“…de Bary remains one of the most economically significant potato diseases which results in losses of at least 15 % of yield annually, and global economic damage, including expenses for chemicals for pathogen control, amounts to 10 bln US dollars [1]. Late blight epidemics of new P. infestans races due to the pathogen evolution and migration periodically destroy up to 70-100 % of yield [2][3][4]. Thus, varieties with durable resistance to a wide range of P. infestans, ensuring significant preservation of plant productivity in case of changes of the pathogen race composition in agrocenosis, are required for successful potato farming.…”

Poppr: an R package for genetic analysis of populations with clonal or partially clonal reproduction

“…These approaches cannot be used as clonal populations violate basic assumptions of panmixia and Hardy-Weinberg equilibrium. Thus, model free methods such as those relying on k-means clustering, dendrograms including bootstrap support for clades, or minimum spanning networks are more appropriate [8][9][10]. Furthermore, analysis of mixed or clonal populations traditionally relies on calculation of diversity of genotypes observed and analysis of clone-censored versus non-censored populations [5,11,12].…”