Differential loss of effector genes in three recently expanded pandemic clonal lineages of the rice blast fungus

Abstract

Background: Understanding the mechanisms and timescales of plant pathogen outbreaks requires a detailed genome-scale analysis of their population history. The fungus Magnaporthe (Syn. Pyricularia) oryzae-the causal agent of blast disease of cereals-is among the most destructive plant pathogens to world agriculture and a major threat to the production of rice, wheat, and other cereals. Although M. oryzae is a multihost pathogen that infects more than 50 species of cereals and grasses, all rice-infecting isolates belong to a single genetically defined lineage. Here, we combined the two largest genomic datasets to reconstruct the genetic history of the rice-infecting lineage of M. oryzae based on 131 isolates from 21 countries. Results: The global population of the rice blast fungus consists mainly of three well-defined genetic groups and a diverse set of individuals. Multiple population genetic tests revealed that the rice-infecting lineage of the blast fungus probably originated from a recombining diverse group in Southeast Asia followed by three independent clonal expansions that took place over the last~200 years. Patterns of allele sharing identified a subpopulation from the recombining diverse group that introgressed with one of the clonal lineages before its global expansion. Remarkably, the four genetic lineages of the rice blast fungus vary in the number and patterns of presence and absence of candidate effector genes. These genes encode secreted proteins that modulate plant defense and allow pathogen colonization. In particular, clonal lineages carry a reduced repertoire of effector genes compared with the diverse group, and specific combinations of presence and absence of effector genes define each of the pandemic clonal lineages. Conclusions: Our analyses reconstruct the genetic history of the rice-infecting lineage of M. oryzae revealing three clonal lineages associated with rice blast pandemics. Each of these lineages displays a specific pattern of presence and absence of effector genes that may have shaped their adaptation to the rice host and their evolutionary history.

Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain

“…Although the high sequence divergence and elevated mutation rates among HMA sequences precluded rigorous dating of the emergence of these key adaptations, the low level of total nucleotide polymorphisms among closely related Pik alleles-in particular, the very few synonymous substitutions among Pikp-and Pikm-related alleles-points to a very recent emergence of the adaptive polymorphisms. Given that the rice-infecting lineage of M. oryzae is estimated to have arisen about 7,000-9,000 years ago (Couch et al, 2005;Latorre et al, 2020), our findings are consistent with the view that Pik-1 alleles evolved during rice domestication as previously suggested (Kanzaki et al, 2012;Zhai et al, 2011). In addition, AVR-Pik is widespread in rice-infecting isolates but absent in other blast fungus lineages (Langner et al, 2020;Latorre et al, 2020;Yoshida et al, 2016).…”

“…Given that the rice-infecting lineage of M. oryzae is estimated to have arisen about 7,000-9,000 years ago (Couch et al, 2005;Latorre et al, 2020), our findings are consistent with the view that Pik-1 alleles evolved during rice domestication as previously suggested (Kanzaki et al, 2012;Zhai et al, 2011). In addition, AVR-Pik is widespread in rice-infecting isolates but absent in other blast fungus lineages (Langner et al, 2020;Latorre et al, 2020;Yoshida et al, 2016). Therefore, it is tempting to speculate that the rice agroecosystem has created the ecological context that led to Pik neofunctionalization towards recognition of the new pathogen threat imposed by the blast fungus.…”

The allelic rice immune receptor Pikh confers extended resistance to strains of the blast fungus through a single polymorphism in the effector binding interface

“…Paired NLR receptors harbouring integrated domains are particularly prevalent in rice [31, 32], and account for some of the most well-characterised resistance genes against rice blast [33]. The effector complement of different blast strains shows signatures of rapid evolution, including presence/absence polymorphisms [34-37]. This allows the blast pathogen to break genetic resistance, producing disease outbreaks that threaten food production worldwide [1, 27, 38].…”

“…The sensor NLR Pik-1 harbours an integrated heavy metal associated (HMA) domain that directly binds AVR-Pik triggering immune responses [20, 21]. In contrast to other blast effectors such as AVR1-CO39 and AVR-Pii, which present presence/absence polymorphisms in blast genomes [34, 35, 42], AVR-Pik displays signatures of positive selection, and occurs as multiple effector variants [39, 43]. To date, six AVR-Pik variants (A to F) have been described [39, 44].…”

Population genomic evidence for a repeated introduction and rapid expansion in Europe of a maize fungal pathogen

“…Disease monitoring is greatly facilitated by genome sequencing to characterize pathogen diversity (Hubbard et al, 2015) although a sequence-based prediction of virulence types remains challenging due to a rapid evolution of pathogen genomes (Lamour et al, 2012;Raffaele et al, 2010;Dong et al, 2015;Thordal-Christensen et al, 2018;Frantzeskakis et al, 2019). Sequencing data were used to track the epidemiology and demographic history of pathogens (e.g., Gladieux et al, 2018;Stam et al, 2019;Latorre et al, 2020) and to reconstruct introductions (Yoshida et al, 2013).…”