Lessons in effector and NLR biology of plant-microbe systems

Białas, Aleksandra; Zess, Erin K.; Concepcion, Juan Carlos De la; Franceschetti, Marina; Pennington, Helen G.; Yoshida, Kentaro; Upson, Jessica; Chanclud, Emilie; Wu, Chih‐Hang; Langner, Thorsten; Maqbool, Abbas; Varden, Freya A.; Derevnina, Lida; Belhaj, Khaoula; Fujisaki, Koki; Saitoh, Hiromasa; Terauchi, Ryohei; Banfield, M.J.; Kamoun, Sophien

doi:10.1101/171223

Cited by 17 publications

(24 citation statements)

References 102 publications

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“…higher rate of non-synonymous over synonymous mutations) [24] . Loss of so-called AVR effector genes -activators of host immunoresponses-can dramatically impact the fitness of the blast fungus by enabling virulence on resistant host genotypes [22,26,27] .…”

Section: Introductionmentioning

confidence: 99%

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

Latorre

Reyes-Avila

Malmgren

et al. 2020

Preprint

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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 multiple genomics 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 of a diverse set of individuals and three well-defined genetic groups. Multiple population genetic tests revealed that the rice-infecting lineage of the blast fungus probably originated from a recombining diverse group in South East 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/absence of candidate effector genes. In particular, clonal lineages carry a reduced repertoire of effector genes compared with the diverse group, and specific combinations of effector presence/absence 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/absence of effector genes that may have shaped their adaptation to the rice host and their evolutionary history.

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Section: Introductionmentioning

confidence: 99%

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

Latorre

Reyes-Avila

Malmgren

et al. 2020

Preprint

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“…At the center of the co-evolutionary dynamics between pathogens and plants are effector proteins, i.e. secreted proteins that manipulate host processes to facilitate infection and colonization [32][33][34][35].In return, host plants have evolved immune receptors that can detect conserved molecular patterns and effector proteins to defend against invading pathogens [36,37]. This generally leads to fast-paced co-evolution between pathogens and their host plants that often follows arms-race dynamics where the frequency of adaptive mutations rises quickly in pathogen populations [16].…”

Section: Introductionmentioning

confidence: 99%

Genomic rearrangements generate hypervariable mini-chromosomes in host-specific lineages of the blast fungus

Langner

Harant

Gómez-Luciano

et al. 2020

Preprint

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Supernumerary mini-chromosomes-a unique type of genomic structural variation-have been implicated in the emergence of virulence traits in plant pathogenic fungi. However, the mechanisms that facilitate the emergence and maintenance of mini-chromosomes across fungi remain poorly understood. In the blast fungus Magnaporthe oryzae, mini-chromosomes have been first described in the early 1990s but, until very recently, have been overlooked in genomic studies. Here we investigated structural variation in four isolates of the blast fungus M. oryzae from different grass hosts and analyzed the sequences of mini-chromosomes in the rice, foxtail millet and goosegrass isolates. The mini-chromosomes of these isolates turned out to be highly diverse with distinct sequence composition. They are enriched in repetitive elements and have lower gene density than core-chromosomes. We identified several virulence-related genes in the mini-chromosome of the rice isolate, including the polyketide synthase Ace1 and the effector gene AVR-Pik. Macrosynteny analyses around these loci revealed structural rearrangements, including inter-chromosomal translocations between core-and mini-chromosomes. Our findings provide evidence that mini-chromosomes independently emerge from structural rearrangements of core-chromosomes and might contribute to adaptive evolution of the blast fungus. Author summaryThe genomes of plant pathogens often exhibit an architecture that facilitates high rates of dynamic rearrangements and genetic diversification in virulence associated regions. These regions, which tend to be gene sparse and repeat rich, are thought to serve as a cradle for adaptive evolution. Supernumerary chromosomes, i.e. chromosomes that are only present in some but not all individuals of a species, are a special type of structural variation that have been observed in plants, animals, and fungi. Here we identified and studied supernumerary mini-chromosomes in the blast fungus Magnaporthe oryzae, a pathogen that causes some of the most destructive plant diseases. We found that rice, foxtail millet and goosegrass isolates of this pathogen contain mini-chromosomes with distinct sequence composition. All minichromosomes are rich in repetitive genetic elements and have lower gene densities than core-chromosomes. Further, we identified virulence-related genes on the mini-chromosome of the rice isolate. We observed large-scale genomic rearrangements around these loci, indicative of a role of mini-chromosomes in facilitating genome dynamics. Taken together, our results indicate that mini-chromosomes facilitate genome rearrangements and possibly adaptive evolution of the blast fungus.

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“…Furthermore, unravelling the key residues from natural variations and their roles in determining the binding specificity between effector and NLR integrated domain reveals the molecular details of a recognition event. These studies underpin novel opportunities for future disease resistance engineering (Maqbool et al ., ; Bialas et al ., ; De la Concepcion et al ., ). So, further investigations that dissect the PsAvr3c/GmSKRP co‐crystal structure will help us test this hypothesis.…”

Section: Discussionmentioning

confidence: 99%

Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c

Huang

Chen

et al. 2018

New Phytologist

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Filamentous pathogens, such as fungi and oomycetes, secrete avirulence (AVR) effectors that trigger plant immune responses and provide striking examples of host adaptations. Avr effector genes display different types of allelic variations, including deletions, epigenetic silencing and sequence polymorphisms, to avoid detection. However, how effector sequence polymorphisms enable pathogens to dodge host immune surveillance remains largely unknown. PsAvr3c is a Phytophthora AVR gene that is recognized by soybean carrying Rps3c. PsAvr3c natural alleles display a rich diversity of single nucleotide polymorphisms in field isolates. We combined both site-directed mutagenesis and population sequence surveys to identify a serine substitution of glycine at position 174 in PsAvr3c that resulted in evasion of Rps3c-mediated soybean immunity. The S174G substitution did not affect the nuclear localization of PsAvr3c in planta, which is required to activate Rps3c, but it significantly impaired the binding affinity of PsAvr3c with a previously identified spliceosome-associated protein GmSKRPs. Silencing GmSKRPs specifically impaired PsAvr3c-triggered cell death in Rps3c soybean. This study uncovered a plant Phytophthora pathogen that adapted to a resistant plant through a key amino acid mutation and subsequently reduced the binding affinity with a plant immune regulator to evade host resistance.

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Lessons in effector and NLR biology of plant-microbe systems

Cited by 17 publications

References 102 publications

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

Recently expanded clonal lineages of the rice blast fungus display distinct patterns of presence/absence of effector genes

Genomic rearrangements generate hypervariable mini-chromosomes in host-specific lineages of the blast fungus

Natural allelic variations provide insights into host adaptation of Phytophthora avirulence effector PsAvr3c

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