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Structure Analysis Uncovers a Highly Diverse but Structurally Conserved Effector Family in Phytopathogenic Fungi

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  • Karine de Guillen
  • Diana Ortiz-Vallejo
  • Jérome Gracy
  • Elisabeth Fournier
  • Thomas Kroj
  • André Padilla

Abstract

Phytopathogenic ascomycete fungi possess huge effector repertoires that are dominated by hundreds of sequence-unrelated small secreted proteins. The molecular function of these effectors and the evolutionary mechanisms that generate this tremendous number of singleton genes are largely unknown. To get a deeper understanding of fungal effectors, we determined by NMR spectroscopy the 3-dimensional structures of the Magnaporthe oryzae effectors AVR1-CO39 and AVR-Pia. Despite a lack of sequence similarity, both proteins have very similar 6 β-sandwich structures that are stabilized in both cases by a disulfide bridge between 2 conserved cysteins located in similar positions of the proteins. Structural similarity searches revealed that AvrPiz-t, another effector from M. oryzae, and ToxB, an effector of the wheat tan spot pathogen Pyrenophora tritici-repentis have the same structures suggesting the existence of a family of sequence-unrelated but structurally conserved fungal effectors that we named MAX-effectors (Magnaporthe Avrs and ToxB like). Structure-informed pattern searches strengthened this hypothesis by identifying MAX-effector candidates in a broad range of ascomycete phytopathogens. Strong expansion of the MAX-effector family was detected in M. oryzae and M. grisea where they seem to be particularly important since they account for 5–10% of the effector repertoire and 50% of the cloned avirulence effectors. Expression analysis indicated that the majority of M. oryzae MAX-effectors are expressed specifically during early infection suggesting important functions during biotrophic host colonization. We hypothesize that the scenario observed for MAX-effectors can serve as a paradigm for ascomycete effector diversity and that the enormous number of sequence-unrelated ascomycete effectors may in fact belong to a restricted set of structurally conserved effector families.Author Summary: Fungal plant pathogens are of outstanding economic and ecological importance and cause destructive diseases on many cultivated and wild plants. Effector proteins that are secreted during infection to manipulate the host and to promote disease are a key element in fungal virulence. Phytopathogenic fungi possess huge effector repertoires that are dominated by hundreds of sequence-unrelated small secreted proteins. The molecular functions of this most important class of fungal effectors and the evolutionary mechanisms that generate this tremendous numbers of apparently unrelated proteins are largely unknown. By investigating the 3-dimensional structures of effectors from the rice blast fungus M. oryzae, we discovered an effector family comprising structurally conserved but sequence-unrelated effectors from M. oryzae and the phylogenetically distant wheat pathogen Pyrenophora tritici-repentis that we named MAX-effectors (M. oryzae Avrs and ToxB). Structure-informed searches of whole genome sequence databases suggest that MAX-effectors are present at low frequencies and with a patchy phylogenetic distribution in many ascomycete phytopathogens. They underwent strong lineage-specific expansion in fungi of the Pyriculariae family that contains M. oryzae where they seem particularly important during biotrophic plant colonization and account for 50% of the cloned Avr effectors and 5–10% of the effector repertoire. Based on our results on the MAX-effectors and the widely accepted concept that fungal effectors evolve according to a birth-and-death model we propose the hypothesis that the majority of the immense numbers of different ascomycete effectors could in fact belong to a limited set of structurally defined families whose members are phylogenetically related.

Suggested Citation

  • Karine de Guillen & Diana Ortiz-Vallejo & Jérome Gracy & Elisabeth Fournier & Thomas Kroj & André Padilla, 2015. "Structure Analysis Uncovers a Highly Diverse but Structurally Conserved Effector Family in Phytopathogenic Fungi," PLOS Pathogens, Public Library of Science, vol. 11(10), pages 1-27, October.
  • Handle: RePEc:plo:ppat00:1005228
    DOI: 10.1371/journal.ppat.1005228
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    References listed on IDEAS

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    1. Jonathan D. G. Jones & Jeffery L. Dangl, 2006. "The plant immune system," Nature, Nature, vol. 444(7117), pages 323-329, November.
    2. Joe Win & Ksenia V Krasileva & Sophien Kamoun & Ken Shirasu & Brian J Staskawicz & Mark J Banfield, 2012. "Sequence Divergent RXLR Effectors Share a Structural Fold Conserved across Plant Pathogenic Oomycete Species," PLOS Pathogens, Public Library of Science, vol. 8(1), pages 1-4, January.
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    1. Mark C. Derbyshire & Sylvain Raffaele, 2023. "Surface frustration re-patterning underlies the structural landscape and evolvability of fungal orphan candidate effectors," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Xin Zhang & Yang Liu & Guixin Yuan & Shiwei Wang & Dongli Wang & Tongtong Zhu & Xuefeng Wu & Mengqi Ma & Liwei Guo & Hailong Guo & Vijai Bhadauria & Junfeng Liu & You-Liang Peng, 2024. "The synthetic NLR RGA5HMA5 requires multiple interfaces within and outside the integrated domain for effector recognition," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Theodora Ijeoma Ekwomadu & Mulunda Mwanza, 2023. "Fusarium Fungi Pathogens, Identification, Adverse Effects, Disease Management, and Global Food Security: A Review of the Latest Research," Agriculture, MDPI, vol. 13(9), pages 1-20, September.
    4. Stella Cesari & Yuxuan Xi & Nathalie Declerck & Véronique Chalvon & Léa Mammri & Martine Pugnière & Corinne Henriquet & Karine Guillen & Vincent Chochois & André Padilla & Thomas Kroj, 2022. "New recognition specificity in a plant immune receptor by molecular engineering of its integrated domain," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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