7nlj › Citations

A single amino acid polymorphism in a conserved effector of the multihost blast fungus pathogen expands host-target binding spectrum.

<div class='caption-title'>APikL2 is conserved across different host-specific lineages of M. oryzae.</div>
<div class='caption-title'>APikL2 sequence diversification is associated with host-specific lineages.</div>
<div class='caption-title'>The APikL2 locus is conserved across diverse genetic lineages of M. oryzae.</div>
Bentham AR, Petit-Houdenot Y, Win J, Chuma I, Terauchi R, Banfield MJ, Kamoun S, Langner T
OpenAccess logo PLoS Pathog 17 e1009957 (2021)
Cited: 24 times
EuropePMC logo PMID: 34758051

Abstract

Accelerated gene evolution is a hallmark of pathogen adaptation and specialization following host-jumps. However, the molecular processes associated with adaptive evolution between host-specific lineages of a multihost plant pathogen remain poorly understood. In the blast fungus Magnaporthe oryzae (Syn. Pyricularia oryzae), host specialization on different grass hosts is generally associated with dynamic patterns of gain and loss of virulence effector genes that tend to define the distinct genetic lineages of this pathogen. Here, we unravelled the biochemical and structural basis of adaptive evolution of APikL2, an exceptionally conserved paralog of the well-studied rice-lineage specific effector AVR-Pik. Whereas AVR-Pik and other members of the six-gene AVR-Pik family show specific patterns of presence/absence polymorphisms between grass-specific lineages of M. oryzae, APikL2 stands out by being ubiquitously present in all blast fungus lineages from 13 different host species. Using biochemical, biophysical and structural biology methods, we show that a single aspartate to asparagine polymorphism expands the binding spectrum of APikL2 to host proteins of the heavy-metal associated (HMA) domain family. This mutation maps to one of the APikL2-HMA binding interfaces and contributes to an altered hydrogen-bonding network. By combining phylogenetic ancestral reconstruction with an analysis of the structural consequences of allelic diversification, we revealed a common mechanism of effector specialization in the AVR-Pik/APikL2 family that involves two major HMA-binding interfaces. Together, our findings provide a detailed molecular evolution and structural biology framework for diversification and adaptation of a fungal pathogen effector family following host-jumps.

Reviews - 7nlj mentioned but not cited (1)

  1. Exploiting Structural Modelling Tools to Explore Host-Translocated Effector Proteins. Amoozadeh S, Johnston J, Meisrimler CN. Int J Mol Sci 22 12962 (2021)

Articles - 7nlj mentioned but not cited (2)

  1. Benchmarking AlphaFold for protein complex modeling reveals accuracy determinants. Yin R, Feng BY, Varshney A, Pierce BG. Protein Sci 31 e4379 (2022)
  2. A single amino acid polymorphism in a conserved effector of the multihost blast fungus pathogen expands host-target binding spectrum. Bentham AR, Petit-Houdenot Y, Win J, Chuma I, Terauchi R, Banfield MJ, Kamoun S, Langner T. PLoS Pathog 17 e1009957 (2021)


Reviews citing this publication (1)

  1. NLR receptors in plant immunity: making sense of the alphabet soup. Contreras MP, Lüdke D, Pai H, Toghani A, Kamoun S. EMBO Rep 24 e57495 (2023)

Articles citing this publication (20)

  1. Two NLR immune receptors acquired high-affinity binding to a fungal effector through convergent evolution of their integrated domain. Białas A, Langner T, Harant A, Contreras MP, Stevenson CE, Lawson DM, Sklenar J, Kellner R, Moscou MJ, Terauchi R, Banfield MJ, Kamoun S. Elife 10 e66961 (2021)
  2. Effector target-guided engineering of an integrated domain expands the disease resistance profile of a rice NLR immune receptor. Maidment JHR, Shimizu M, Bentham AR, Vera S, Franceschetti M, Longya A, Stevenson CEM, De la Concepcion JC, Białas A, Kamoun S, Terauchi R, Banfield MJ. Elife 12 e81123 (2023)
  3. Functional diversification gave rise to allelic specialization in a rice NLR immune receptor pair. De la Concepcion JC, Vega Benjumea J, Bialas A, Terauchi R, Kamoun S, Banfield MJ. Elife 10 e71662 (2021)
  4. A blast fungus zinc-finger fold effector binds to a hydrophobic pocket in host Exo70 proteins to modulate immune recognition in rice. De la Concepcion JC, Fujisaki K, Bentham AR, Cruz Mireles N, Sanchez de Medina Hernandez V, Shimizu M, Lawson DM, Kamoun S, Terauchi R, Banfield MJ. Proc Natl Acad Sci U S A 119 e2210559119 (2022)
  5. Disentangling the complex gene interaction networks between rice and the blast fungus identifies a new pathogen effector. Sugihara Y, Abe Y, Takagi H, Abe A, Shimizu M, Ito K, Kanzaki E, Oikawa K, Kourelis J, Langner T, Win J, Białas A, Lüdke D, Contreras MP, Chuma I, Saitoh H, Kobayashi M, Zheng S, Tosa Y, Banfield MJ, Kamoun S, Terauchi R, Fujisaki K. PLoS Biol 21 e3001945 (2023)
  6. Adaptive evolution in virulence effectors of the rice blast fungus Pyricularia oryzae. Le Naour-Vernet M, Charriat F, Gracy J, Cros-Arteil S, Ravel S, Veillet F, Meusnier I, Padilla A, Kroj T, Cesari S, Gladieux P. PLoS Pathog 19 e1011294 (2023)
  7. Microbial community composition in the rhizosphere of Pteris vittata and its effects on arsenic phytoremediation under a natural arsenic contamination gradient. Jia P, Li F, Zhang S, Wu G, Wang Y, Li JT. Front Microbiol 13 989272 (2022)
  8. Regressive evolution of an effector following a host jump in the Irish potato famine pathogen lineage. Zess EK, Dagdas YF, Peers E, Maqbool A, Banfield MJ, Bozkurt TO, Kamoun S. PLoS Pathog 18 e1010918 (2022)
  9. Structure-Aided Identification of an Inhibitor Targets Mps1 for the Management of Plant-Pathogenic Fungi. Kong Z, Zhang X, Zhou F, Tang L, Chen Y, Li S, Zhang X, Kuai L, Su W, Cui W, Cai J, Wang Y, Yang J, Peng YL, Wang D, Liu J. mBio 14 e0288322 (2023)
  10. Quantitative and qualitative plant-pathogen interactions call upon similar pathogenicity genes with a spectrum of effects. Langlands-Perry C, Pitarch A, Lapalu N, Cuenin M, Bergez C, Noly A, Amezrou R, Gélisse S, Barrachina C, Parrinello H, Suffert F, Valade R, Marcel TC. Front Plant Sci 14 1128546 (2023)
  11. Structured Framework and Genome Analysis of Magnaporthe grisea Inciting Pearl Millet Blast Disease Reveals Versatile Metabolic Pathways, Protein Families, and Virulence Factors. Reddy B, Mehta S, Prakash G, Sheoran N, Kumar A. J Fungi (Basel) 8 614 (2022)
  12. The Molecular Docking of MAX Fungal Effectors with Plant HMA Domain-Binding Proteins. Rozano L, Hane JK, Mancera RL. Int J Mol Sci 24 15239 (2023)
  13. Does a Similar 3D Structure Mean a Similar Folding Pathway? The Presence of a C-Terminal α-Helical Extension in the 3D Structure of MAX60 Drastically Changes the Folding Pathway Described for Other MAX-Effectors from Magnaporthe oryzae. Lahfa M, Mouhand A, de Guillen K, Barthe P, Kroj T, Padilla A, Roumestand C. Molecules 28 6068 (2023)
  14. Genomic biosurveillance detects a sexual hybrid in the sudden oak death pathogen. Hamelin RC, Bilodeau GJ, Heinzelmann R, Hrywkiw K, Capron A, Dort E, Dale AL, Giroux E, Kus S, Carleson NC, Grünwald NJ, Feau N. Commun Biol 5 477 (2022)
  15. Target degradation specificity of phytoplasma effector phyllogen is regulated by the recruitment of host proteasome shuttle protein. Suzuki M, Kitazawa Y, Iwabuchi N, Maejima K, Matsuyama J, Matsumoto O, Oshima K, Namba S, Yamaji Y. Mol Plant Pathol 25 e13410 (2024)
  16. Bacterial host adaptation through sequence and structural variations of a single type III effector gene. Lauber E, González-Fuente M, Escouboué M, Vicédo C, Luneau JS, Pouzet C, Jauneau A, Gris C, Zhang ZM, Pichereaux C, Carrère S, Deslandes L, Noël LD. iScience 27 109224 (2024)
  17. Bioengineering a plant NLR immune receptor with a robust binding interface toward a conserved fungal pathogen effector. Zdrzałek R, Xi Y, Langner T, Bentham AR, Petit-Houdenot Y, De la Concepcion JC, Harant A, Shimizu M, Were V, Talbot NJ, Terauchi R, Kamoun S, Banfield MJ. Proc Natl Acad Sci U S A 121 e2402872121 (2024)
  18. Effects of temperature and microwave on the stability of the blast effector complex APikL2A/sHMA25 as determined by molecular dynamics analyses. Zhao L, Zhang T, Luo Y, Li L, Cheng R, Shi Z, Wang G, Ren T. J Mol Model 29 134 (2023)
  19. Wheat blast: The last enemy of hunger fighters. Nizolli VO, Viana VE, Pegoraro C, Maia LCD, Oliveira AC. Genet Mol Biol 46 e20220002 (2023)
  20. Zinc-finger (ZiF) fold secreted effectors form a functionally diverse family across lineages of the blast fungus Magnaporthe oryzae. De la Concepcion JC, Langner T, Fujisaki K, Yan X, Were V, Lam AHC, Saado I, Brabham HJ, Win J, Yoshida K, Talbot NJ, Terauchi R, Kamoun S, Banfield MJ. PLoS Pathog 20 e1012277 (2024)


Quick links