The repertoire of effector candidates in Colletotrichum lindemuthianum reveals important information about Colletotrichum genus lifestyle

  • Casley Borges de Queiroz
  • Hilberty L. Nunes Correia
  • Mateus Ferreira Santana
  • Diego Silva Batista
  • Pedro M. Pereira Vidigal
  • Sérgio Hermínio Brommonschenkel
  • Marisa Vieira de QueirozEmail author
Genomics, transcriptomics, proteomics


The fungus Colletotrichum lindemuthianum is the causal agent of anthracnose in the common bean (Phaseolus vulgaris), and anthracnose is one of the most devastating diseases of this plant species. However, little is known about the proteins that are essential for the fungus-plant interactions. Knowledge of the fungus’ arsenal of effector proteins is of great importance for understanding this pathosystem. In this work, we analyzed for the first time the arsenal of Colletotrichum lindemuthianum effector candidates (ClECs) and compared them with effector proteins from other species of the genus Colletotrichum, providing a valuable resource for studying the infection mechanisms of these pathogens in their hosts. Isolates of two physiological races (83.501 and 89 A2 2-3) of C. lindemuthianum were used to predict 353 and 349 ClECs, respectively. Of these ClECs, 63% were found to be rich in cysteine, have repetitive sequences of amino acids, and/or possess nuclear localization sequences. Several conserved domains were found between the ClECs. We also applied the effector prediction to nine species in the genus Colletotrichum, and the results ranged from 247 predicted effectors in Colletotrichum graminicola to 446 in Colletotrichum orbiculare. Twelve conserved domains were predicted in the effector candidates of all analyzed species of Colletotrichum. An expression analysis of the eight genes encoding the effector candidates in C. lindemuthianum revealed their induction during the biotrophic phase of the fungus on the bean.


Anthracnose Fungal pathogenicity Fungal effector biology Small secreted proteins 



This work was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais – FAPEMIG, and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). We are grateful to the Núcleo de Análises de Biomoléculas (NuBioMol) of the Universidade Federal de Viçosa for providing the facilities for the data analysis.


This work was supported by Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

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  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410CrossRefPubMedGoogle Scholar
  2. Alzate-Marin AL, Barros EG, Moreira MA (1999) Co-evolution model of Colletotrichum lindemuthianum (Melanconiaceae, Melanconiales) races that occur in some Brazilian regions. Genet Mol Biol 22(1):115–118. CrossRefGoogle Scholar
  3. Asai S, Shirasu K (2015) Plant cells under siege: plant immune system versus pathogen effectors. Curr Opin Plant Biol 28:1–8. CrossRefPubMedGoogle Scholar
  4. Azmi NSA, Singkaravanit-Ogawa S, Ikeda K, Kitakura S, Inoue Y, Narusaka Y, Shirasu K, Kaido M, Mise K, Takano Y (2018) Inappropriate expression of an NLP effector in Colletotrichum orbiculare impairs infection on Cucurbitaceae cultivars via plant recognition of the C-Terminal region. Mol Plant-Microbe Interact 31(1):101–111. CrossRefPubMedGoogle Scholar
  5. Barrus MF (1918) Varietal susceptibility of beans to strains of Colletotrichum lindemuthianum (Sacc. & Magn.) B & C. Phytopathology 8:589–605Google Scholar
  6. Bhadauria V, Banniza S, Vandenberg A, Selvaraj G, Wei Y (2013) Overexpression of a novel biotrophy-specific Colletotrichum truncatum effector, CtNUDIX, in hemibiotrophic fungal phytopathogens causes incompatibility with their host plants. Eukaryot Cell 12(1):2–11. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bhadauria V, MacLachlan R, Pozniak C, Banniza S (2015) Candidate effectors contribute to race differentiation and virulence of the lentil anthracnose pathogen Colletotrichum lentis. BMC Genomics 16:628. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Blümke A, Falter C, Herrfurth C, Sode B, Bode R, Schäfer W, Feussner I, Voigt CA (2014) Secreted fungal effector lipase releases free fatty acids to inhibit innate immunity-related callose formation during wheat head infection. Plant Physiol 165(1):346–358. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bolton MD, van Esse HP, Vossen JH, de Jonge R, Stergiopoulos I, Stulemeijer IJ, van den Berg GC, Borrás-Hidalgo O, Dekker HL, de Koster CG, de Wit PJ, Joosten MH, Thomma BP (2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 69(1):119–136. CrossRefPubMedGoogle Scholar
  10. Bruns S, Kniemeyer O, Hasenberg M, Aimanianda V, Nietzsche S, Thywissen A, Jeron A, Latgé JP, Brakhage AA, Gunzer M (2010) Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog 6(4):e1000873. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cao Y, Liang Y, Tanaka K, Nguyen CT, Jedrzejczak RP, Joachimiak A, Stacey G (2014) The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 3.
  12. Chakrabartya AM (2016) Bacterial azurin in potential cancer therapy. Cell Cycle 15(13):1665–1666. CrossRefGoogle Scholar
  13. Chen S, Songkumarn P, Venu RC, Gowda M, Bellizzi M, Hu J, Liu W, Ebbole D, Meyers B, Mitchell T, Wang GL (2013) Identification and characterization of in planta-expressed secreted effector proteins from Magnaporthe oryzae that induce cell death in rice. Mol Plant-Microbe Interact 26(2):191–202. CrossRefPubMedGoogle Scholar
  14. Cheng Q, Wang H, Xu B, Zhu S, Hu L, Huang M (2014) Discovery of a novel small secreted protein family with conserved N-terminal IGY motif in Dikarya fungi. BMC Genomics 15:1151. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Crouch JA, O’Connell R, Gan P, Buiate E, Torres MF, Beirn L, Shirasu K, Vaillancourt L (2014) The genomics of Colletotrichum. In: Dean RA, Lichens-Park A, Kole C (eds) Genomics of plant-associated fungi: monocot pathogens. Springer Verlag, Berlin, pp 69–102.
  16. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329(5994):953–955. CrossRefPubMedGoogle Scholar
  17. Dean R, van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13(4):414–430. CrossRefPubMedGoogle Scholar
  18. Delmas S, Pullan ST, Gaddipati S, Kokolski M, Malla S, Blythe MJ, Ibbett R, Campbell M, Liddell S, Aboobaker A, Tucker GA, Archer DB (2012) Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 8(8):e1002875. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Schwarz H, Macek B, Mann M, Kahmann R (2011) Metabolic priming by a secreted fungal effector. Nature 478(7369):395–398. CrossRefGoogle Scholar
  20. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11(8):539–548. CrossRefPubMedGoogle Scholar
  21. Dong S, Kong G, Qutob D, Yu X, Tang J, Kang J, Dai T, Wang H, Gijzen M, Wang Y (2012) The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol Plant-Microbe Interact 25(7):896–909. CrossRefPubMedGoogle Scholar
  22. Doré J, Kohler A, Dubost A, Hundley H, Singan V, Peng Y, Kuo A, Grigoriev IV, Martin F, Marmeisse R, Gay G (2017) The ectomycorrhizal basidiomycete Hebeloma cylindrosporum undergoes early waves of transcriptional reprogramming prior to symbiotic structures differentiation. Environ Microbiol 19(3):1338–1354. CrossRefPubMedGoogle Scholar
  23. dos Santos LV, de Queiroz MV, Santana MF, Soares MA, de Barros EG, de Araújo EF, Langin T (2012) Development of new molecular markers for the Colletotrichum genus using RetroCl1 sequences. World J Microbiol Biotechnol 28(3):1087–1095. CrossRefPubMedGoogle Scholar
  24. Eisenhaber B, Schneider G, Wildpaner M, Eisenhaber F (2004) A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J Mol Biol 337(2):243–253. CrossRefPubMedGoogle Scholar
  25. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300(4):1005–1016. CrossRefPubMedGoogle Scholar
  26. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2(4):953–971. CrossRefPubMedGoogle Scholar
  27. Fellbrich G, Romanski A, Varet A, Blume B, Brunner F, Engelhardt S, Felix G, Kemmerling B, Krzymowska M, Nürnberger T (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J 32(3):375–390CrossRefPubMedGoogle Scholar
  28. Ferreira JJ, Campa A, Kelly JD (2013) Organization of genes conferring resistance to anthracnose in common bean. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding: biotic stress. Wiley-Blackwell, New York, pp 151–176. CrossRefGoogle Scholar
  29. Fontenelle MR, Santana MF, Cnossen A, Bazzolli DMS, Bromonschenkel SH, Araújo EF, Queiroz MV (2017) Differential expression of genes during the interaction between Colletotrichum lindemuthianum and Phaseolus vulgaris. Eur J Plant Pathol 147(3):653–670.
  30. Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, Eckert MR, Cattolico L, Bernard-Samain S, Balesdent MH, Rouxel T (2007) Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol Plant-Microbe Interact 20(4):459–470CrossRefPubMedGoogle Scholar
  31. Gan P, Narusaka M, Kumakura N, Tsushima A, Takano Y, Narusaka Y, Shirasu K (2016) Genus-wide comparative genome analyses of Colletotrichum species reveal specific gene family losses and gains during adaptation to specific infection lifestyles. Genome Biol Evol 8(5):1467–1481. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Garnica DP, Upadhyaya NM, Dodds PN, Rathjen JP (2013) Strategies for wheat stripe rust pathogenicity identified by transcriptome sequencing. PLoS One 8(6):e67150. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gehring C (2010) Adenyl cyclases and cAMP in plant signaling - past and present. Cell Commun Signal 8:15. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Giraldo MC, Valent B (2013) Filamentous plant pathogen effectors in action. Nat Rev Microbiol 11(11):800–814. CrossRefPubMedGoogle Scholar
  35. Gladyshev E (2017) Repeat-induced point mutation and other genome defense mechanisms in fungi. Microbiol Spectr 5(4).
  36. Gladyshev E, Kleckner N (2017) Recombination-independent recognition of DNA homology for repeat-induced point mutation. Curr Genet 63(3):389–400. CrossRefPubMedGoogle Scholar
  37. Göhre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46:189–215. CrossRefPubMedGoogle Scholar
  38. González AM, Yuste-Lisbona FJ, Rodiño AP, De Ron AM, Capel C, García-Alcázar M, Lozano R, Santalla M (2015) Uncovering the genetic architecture of Colletotrichum lindemuthianum resistance through QTL mapping and epistatic interaction analysis in common bean. Front Plant Sci 6:141. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Guyon K, Balagué C, Roby D, Raffaele S (2014) Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics 15:336. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hacquard S, Joly DL, Lin YC, Tisserant E, Feau N, Delaruelle C, Legué V, Kohler A, Tanguay P, Petre B, Frey P, Van de Peer Y, Rouzé P, Martin F, Hamelin RC, Duplessis S (2012) A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). Mol Plant-Microbe Interact 25(3):279–293. CrossRefPubMedGoogle Scholar
  41. Hicks SW, Galán JE (2013) Exploitation of eukaryotic subcellular targeting mechanisms by bacterial effectors. Nat Rev Microbiol 11(5):316–326. CrossRefPubMedGoogle Scholar
  42. Hiruma K, Gerlach N, Sacristán S, Nakano RT, Hacquard S, Kracher B, Neumann U, Ramírez D, Bucher M, O'Connell RJ, Schulze-Lefert P (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165(2):464–474. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hofrichter M, Ullrich R (2006) Heme-thiolate haloperoxidases: versatile biocatalysts with biotechnological and environmental significance. Appl Microbiol Biotechnol 71(3):276–288. CrossRefPubMedGoogle Scholar
  44. Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35(Web Server):W585–W587CrossRefPubMedPubMedCentralGoogle Scholar
  45. Huang YJ, Li ZQ, Evans N Rouxel T, Fitt BDL, Balesdent MH (2006) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur J Plant Pathol 114(1):77–89. CrossRefGoogle Scholar
  46. Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26(5):680–682. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Irieda H, Maeda H, Akiyama K, Hagiwara A, Saitoh H, Uemura A, Terauchi R, Takano Y (2014) Colletotrichum orbiculare secretes virulence effectors to a biotrophic interface at the primary hyphal neck via exocytosis coupled with SEC22-mediated traffic. Plant Cell 26(5):2265–2281. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Izano EA, Amarante MA, Kher WB, Kaplan JB (2008) Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 74(2):470–476. CrossRefPubMedGoogle Scholar
  49. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19(15):4004–4014. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Jorda J, Kajava AV (2009) T-REKS: Identification of Tandem REpeats in sequences with a K-meanS based algorithm. Bioinformatics 25(20):2632–2638. CrossRefPubMedGoogle Scholar
  52. Käll L, Krogh A, Sonnhammer EL (2007) Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res 35(Web Server issue):W429–W432CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kang S, Lebrun MH, Farrall L, Valent B (2001) Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol Plant-Microbe Interact 14(5):671–674. CrossRefPubMedGoogle Scholar
  54. Kemen E, Kemen AC, Rafiqi M, Hempel U, Mendgen K, Hahn M, Voegele RT (2005) Identification of a protein from rust fungi transferred from haustoria into infected plant cells. Mol Plant-Microbe Interact 18(11):1130–1139. CrossRefPubMedGoogle Scholar
  55. Khang CH, Park SY, Lee YH, Valent B, Kang S (2008) Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Mol Plant-Microbe Interact 21(5):658–670. CrossRefPubMedGoogle Scholar
  56. Kleemann J, Rincon-Rivera LJ, Takahara H, Neumann U, Ver Loren van Themaat E, van der Does HC, Hacquard S, Stüber K, Will I, Schmalenbach W, Schmelzer E, O'Connell RJ (2012) Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum. PLoS Pathog 8(4):e1002643. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Koharudin LM, Debiec KT, Gronenborn AM (2015) Structural insight into fungal cell wall recognition by a CVNH protein with a single LysM domain. Structure 23(11):2143–2154. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Kolde R (2018) Package ‘pheatmap’ for R. Version 1.0.10. Accessed 21 Nov 2018
  59. Kombrink A, Rovenich H, Shi-Kunne X, Rojas-Padilla E, van den Berg GC, Domazakis E, de Jonge R, Valkenburg DJ, Sánchez-Vallet A, Seidl MF, Thomma BPI (2016) Verticillium dahliae LysM effectors differentially contribute to virulence on plant hosts. Mol Plant Pathol 18(4):596–608. CrossRefGoogle Scholar
  60. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408. CrossRefPubMedGoogle Scholar
  61. Lu S, Edwards MC (2016) Genome-wide analysis of small secreted cysteine-rich proteins identifies candidate effector proteins potentially involved in Fusarium graminearum-wheat interactions. Phytopathology 106(2):166–176. CrossRefPubMedGoogle Scholar
  62. Ma L, Cornelissen BJ, Takken FL (2013) A nuclear localization for Avr2 from Fusarium oxysporum is required to activate the tomato resistance protein I-2. Front Plant Sci 4:94.
  63. Ma Z, Song T, Zhu L, Ye W, Wang Y, Shao Y, Dong S, Zhang Z, Dou D, Zheng X, Tyler BM, Wang Y (2015) A Phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP. Plant Cell 27(7):2057–2072. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Mahuku GS, Riascos JJ (2004) Virulence and molecular diversity within Colletotrichum lindemuthianum isolates from Andean and Mesoamerican bean varieties and regions. Eur J Plant Pathol 110(3):253–263. CrossRefGoogle Scholar
  65. Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J, Hammond-Kosack KE, Thomma BP, Rudd JJ (2011) Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol 156(2):756–769. CrossRefPubMedPubMedCentralGoogle Scholar
  66. Mateos FV, Rickauer M, Esquerré-Tugayé MT (1997) Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities. Mol Plant-Microbe Interact 10(9):1045–1053. CrossRefPubMedGoogle Scholar
  67. Mejía LC, Herre EA, Sparks JP, Winter K, García MN, Van Bael SA, Stitt J, Shi Z, Zhang Y, Guiltinan MJ, Maximova SN (2014) Pervasive effects of a dominant foliar endophytic fungus on host genetic and phenotypic expression in a tropical tree. Front Microbiol 5:479. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BP, Talbot NJ (2012) Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24(1):322–335. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Mesarich CH, Bowen JK, Hamiaux C, Templeton MD (2015) Repeat-containing protein effectors of plant-associated organisms. Front Plant Sci 6:872. CrossRefPubMedPubMedCentralGoogle Scholar
  70. Morais do Amaral A, Antoniw J, Rudd JJ, Hammond-Kosack KE (2012) Defining the predicted protein secretome of the fungal wheat leaf pathogen Mycosphaerella graminicola. PLoS One 7(12):e49904. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21(4):1273–1290. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Mota SF, Barcelos QL, Dias MA, Souza EA (2016) Variability of Colletotrichum spp. in common bean. Genet Mol Res 15(2):gmr7176. CrossRefGoogle Scholar
  73. Newman AM, Cooper JB (2007) XSTREAM: a practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics 8:382. CrossRefPubMedPubMedCentralGoogle Scholar
  74. Nguyen Ba AN, Pogoutse A, Provart N, Moses AM (2009) NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:202. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Nogueira GB, dos Santos LV, Queiroz CB, Correa TLR, Menicucci RP, Bazzolli DMS, Araújo EF, Queiroz MV (2018) The histidine kinase slnCl1 of Colletotrichum lindemuthianum as a pathogenicity factor against Phaseolus vulgaris L. Microbiol Res 219:110–122. CrossRefGoogle Scholar
  76. O'Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, Damm U, Buiate EA, Epstein L, Alkan N, Altmüller J, Alvarado-Balderrama L, Bauser CA, Becker C, Birren BW, Chen Z, Choi J, Crouch JA, Duvick JP, Farman MA, Gan P, Heiman D, Henrissat B, Howard RJ, Kabbage M, Koch C, Kracher B, Kubo Y, Law AD, Lebrun MH, Lee YH, Miyara I, Moore N, Neumann U, Nordström K, Panaccione DG, Panstruga R, Place M, Proctor RH, Prusky D, Rech G, Reinhardt R, Rollins JA, Rounsley S, Schardl CL, Schwartz DC, Shenoy N, Shirasu K, Sikhakolli UR, Stüber K, Sukno SA, Sweigard JA, Takano Y, Takahara H, Trail F, van der Does HC, Voll LM, Will I, Young S, Zeng Q, Zhang J, Zhou S, Dickman MB, Schulze-Lefert P, Ver Loren van Themaat E, Ma LJ, Vaillancourt LJ (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44(9):1060–1065. CrossRefPubMedGoogle Scholar
  77. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kosti I, LaButti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GH, Lawrence C, Scott JA, Spatafora JW, Turgeon BG, de Wit PJ, Zhong S, Goodwin SB, Grigoriev IV (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 8(12):e1003037. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Padder BA, Sharma PN, Sharma OP, Kapoor V (2007) Genetic diversity and gene flow estimates among five populations of Colletotrichum lindemuthianum across Himachal Pradesh. Physiol Mol Plant Pathol 70:8–12. CrossRefGoogle Scholar
  79. Pareja-Jaime Y, Roncero MI, Ruiz-Roldán MC (2008) Tomatinase from Fusarium oxysporum f. sp. lycopersici is required for full virulence on tomato plants. Mol Plant-Microbe Interact 21(6):728–736. CrossRefPubMedGoogle Scholar
  80. Pattemore JA, Hane JK, Williams AH, Wilson BA, Stodart BJ, Ash GJ (2014) The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species. BMC Genomics 15:660. CrossRefPubMedPubMedCentralGoogle Scholar
  81. Percudani R, Montanini B, Ottonello S (2005) The anti-HIV cyanovirin-N domain is evolutionarily conserved and occurs as a protein module in eukaryotes. Proteins Struct Funct Genet 60(4):670–678. CrossRefPubMedGoogle Scholar
  82. Perfect SE, Hughes HB, O'Connell RJ, Green JR (1999) Colletotrichum: A model genus for studies on pathology and fungal-plant interactions. Fungal Genet Biol 27(2–3):186–198. CrossRefPubMedGoogle Scholar
  83. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785–786. CrossRefPubMedGoogle Scholar
  84. Petre B, Saunders DG, Sklenar J, Lorrain C, Win J, Duplessis S, Kamoun S (2015) Candidate effector proteins of the rust pathogen Melampsora larici-Populina target diverse plant cell compartments. Mol Plant-Microbe Interact 28(6):689–700. CrossRefPubMedGoogle Scholar
  85. Punj V, Das Gupta TK, Chakrabarty AM (2003) Bacterial cupredoxin azurin and its interactions with the tumor suppressor protein p53. Biochem Biophys Res Commun 312(1):109–114CrossRefPubMedGoogle Scholar
  86. Punj V, Bhattacharyya S, Saint-Dic D, Vasu C, Cunningham EA, Graves J, Yamada T, Constantinou AI, Christov K, White B, Li G, Majumdar D, Chakrabarty AM, Das Gupta TK (2004) Bacterial cupredoxin azurin as an inducer of apoptosis and regression in human breast cancer. Oncogene 23(13):2367–2378. CrossRefPubMedGoogle Scholar
  87. Queiroz CB, Correia HLN, Menicucci RP, Vidigal PMP, Queiroz MV (2017) Draft genome sequences of two isolates of Colletotrichum lindemuthianum, the causal agent of anthracnose in common beans. Genome Announc 5(18):e00214–e00217. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Qutob D, Kamoun S, Gijzen M (2002) Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J 32(3):361–373CrossRefPubMedGoogle Scholar
  89. Rafiqi M, Ellis JG, Ludowici VA, Hardham AR, Dodds PN (2012) Challenges and progress towards understanding the role of effectors in plant-fungal interactions. Curr Opin Plant Biol 15(4):477–482. CrossRefPubMedGoogle Scholar
  90. Redkar A, Villajuana-Bonequi M, Doehlemann G (2015) Conservation of the Ustilago maydis effector See1 in related smuts. Plant Signal Behav 10(12):e1086855. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Richard MM, Pflieger S, Sévignac M, Thareau V, Blanchet S, Li Y, Jackson SA, Geffroy V (2014) Fine mapping of Co-x, an anthracnose resistance gene to a highly virulent strain of Colletotrichum lindemuthianum in common bean. Theor Appl Genet 127(7):1653–1666. CrossRefPubMedGoogle Scholar
  92. Robin GP, Kleemann J, Neumann U, Cabre L, Dallery JF, Lapalu N, O'Connell RJ (2018) Subcellular localization screening of Colletotrichum higginsianum effector candidates identifies fungal proteins targeted to plant peroxisomes, golgi bodies, and microtubules. Front Plant Sci 9:562. CrossRefPubMedPubMedCentralGoogle Scholar
  93. Rodríguez-Guerra R, Acosta-Gallegos JA, González-Chavira MM, Simpson J (2006) Patotipos de Colletotrichum lindemuthianum y su implicación en la generación de cultivares resistentes de frijol. Agric Téc Méx 32:101–114Google Scholar
  94. Rose JK, Ham KS, Darvill AG, Albersheim P (2002) Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. Plant Cell 14(6):1329–1345CrossRefPubMedPubMedCentralGoogle Scholar
  95. Sánchez M, Colom F (2010) Extracellular DNase activity of Cryptococcus neoformans and Cryptococcus gattii. Rev Iberoam Micol 27(1):10–13. CrossRefPubMedGoogle Scholar
  96. Santhanam P, van Esse HP, Albert I, Faino L, Nürnberger T, Thomma BP (2013) Evidence for functional diversification within a fungal NEP1-Like protein family. Mol Plant-Microbe Interact 26(3):278–286. CrossRefPubMedGoogle Scholar
  97. Sanz-Martín JM, Pacheco-Arjona JR, Bello-Rico V, Vargas WA, Monod M, Díaz-Mínguez JM, Thon MR, Sukno SA (2016) A highly conserved metalloprotease effector enhances virulence in the maize anthracnose fungus Colletotrichum graminicola. Mol Plant Pathol 17(7):1048–1062. CrossRefPubMedGoogle Scholar
  98. Saunders DG, Win J, Cano LM, Szabo LJ, Kamoun S, Raffaele S (2012) Using hierarchical clustering of secreted protein families to classify and rank candidate effectors of rust fungi. PLoS One 7(1):e29847. CrossRefPubMedPubMedCentralGoogle Scholar
  99. Schornack S, van Damme M, Bozkurt TO, Cano LM, Smoker M, Thines M, Gaulin E, Kamoun S, Huitema E (2010) Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci U S A 107(40):17421–17426. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Schouten A, van Baarlen P, van Kan JA (2008) Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytol 177(2):493–505. CrossRefPubMedGoogle Scholar
  101. Schwartz HF, Steadman JR, Hall R, Forster RL (2005) Compendium of bean diseases. The American Phytopathological Society Press, St. PaulGoogle Scholar
  102. Selin C, de Kievit TR, Belmonte MF, Fernando WG (2016) Elucidating the role of effectors in plant-fungal interactions: progress and challenges. Front Microbiol 7:600. CrossRefPubMedPubMedCentralGoogle Scholar
  103. Selker EU (1990) Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet 24:579–5613CrossRefPubMedGoogle Scholar
  104. Selker EU, Cambareri EB, Jensen BC, Haack KR (1987) Rearrangement of duplicated DNA in specialised cells of Neurospora. Cell 51(5):741–752CrossRefPubMedGoogle Scholar
  105. Shan W, Cao M, Leung D, Tyler BM (2004) The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol Plant-Microbe Interact 17(4):394–403. CrossRefPubMedGoogle Scholar
  106. Soares MA, Nogueira GB, Bazzolli DMS, Araújo EF, Langin T, Queiroz MV (2014) PacCl, a pH-responsive transcriptional regulator, is essential in the pathogenicity of Colletotrichum lindemuthianum, a causal agent of anthracnose in bean plants. Eur J Plant Pathol 140(4):769–785. CrossRefGoogle Scholar
  107. Sperschneider J, Dodds PN, Gardiner DM, Singh KB, Taylor JM (2018) Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Mol Plant Pathol 19(9):2094–2110. CrossRefPubMedGoogle Scholar
  108. Takahara H, Hacquard S, Kombrink A, Hughes HB, Halder V, Robin GP, Hiruma K, Neumann U, Shinya T, Kombrink E, Shibuya N, Thomma BP, O'Connell RJ (2016) Colletotrichum higginsianum extracellular LysM proteins play dual roles in appressorial function and suppression of chitin-triggered plant immunity. New Phytol 211(4):1323–1337. CrossRefPubMedGoogle Scholar
  109. Takahashi M, Ashizawa T, Hirayae K, Moriwaki J, Sone T, Sonoda R, Noguchi MT, Nagashima S, Ishikawa K, Arai M (2010) One of two major paralogs of AVR-Pita1 is functional in Japanese rice blast isolates. Phytopathology 100(6):612–618. CrossRefPubMedGoogle Scholar
  110. Urban M, Cuzick A, Rutherford K, Irvine A, Pedro H, Pant R, Sadanadan V, Khamari L, Billal S, Mohanty S, Hammond-Kosack KE (2015) The Pathogen-Host Interactions database (PHI-base): additions and future developments. Nucleic Acids Res 45(D1):D604–D610. CrossRefGoogle Scholar
  111. Vargas WA, Sanz-Martín JM, Rech GE, Armijos-Jaramillo VD, Rivera LP, Echeverria MM, Díaz-Mínguez JM, Thon MR, Sukno SA (2016) A fungal effector with host nuclear localization and DNA-binding properties is required for maize anthracnose development. Mol Plant-Microbe Interact 29(2):83–95. CrossRefPubMedGoogle Scholar
  112. Veit S, Wörle JM, Nürnberger T, Koch W, Seitz HU (2001) A novel protein elicitor (PaNie) from Pythium aphanidermatum induces multiple defense responses in carrot, Arabidopsis, and tobacco. Plant Physiol 127(3):832–841CrossRefPubMedPubMedCentralGoogle Scholar
  113. Wartha F, Beiter K, Normark S, Henriques-Normark B (2007) Neutrophil extracellular traps: casting the NET over pathogenesis. Curr Opin Microbiol 10(1):52–56. CrossRefPubMedGoogle Scholar
  114. Wen F, White GJ, VanEtten HD, Xiong Z, Hawes MC (2009) Extracellular DNA is required for root tip resistance to fungal infection. Plant Physiol 151(2):820–829. CrossRefPubMedPubMedCentralGoogle Scholar
  115. Whisson S, Vetukuri R, Avrova A, Dixelius C (2012) Can silencing of transposons contribute to variation in effector gene expression in Phytophhthora infestans? Mob Genet Elem 2(2):110–114. CrossRefGoogle Scholar
  116. Xu C, Chen H, Gleason ML, Xu JR, Liu H, Zhang R, Sun G (2016) Peltaster fructicola genome reveals evolution from an invasive phytopathogen to an ectophytic parasite. Sci Rep 6:22926. CrossRefPubMedPubMedCentralGoogle Scholar
  117. Yan H, Zhou HF, Akk A, Hu Y, Springer LE, Ennis TL, Pham CTN (2016) Neutrophil proteases promote experimental abdominal aortic aneurysm via extracellular trap release and plasmacytoid dendritic cell activation. Arterioscler Thromb Vasc Biol 36(8):1660–1669. CrossRefPubMedPubMedCentralGoogle Scholar
  118. Yang Y, Zhang H, Li G, Li W, Wang X, Song F (2009) Ectopic expression of MgSM1, a cerato-platanin family protein from Magnaporthe grisea, confers broad-spectrum disease resistance in Arabidopsis. Plant Biotechnol J 7(8):763–777. CrossRefPubMedGoogle Scholar
  119. Yoshino K, Irieda H, Sugimoto F, Yoshioka H, Okuno T, Takano Y (2012) Cell death of Nicotiana benthamiana is induced by secreted protein NIS1 of Colletotrichum orbiculare and is suppressed by a homologue of CgDN3. Mol Plant-Microbe Interact 25(5):625–636. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Casley Borges de Queiroz
    • 1
  • Hilberty L. Nunes Correia
    • 1
  • Mateus Ferreira Santana
    • 1
  • Diego Silva Batista
    • 2
  • Pedro M. Pereira Vidigal
    • 3
  • Sérgio Hermínio Brommonschenkel
    • 4
  • Marisa Vieira de Queiroz
    • 1
    Email author
  1. 1.Laboratório de Genética Molecular de Fungos (LGMF)/BIOAGRO, Departamento de MicrobiologiaUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Universidade Estadual do MaranhãoSão LuísBrazil
  3. 3.Núcleo de Análise de Biomoléculas (NuBioMol), Centro de Ciências BiológicasUniversidade Federal de ViçosaViçosaBrazil
  4. 4.Departamento de FitopatologiaUniversidade Federal de ViçosaViçosaBrazil

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