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Abstract

Expansins, cerato-platanins and swollenins (which we will henceforth refer to as expansin-related proteins) are a group of microbial proteins involved in microbe-plant interactions. Although they share very low sequence similarity, some of their composing domains are near-identical at the structural level. Expansin-related proteins have their target in the plant cell wall, in which they act through a non-enzymatic, but still uncharacterized, mechanism. In most cases, mutagenesis of expansin-related genes affects plant colonization or plant pathogenesis of different bacterial and fungal species, and thus, in many cases they are considered virulence factors. Additionally, plant treatment with expansin-related proteins activate several plant defenses resulting in the priming and protection towards subsequent pathogen encounters. Plant-defence responses induced by these proteins are reminiscent of pattern-triggered immunity or hypersensitive response in some cases. Plant immunity to expansin-related proteins could be caused by the following: (i) protein detection by specific host-cell receptors, (ii) alterations to the cell-wall-barrier properties sensed by the host, (iii) displacement of cell-wall polysaccharides detected by the host. Expansin-related proteins may also target polysaccharides on the wall of the microbes that produced them under certain physiological instances. Here, we review biochemical, evolutionary and biological aspects of these relatively understudied proteins and different immune responses they induce in plant hosts.

Funding
This study was supported by the:
  • Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (Award IN203720)
    • Principle Award Recipient: Mario Serrano
  • Consejo Nacional de Ciencia y Tecnología (Award 252551)
    • Principle Award Recipient: Claudia Martinez-Anaya
  • Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (Award IN211116 & IN211019)
    • Principle Award Recipient: Claudia Martinez-Anaya
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2020-11-02
2024-04-24
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References

  1. Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S et al. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 2015; 79:293–320 [View Article][PubMed]
    [Google Scholar]
  2. Phelan VV, Liu W-T, Pogliano K, Dorrestein PC. Microbial metabolic exchange—the chemotype-to-phenotype link. Nat Chem Biol 2012; 8:26–35 [View Article]
    [Google Scholar]
  3. Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH et al. The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 2012; 76:46–65 [View Article][PubMed]
    [Google Scholar]
  4. Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S et al. Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci U S A 2008; 105:16876–16881 [View Article][PubMed]
    [Google Scholar]
  5. Tancos MA, Lowe-Power TM, Peritore-Galve FC, Tran TM, Allen C et al. Plant-like bacterial expansins play contrasting roles in two tomato vascular pathogens. Mol Plant Pathol 2018; 19:1210–1221 [View Article][PubMed]
    [Google Scholar]
  6. Narváez-Barragán DA, Tovar-Herrera OE, Torres M, Rodríguez M, Humphris S et al. Expansin-like Exl1 from Pectobacterium is a virulence factor required for host infection, and induces a defence plant response involving ROS, and jasmonate, ethylene and salicylic acid signalling pathways in Arabidopsis thaliana. Sci Rep 2020; 10:7747 [View Article][PubMed]
    [Google Scholar]
  7. Liu J, Peng H, Cui J, Huang W, Kong L et al. Molecular characterization of a novel effector Expansin-like protein from Heterodera avenae that induces cell death in Nicotiana benthamiana. Sci Rep 2016; 6:35677 [View Article][PubMed]
    [Google Scholar]
  8. Georgelis N, Nikolaidis N, Cosgrove DJ. Bacterial expansins and related proteins from the world of microbes. Appl Microbiol Biotechnol 2015; 99:3807–3823 [View Article][PubMed]
    [Google Scholar]
  9. Kende H, Bradford K, Brummell D, Cho HT, Cosgrove D et al. Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 2004; 55:311–314 [View Article][PubMed]
    [Google Scholar]
  10. Chase WR, Zhaxybayeva O, Rocha J, Cosgrove DJ, Shapiro LR. Global cellulose biomass, horizontal gene transfers and domain fusions drive microbial expansin evolution. New Phytol 2020; 226:921–938 [View Article][PubMed]
    [Google Scholar]
  11. Pazzagli L, Cappugi G, Manao G, Camici G, Santini A, Cappugi G, Manao G et al. Purification, characterization, and amino acid sequence of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani. J Biol Chem 1999; 274:24959–24964 [View Article][PubMed]
    [Google Scholar]
  12. Santos CA, Ferreira-Filho JA, O'Donovan A, Gupta VK, Tuohy MG et al. Production of a recombinant swollenin from Trichoderma harzianum in Escherichia coli and its potential synergistic role in biomass degradation. Microb Cell Fact 2017; 16:83 [View Article][PubMed]
    [Google Scholar]
  13. Meng X, Miao Y, Liu Q, Ma L, Guo K et al. TgSWO from Trichoderma guizhouense NJAU4742 promotes growth in cucumber plants by modifying the root morphology and the cell wall architecture. Microb Cell Fact 2019; 18:148 [View Article][PubMed]
    [Google Scholar]
  14. Rocha J, Shapiro LR, Kolter R. A horizontally acquired expansin gene increases virulence of the emerging plant pathogen Erwinia tracheiphila. bioRxiv 2019681643
    [Google Scholar]
  15. Ingel B, Jeske DR, Sun Q, Grosskopf J, Roper MC. Xylella fastidiosa endoglucanases mediate the rate of pierce’s disease development in Vitis vinifera in a cultivar-dependent manner. Mol Plant Microbe Interact 2019; 32:1402–1414 [View Article][PubMed]
    [Google Scholar]
  16. Jahr H, Dreier J, Meletzus D, Bahro R, Eichenlaub R. The endo-beta-1,4-glucanase CelA of Clavibacter michiganensis subsp. michiganensis is a pathogenicity determinant required for induction of bacterial wilt of tomato. Mol Plant Microbe Interact 2000; 13:703–714 [View Article][PubMed]
    [Google Scholar]
  17. Frías M, González C, Brito N. BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host. New Phytol 2011; 192:483–495 [View Article][PubMed]
    [Google Scholar]
  18. Jeong JS, Mitchell TK, Dean RA. The Magnaporthe grisea snodprot1 homolog, msp1, is required for virulence. FEMS Microbiol Lett 2007; 273:157–165 [View Article][PubMed]
    [Google Scholar]
  19. Zhang Y, Gao Y, Liang Y, Dong Y, Yang X et al. The verticillium dahliae snodprot1-like protein VdCP1 contributes to virulence and triggers the plant immune system. Front Plant Sci 2017; 8:1–13 [View Article]
    [Google Scholar]
  20. Brotman Y, Briff E, Viterbo A, Chet I. Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 2008; 147:779–789 [View Article][PubMed]
    [Google Scholar]
  21. Wang T, Park YB, Caporini MA, Rosay M, Zhong L et al. Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls. Proc Natl Acad Sci U S A 2013; 110:16444–16449 [View Article][PubMed]
    [Google Scholar]
  22. Lombardi L, Faoro F, Luti S, Baccelli I, Martellini F et al. Differential timing of defense-related responses induced by cerato-platanin and cerato-populin, two non-catalytic fungal elicitors. Physiol Plant 2013; 149:n/a [View Article][PubMed]
    [Google Scholar]
  23. Martellini F, Faoro F, Carresi L, Pantera B, Baccelli I et al. Cerato-populin and cerato-platanin, two non-catalytic proteins from phytopathogenic fungi, interact with hydrophobic inanimate surfaces and leaves. Mol Biotechnol 2013; 55:27–42 [View Article][PubMed]
    [Google Scholar]
  24. Yang Y, Zhang H, Li G, Li W, Wang Xiao'e, Wang X et al. Ectopic expression of MgSM1, a cerato-platanin family protein from Magnaporthe grisea, confers broad-spectrum disease resistance in Arabidopsis. Plant Biotechnol J 2009; 7:763–777 [View Article][PubMed]
    [Google Scholar]
  25. Vargas WA, Djonović S, Sukno SA, Kenerley CM. Dimerization controls the activity of fungal elicitors that trigger systemic resistance in plants. J Biol Chem 2008; 283:19804–19815 [View Article][PubMed]
    [Google Scholar]
  26. Li S, Dong Y, Li L, Zhang Y, Yang X et al. The novel cerato-platanin-like protein FocCP1 from Fusarium oxysporum triggers an immune response in plants. Int J Mol Sci 2019; 20:2849 [View Article][PubMed]
    [Google Scholar]
  27. Frías M, Brito N, González M, González C. The phytotoxic activity of the cerato-platanin BcSpl1 resides in a two-peptide motif on the protein surface. Mol Plant Pathol 2014; 15:342–351 [View Article][PubMed]
    [Google Scholar]
  28. Pazzagli L, Seidl-Seiboth V, Barsottini M, Vargas WA, Scala A et al. Cerato-platanins: elicitors and effectors. Plant Sci 2014; 228:79–87 [View Article][PubMed]
    [Google Scholar]
  29. Tovar-Herrera OE, Batista-García RA, Sánchez-Carbente MdelR, Iracheta-Cárdenas MM, Arévalo-Niño K et al. A novel expansin protein from the white-rot fungus Schizophyllum commune. PLoS One 2015; 10:e0122296 [View Article][PubMed]
    [Google Scholar]
  30. Cosgrove DJ. Plant expansins: diversity and interactions with plant cell walls. Curr Opin Plant Biol 2015; 25:162–172 [View Article][PubMed]
    [Google Scholar]
  31. Olarte-Lozano M, Mendoza-Nuñez MA, Pastor N, Segovia L, Folch-Mallol J et al. PcExl1 a novel acid expansin-like protein from the plant pathogen Pectobacterium carotovorum, binds cell walls differently to BsEXLX1. PLoS One 2014; 9:e95638 [View Article][PubMed]
    [Google Scholar]
  32. Georgelis N, Tabuchi A, Nikolaidis N, Cosgrove DJ. Structure-function analysis of the bacterial expansin EXLX1. J Biol Chem 2011; 286:16814–16823 [View Article][PubMed]
    [Google Scholar]
  33. Georgelis N, Nikolaidis N, Cosgrove DJ. Biochemical analysis of expansin-like proteins from microbes. Carbohydr Polym 2014; 100:17–23 [View Article][PubMed]
    [Google Scholar]
  34. Price DC, Chan CX, Yoon HS, Yang EC, Qiu H et al. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 2012; 335:843–847 [View Article][PubMed]
    [Google Scholar]
  35. Darley CP, Li Y, Schaap P, McQueen-Mason SJ. Expression of a family of expansin-like proteins during the development of Dictyostelium discoideum. FEBS Lett 2003; 546:416–418 [View Article][PubMed]
    [Google Scholar]
  36. Lofgren LA, LeBlanc NR, Certano AK, Nachtigall J, LaBine KM et al. Fusarium graminearum: pathogen or endophyte of North American grasses?. New Phytol 2018
    [Google Scholar]
  37. Lohoff C, Buchholz PCF, Le Roes-Hill M, Pleiss J. The expansin engineering database: a navigation and classification tool for expansins and homologues. proteins. Struct Funct Bioinforma 2020; 1:
    [Google Scholar]
  38. Neil RB, Hite D, Kelrick MI, Lockhart ML, Lee K. Myxobacterial biodiversity in an established oak-hickory forest and a savanna restoration site. Curr Microbiol 2005; 50:88–95 [View Article][PubMed]
    [Google Scholar]
  39. Loria R, Kers J, Joshi M. Evolution of plant pathogenicity in Streptomyces. Annu Rev Phytopathol 2006; 44:469–487 [View Article][PubMed]
    [Google Scholar]
  40. Bae C, Han SW, Song YR, Kim BY, Lee HJ et al. Infection processes of xylem-colonizing pathogenic bacteria: possible explanations for the scarcity of qualitative disease resistance genes against them in crops. Theor Appl Genet 2015; 128:1219–1229 [View Article][PubMed]
    [Google Scholar]
  41. Nikolaidis N, Doran N, Cosgrove DJ. Plant expansins in bacteria and fungi: evolution by horizontal gene transfer and independent domain fusion. Mol Biol Evol 2014; 31:376–386 [View Article][PubMed]
    [Google Scholar]
  42. Smillie CS, Smith MB, Friedman J, Cordero OX, David LA et al. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 2011; 480:241–244 [View Article][PubMed]
    [Google Scholar]
  43. Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P et al. The timescale of early land plant evolution. Proc Natl Acad Sci U S A 2018; 115:E2274–E2283 [View Article][PubMed]
    [Google Scholar]
  44. McDonald BR, Currie CR. Lateral gene transfer dynamics in the ancient bacterial genus Streptomyces. mBio 2017; 8:e00644–17 [View Article][PubMed]
    [Google Scholar]
  45. Kikuchi T, Li H, Karim N, Kennedy MW, Moens M et al. Identification of putative expansin-like genes from the pine wood nematode, Bursaphelenchus xylophilus, and evolution of the expansin gene family within the Nematoda. Nematology 2009; 11:355–364
    [Google Scholar]
  46. Chen H, Kovalchuk A, Keriö S, Asiegbu FO. Distribution and bioinformatic analysis of the cerato-platanin protein family in Dikarya. Mycologia 2013; 105:1479–1488 [View Article][PubMed]
    [Google Scholar]
  47. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2014; 42:D490–D495 [View Article][PubMed]
    [Google Scholar]
  48. Pastor N, Dávila S, Pérez-Rueda E, Segovia L, Martínez-Anaya C. Electrostatic analysis of bacterial expansins. Proteins 2015; 83:215–223 [View Article][PubMed]
    [Google Scholar]
  49. Silveira RL, Skaf MS. Molecular dynamics of the Bacillus subtilis expansin EXLX1: interaction with substrates and structural basis of the lack of activity of mutants. Phys Chem Chem Phys 2016; 18:3510–3521 [View Article][PubMed]
    [Google Scholar]
  50. Tovar-Herrera OE, Rodríguez M, Olarte-Lozano M, Sampedro-Guerrero JA, Guerrero A et al. Analysis of the binding of expansin Exl1, from Pectobacterium carotovorum, to plant Xylem and comparison to EXLX1 from Bacillus subtilis. ACS Omega 2018; 3:7008–7018 [View Article][PubMed]
    [Google Scholar]
  51. Luti S, Martellini F, Bemporad F, Mazzoli L, Paoli P et al. A single amino acid mutation affects elicitor and expansins-like activities of cerato-platanin, a non-catalytic fungal protein. PLoS One 2017; 12:e0178337–18 [View Article][PubMed]
    [Google Scholar]
  52. de Oliveira AL, Gallo M, Pazzagli L, Benedetti CE, Cappugi G et al. The structure of the elicitor Cerato-platanin (CP), the first member of the CP fungal protein family, reveals a double ψβ-barrel fold and carbohydrate binding. J Biol Chem 2011; 286:17560–17568 [View Article][PubMed]
    [Google Scholar]
  53. de Barsottini MR, de Oliveira JF, Teixeira PJPL, Teixeira PJPL, do Prado PFV et al. Functional diversification of cerato-platanins in Moniliophthora perniciosa as seen by differential expression and protein function specialization. Mol Plant Microbe Interact 2013; 26:1281–1293 [View Article][PubMed]
    [Google Scholar]
  54. Baccelli I, Luti S, Bernardi R, Scala A, Pazzagli L. Cerato-Platanin shows expansin-like activity on cellulosic materials. Appl Microbiol Biotechnol 2014; 98:175–184 [View Article][PubMed]
    [Google Scholar]
  55. Baccelli I. Cerato-Platanin family proteins: one function for multiple biological roles?. Front Plant Sci 2014; 5:2013–2016 [View Article][PubMed]
    [Google Scholar]
  56. Frischmann A, Neudl S, Gaderer R, Bonazza K, Zach S et al. Self-assembly at air/water interfaces and carbohydrate binding properties of the small secreted protein EPL1 from the fungus Trichoderma atroviride. J Biol Chem 2013; 288:4278–4287 [View Article][PubMed]
    [Google Scholar]
  57. Carresi L, Pantera B, Zoppi C, Cappugi G, Oliveira AL et al. Cerato-Platanin, a phytotoxic protein from Ceratocystis fimbriata: expression in Pichia pastoris, purification and characterization. Protein Expr Purif 2006; 49:159–167 [View Article][PubMed]
    [Google Scholar]
  58. Quiroz-Castañeda RE, Martínez-Anaya C, Cuervo-Soto LI, Segovia L, Folch-Mallol JL. Loosenin, a novel protein with cellulose-disrupting activity from Bjerkandera adusta. Microb Cell Fact 2011; 10:8 [View Article][PubMed]
    [Google Scholar]
  59. Campos-Oliver A, Quiroz-Castañeda RE, Ortiz-Suri E, Folch-Mallol JL. Cloning and expression of a hypothetical Loosenin from Neurospora crassa. Rev Latinoam Biotecnol Ambient Algal 2014; 5:1–7 [View Article]
    [Google Scholar]
  60. Suzuki H, Vuong TV, Gong Y, Chan K, Ho C-Y et al. Sequence diversity and gene expression analyses of expansin-related proteins in the white-rot basidiomycete, Phanerochaete carnosa. Fungal Genet Biol 2014; 72:115–123 [View Article][PubMed]
    [Google Scholar]
  61. Saloheimo M, Paloheimo M, Hakola S, Pere J, Swanson B et al. Swollenin, a Trichoderma reesei protein with sequence similarity to the plant expansins, exhibits disruption activity on cellulosic materials. Eur J Biochem 2002; 269:4202–4211 [View Article][PubMed]
    [Google Scholar]
  62. Yennawar NH, Li L-C, Dudzinski DM, Tabuchi A, Cosgrove DJ. Crystal structure and activities of EXPB1 (Zea M 1), a beta-expansin and group-1 pollen allergen from maize. Proc Natl Acad Sci U S A 2006; 103:14664–14671 [View Article][PubMed]
    [Google Scholar]
  63. Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 2012; 13:614–629 [View Article][PubMed]
    [Google Scholar]
  64. Cosgrove DJ. Microbial expansins. Annu Rev Microbiol 2017; 71:479–497 [View Article][PubMed]
    [Google Scholar]
  65. Hayward AC. Biology and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annu Rev Phytopathol 1991; 29:65–87 [View Article][PubMed]
    [Google Scholar]
  66. Pérombelon MCM. Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol 2002; 51:1–12 [View Article]
    [Google Scholar]
  67. Toth IK, Bell KS, Holeva MC, Birch PRJ. Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 2003; 4:17–30 [View Article][PubMed]
    [Google Scholar]
  68. Narváez-Barragán DA, de Sandozequi A, Rodríguez M, Estrada K, Tovar-Herrera OE et al. Analysis of two Mexican Pectobacterium brasiliense strains reveals an inverted relationship between c-di-GMP levels with exopolysaccharide production and swarming motility. Microbiol Res 2020; 235:126427 [View Article][PubMed]
    [Google Scholar]
  69. Tancos MA, Chalupowicz L, Barash I, Manulis-Sasson S, Smart CD. Tomato fruit and seed colonization by Clavibacter michiganensis subsp. michiganensis through external and internal routes. Appl Environ Microbiol 2013; 79:6948–6957 [View Article][PubMed]
    [Google Scholar]
  70. Laine MJ, Haapalainen M, Wahlroos T, Kankare K, Nissinen R et al. The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp. sepedonicus plays a role in virulence and contains an expansin-like domain. Physiol Mol Plant Pathol 2000; 57:221–233 [View Article]
    [Google Scholar]
  71. Bais HP, Fall R, Vivanco JM. Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 2004; 134:307–319 [View Article][PubMed]
    [Google Scholar]
  72. Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A et al. The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 2012; 13:804 [View Article]
    [Google Scholar]
  73. Wilson LM, Idnurm A, Howlett BJ. Characterization of a gene (Sp1) encoding a secreted protein from Leptosphaeria maculans, the blackleg pathogen of Brassica napus. Mol Plant Pathol 2002; 3:487–493 [View Article][PubMed]
    [Google Scholar]
  74. Quarantin A, Glasenapp A, Schäfer W, Favaron F, Sella L. Involvement of the Fusarium graminearum cerato-platanin proteins in fungal growth and plant infection. Plant Physiol Biochem 2016; 109:220–229 [View Article][PubMed]
    [Google Scholar]
  75. Djonović S, Pozo MJ, Dangott LJ, Howell CR, Kenerley CM. Sm1, a proteinaceous elicitor secreted by the biocontrol fungus Trichoderma virens induces plant defense responses and systemic resistance. Mol Plant Microbe Interact 2006; 19:838–853 [View Article][PubMed]
    [Google Scholar]
  76. Viterbo A, Chet I. TasHyd1, a new hydrophobin gene from the biocontrol agent Trichoderma asperellum, is involved in plant root colonization. Mol Plant Pathol 2006; 7:249–258 [View Article][PubMed]
    [Google Scholar]
  77. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2004; 2:43–56 [View Article][PubMed]
    [Google Scholar]
  78. Ali S, Magne M, Chen S, Côté O, Stare BG et al. Analysis of putative apoplastic effectors from the nematode, Globodera rostochiensis, and identification of an expansin-like protein that can induce and suppress host defenses. PLoS One 2015; 10:e0115042 [View Article][PubMed]
    [Google Scholar]
  79. Fontana F, Santini A, Salvini M, Pazzagli L, Cappugi G et al. Cerato-Platanin treated plane leaves restrict ceratocystis platani growth and overexpress defence-related genes. J Plant Pathol 2008; 90:295–306
    [Google Scholar]
  80. Frías M, Brito N, González C. The Botrytis cinerea cerato-platanin BcSpl1 is a potent inducer of systemic acquired resistance (SAR) in tobacco and generates a wave of salicylic acid expanding from the site of application; 2013; 14191–196
  81. Vieira P, Nemchinov LG. An Expansin-like candidate effector protein from Pratylenchus penetrans modulates immune responses in Nicotiana benthamiana. Phytopathology 2020; 110:684–693 [View Article][PubMed]
    [Google Scholar]
  82. Bhadauria V, Banniza S, Vandenberg A, Selvaraj G, Wei Y. EST mining identifies proteins putatively secreted by the anthracnose pathogen Colletotrichum truncatum. BMC Genomics 2011; 12:327 [View Article][PubMed]
    [Google Scholar]
  83. Yu H, Duan J, Wang B, Jiang X. The function of snodprot in the cerato-platanin family from Dactylellina cionopaga in nematophagous fungi. Biosci Biotechnol Biochem 2012; 76:1835–1842 [View Article][PubMed]
    [Google Scholar]
  84. Qin L, Kudla U, Roze EHA, Goverse A, Popeijus H et al. A nematode expansin acting on plants. Nature 2004; 427:30 [View Article]
    [Google Scholar]
  85. Long H, Peng D, Huang W, Liu Y, Peng H. Identification of a putative expansin gene expressed in the subventral glands of the cereal cyst nematode Heterodera avenae. Nematology 2012; 14:571–577 [View Article]
    [Google Scholar]
  86. Boddi S, Comparini C, Calamassi R, Pazzagli L, Cappugi G et al. Cerato-Platanin protein is located in the cell walls of ascospores, conidia and hyphae of ceratocystis fimbriata f. sp. platani. FEMS Microbiol Lett 2004; 233:341–346 [View Article][PubMed]
    [Google Scholar]
  87. Gaderer R, Bonazza K, Seidl-Seiboth V. Cerato-platanins: a fungal protein family with intriguing properties and application potential. Appl Microbiol Biotechnol 2014; 98:4795–4803 [View Article][PubMed]
    [Google Scholar]
  88. Veneault-Fourrey C, Commun C, Kohler A, Morin E, Balestrini R et al. Genomic and transcriptomic analysis of Laccaria bicolor CAZome reveals insights into polysaccharides remodelling during symbiosis establishment. Fungal Genet Biol 2014; 72:168–181 [View Article][PubMed]
    [Google Scholar]
  89. Nordberg H, Cantor M, Dusheyko S, Hua S, Poliakov A et al. The genome portal of the Department of energy joint genome Institute: 2014 updates. Nucleic Acids Res 2014; 42:D26–D31 [View Article][PubMed]
    [Google Scholar]
  90. Baccelli I, Comparini C, Bettini PP, Martellini F, Ruocco M et al. The expression of the cerato-platanin gene is related to hyphal growth and chlamydospores formation in Ceratocystis platani. FEMS Microbiol Lett 2012; 327:155–163 [View Article][PubMed]
    [Google Scholar]
  91. Luti S, Sella L, Quarantin A, Pazzagli L, Baccelli I. Twenty years of research on cerato-platanin family proteins: clues, conclusions, and unsolved issues. vol. 34, fungal biology reviews. Elsevier Ltd 202013–24
    [Google Scholar]
  92. Yang J, Zhang Y. Protein structure and function prediction using I‐TASSER. Curr Protoc Bioinforma 2015; 52:5.8.1–5.8.5 [View Article]
    [Google Scholar]
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