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Abstract

Chitin is a structural polymer in many eukaryotes. Many organisms can degrade chitin to defend against chitinous pathogens or use chitin oligomers as food. Beneficial microorganisms like nitrogen-fixing symbiotic rhizobia and mycorrhizal fungi produce chitin-based signal molecules called lipo-chitooligosaccharides (LCOs) and short chitin oligomers to initiate a symbiotic relationship with their compatible hosts and exchange nutrients. A recent study revealed that a broad range of fungi produce LCOs and chitooligosaccharides (COs), suggesting that these signaling molecules are not limited to beneficial microbes. The fungal LCOs also affect fungal growth and development, indicating that the roles of LCOs beyond symbiosis and LCO production may predate mycorrhizal symbiosis. This review describes the diverse structures of chitin; their perception by eukaryotes and prokaryotes; and their roles in symbiotic interactions, defense, and microbe-microbe interactions. We also discuss potential strategies of fungi to synthesize LCOs and their roles in fungi with different lifestyles.

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2021-10-08
2024-04-20
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Literature Cited

  1. 1. 
    Andrés E, Albesa-Jové D, Biarnés X, Moerschbacher BM, Guerin ME, Planas A 2014. Structural basis of chitin oligosaccharide deacetylation. Angew. Chem. Int. Ed. Engl. 53:276882–87
    [Google Scholar]
  2. 2. 
    Ané J-M, Kalil A, Maeda J 2016. Chitin oligomers for use in promoting non-leguminous plant growth and development US Patent 2016/0366883 A1
  3. 3. 
    Ané J-M, Lévy J, Thoquet P, Kulikova O, de Billy F et al. 2002. Genetic and cytogenetic mapping of DMI1, DMI2, and DMI3 genes of Medicago truncatula involved in Nod factor transduction, nodulation, and mycorrhization. Mol. Plant-Microbe Interact. 15:111108–18
    [Google Scholar]
  4. 4. 
    Antolín-Llovera M, Ried MK, Parniske M. 2014. Cleavage of the SYMBIOSIS RECEPTOR-LIKE KINASE ectodomain promotes complex formation with Nod factor receptor 5. Curr. Biol. 24:4422–27
    [Google Scholar]
  5. 5. 
    Arrighi J-F, Barre A, Ben Amor B, Bersoult A, Soriano LC et al. 2006. The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142:1265–79
    [Google Scholar]
  6. 6. 
    Berlemont R. 2017. Distribution and diversity of enzymes for polysaccharide degradation in fungi. Sci. Rep. 7:1222
    [Google Scholar]
  7. 7. 
    Bozsoki Z, Cheng J, Feng F, Gysel K, Vinther M et al. 2017. Receptor-mediated chitin perception in legume roots is functionally separable from Nod factor perception. PNAS 114:38E8118–27
    [Google Scholar]
  8. 8. 
    Bozsoki Z, Gysel K, Hansen SB, Lironi D, Krönauer C et al. 2020. Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity. Science 369:6504663–70
    [Google Scholar]
  9. 9. 
    Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT et al. 2012. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. PNAS 109:3413859–64
    [Google Scholar]
  10. 10. 
    Buendia L, Girardin A, Wang T, Cottret L, Lefebvre B. 2018. LysM receptor-like kinase and LysM receptor-like protein families: an update on phylogeny and functional characterization. Front. Plant Sci. 9:1531
    [Google Scholar]
  11. 11. 
    Bulawa CE. 1993. Genetics and molecular biology of chitin synthesis in fungi. Annu. Rev. Microbiol. 47:505–34
    [Google Scholar]
  12. 12. 
    Cai J, Zhang L-Y, Liu W, Tian Y, Xiong J-S et al. 2018. Role of the Nod factor hydrolase MtNFH1 in regulating Nod factor levels during rhizobial infection and in mature nodules of Medicago truncatula. Plant Cell 30:2397–414
    [Google Scholar]
  13. 13. 
    Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M et al. 2011. Nuclear membranes control symbiotic calcium signaling of legumes. PNAS 108:3414348–53
    [Google Scholar]
  14. 14. 
    Chabaud M, Gherbi H, Pirolles E, Vaissayre V, Fournier J et al. 2016. Chitinase-resistant hydrophilic symbiotic factors secreted by Frankia activate both Ca2+ spiking and NIN gene expression in the actinorhizal plant Casuarina glauca. New Phytol 209:186–93
    [Google Scholar]
  15. 15. 
    Chang Y, Wang S, Sekimoto S, Aerts AL, Choi C et al. 2015. Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biol. Evol. 7:61590–601
    [Google Scholar]
  16. 16. 
    Charpentier M, Sun J, Vaz Martins T, Radhakrishnan GV, Findlay K et al. 2016. Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science 352:62891102–5
    [Google Scholar]
  17. 17. 
    Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G et al. 2018. High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol 220:41161–71
    [Google Scholar]
  18. 18. 
    Conn CE, Nelson DC. 2015. Evidence that KARRIKIN-INSENSITIVE2 (KAI2) receptors may perceive an unknown signal that is not karrikin or strigolactone. Front. Plant Sci. 6:1219
    [Google Scholar]
  19. 19. 
    Cope KR, Bascaules A, Irving TB, Venkateshwaran M, Maeda J et al. 2019. The ectomycorrhizal fungus Laccaria bicolor produces lipochitooligosaccharides and uses the common symbiosis pathway to colonize Populus roots. Plant Cell 31:102386–410
    [Google Scholar]
  20. 20. 
    Cord-Landwehr S, Melcher RLJ, Kolkenbrock S, Moerschbacher BM. 2016. A chitin deacetylase from the endophytic fungus Pestalotiopsis sp. efficiently inactivates the elicitor activity of chitin oligomers in rice cells. Sci. Rep. 6:38018
    [Google Scholar]
  21. 21. 
    Deakin WJ, Broughton WJ. 2009. Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:4312–20
    [Google Scholar]
  22. 22. 
    Delaux P-M, Radhakrishnan GV, Jayaraman D, Cheema J, Malbreil M et al. 2015. Algal ancestor of land plants was preadapted for symbiosis. PNAS 112:4313390–95
    [Google Scholar]
  23. 23. 
    Delaux P-M, Varala K, Edger PP, Coruzzi GM, Pires JC, Ané J-M. 2014. Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLOS Genet 10:7e1004487
    [Google Scholar]
  24. 24. 
    Dénarié J, Debellé F, Promé JC. 1996. Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65:503–35
    [Google Scholar]
  25. 25. 
    Dénarié J, Debellé F, Rosenberg C. 1992. Signaling and host range variation in nodulation. Annu. Rev. Microbiol. 46:497–531
    [Google Scholar]
  26. 26. 
    Desaki Y, Kohari M, Shibuya N, Kaku H. 2019. MAMP-triggered plant immunity mediated by the LysM-receptor kinase CERK1. J. Gen. Plant Pathol. 85:11–11
    [Google Scholar]
  27. 27. 
    Doares SH, Syrovets T, Weiler EW, Ryan CA 1995. Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. PNAS 92:104095–98
    [Google Scholar]
  28. 28. 
    Eide KB, Lindbom AR, Eijsink VGH, Norberg AL, Sørlie M. 2013. Analysis of productive binding modes in the human chitotriosidase. FEBS Lett 587:213508–13
    [Google Scholar]
  29. 29. 
    El-Sayed E-SA, El-Didamony G, El-Sayed EF. 2002. Effects of mycorrhizae and chitin-hydrolysing microbes on Vicia faba. World J. Microbiol. Biotechnol. 18:6505–15
    [Google Scholar]
  30. 30. 
    Esseling JJ, Lhuissier FGP, Emons AMC. 2004. A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16:4933–44
    [Google Scholar]
  31. 31. 
    Feng F, Sun J, Radhakrishnan GV, Lee T, Bozsóki Z et al. 2019. A combination of chitooligosaccharide and lipochitooligosaccharide recognition promotes arbuscular mycorrhizal associations in Medicago truncatula. Nat. Commun. 10:15047
    [Google Scholar]
  32. 32. 
    Fliegmann J, Jauneau A, Pichereaux C, Rosenberg C, Gasciolli V et al. 2016. LYR 3, a high-affinity LCO-binding protein of Medicago truncatula, interacts with LYK3, a key symbiotic receptor. FEBS Lett 590:101477–87
    [Google Scholar]
  33. 33. 
    Frey-Klett P, Garbaye J, Tarkka M. 2007. The mycorrhiza helper bacteria revisited. New Phytol 176:122–36
    [Google Scholar]
  34. 34. 
    Fujishige NA, Lum MR, De Hoff PL, Whitelegge JP, Faull KF, Hirsch AM. 2008. Rhizobium common nod genes are required for biofilm formation. Mol. Microbiol. 67:3504–15
    [Google Scholar]
  35. 35. 
    Garcia K, Delaux P-M, Cope KR, Ané J-M. 2015. Molecular signals required for the establishment and maintenance of ectomycorrhizal symbioses. New Phytol 208:179–87
    [Google Scholar]
  36. 36. 
    Garcia M, Dunlap J, Loh J, Stacey G. 1996. Phenotypic characterization and regulation of the nolA gene of Bradyrhizobium japonicum. Mol. Plant-Microbe Interact. 9:7625–36
    [Google Scholar]
  37. 37. 
    Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M et al. 2013. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol 198:1190–202
    [Google Scholar]
  38. 38. 
    Genre A, Ortu G, Bertoldo C, Martino E, Bonfante P 2009. Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiol 149:31424–34
    [Google Scholar]
  39. 39. 
    Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D et al. 2008. SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. PNAS 105:124928–32
    [Google Scholar]
  40. 40. 
    Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E et al. 2007. Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316:58291307–12
    [Google Scholar]
  41. 41. 
    Glaser L, Brown DH. 1957. The synthesis of chitin in cell-free extracts of Neurospora crassa. J. Biol. Chem. 228:2729–42
    [Google Scholar]
  42. 42. 
    Gonçalves IR, Brouillet S, Soulié M-C, Gribaldo S, Sirven C et al. 2016. Genome-wide analyses of chitin synthases identify horizontal gene transfers towards bacteria and allow a robust and unifying classification into fungi. BMC Evol. Biol. 16:1252
    [Google Scholar]
  43. 43. 
    Gong B-Q, Wang F-Z, Li J-F. 2020. Hide-and-seek: chitin-triggered plant immunity and fungal counterstrategies. Trends Plant Sci 25:8805–16
    [Google Scholar]
  44. 44. 
    Gow NAR, Gooday GW. 1983. Ultrastructure of chitin in hyphae of Candida albicans and other dimorphic and mycelial fungi. Protoplasma 115:52–58
    [Google Scholar]
  45. 45. 
    Gow NAR, Latge J-P, Munro CA. 2017. The fungal cell wall: structure, biosynthesis, and function. Microbiol. Spectr. 5:3 https://doi.org/10.1128/microbiolspec.FUNK-0035-2016
    [Crossref] [Google Scholar]
  46. 46. 
    Grifoll-Romero L, Pascual S, Aragunde H, Biarnés X, Planas A. 2018. Chitin deacetylases: structures, specificities, and biotech applications. Polymers 10:4352
    [Google Scholar]
  47. 47. 
    Gueddou A, Swanson E, Hezbri K, Nouioui I, Ktari A et al. 2019. Draft genome sequence of the symbiotic Frankia sp. strain BMG5.30 isolated from root nodules of Coriaria myrtifolia in Tunisia. Antonie Van Leeuwenhoek 112:167–74
    [Google Scholar]
  48. 48. 
    Gutjahr C, Banba M, Croset V, An K, Miyao A et al. 2008. Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:112989–3005
    [Google Scholar]
  49. 49. 
    Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston MG et al. 2015. Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350:62671521–24
    [Google Scholar]
  50. 50. 
    Hayafune M, Berisio R, Marchetti R, Silipo A, Kayama M et al. 2014. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. PNAS 111:3E404–13
    [Google Scholar]
  51. 51. 
    Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293:55321129–33
    [Google Scholar]
  52. 52. 
    Heggset EB, Hoell IA, Kristoffersen M, Eijsink VGH, Vårum KM. 2009. Degradation of chitosans with chitinase G from Streptomyces coelicolor A3(2): production of chito-oligosaccharides and insight into subsite specificities. Biomacromolecules 10:4892–99
    [Google Scholar]
  53. 53. 
    Hirano T, Shiraishi H, Ikejima M, Uehara R, Hakamata W, Nishio T. 2017. Chitin oligosaccharide deacetylase from Shewanella baltica ATCC BAA-1091. Biosci. Biotechnol. Biochem. 81:3547–50
    [Google Scholar]
  54. 54. 
    Hirsch S, Kim J, Muñoz A, Heckmann AB, Allan Downie J, Oldroyd GED 2009. GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:2545–57
    [Google Scholar]
  55. 55. 
    Hjort K, Presti I, Elväng A, Marinelli F, Sjöling S. 2014. Bacterial chitinase with phytopathogen control capacity from suppressive soil revealed by functional metagenomics. Appl. Microbiol. Biotechnol. 98:62819–28
    [Google Scholar]
  56. 56. 
    Horn SJ, Sørbotten A, Synstad B, Sikorski P, Sørlie M et al. 2006. Endo/exo mechanism and processivity of family 18 chitinases produced by Serratia marcescens. FEBS J 273:3491–503
    [Google Scholar]
  57. 57. 
    Ichinomiya M, Yamada E, Yamashita S, Ohta A, Horiuchi H. 2005. Class I and class II chitin synthases are involved in septum formation in the filamentous fungus Aspergillus nidulans. Eukaryot. Cell 4:61125–36
    [Google Scholar]
  58. 58. 
    Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H et al. 2005. Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:7025527–31
    [Google Scholar]
  59. 59. 
    Itoh T, Kimoto H. 2019. Bacterial chitinase system as a model of chitin biodegradation. Adv. Exp. Med. Biol. 1142:131–51
    [Google Scholar]
  60. 60. 
    James TY, Porter D, Leander CA, Vilgalys R, Longcore JE. 2000. Molecular phylogenetics of the Chytridiomycota supports the utility of ultrastructural data in chytrid systematics. Can. J. Bot. 78:3336–50
    [Google Scholar]
  61. 61. 
    Jiménez-Ortigosa C, Aimanianda V, Muszkieta L, Mouyna I, Alsteens D et al. 2012. Chitin synthases with a myosin motor-like domain control the resistance of Aspergillus fumigatus to echinocandins. Antimicrob. Agents Chemother. 56:126121–31
    [Google Scholar]
  62. 62. 
    John M, Röhrig H, Schmidt J, Wieneke U, Schell J. 1993. Rhizobium NodB protein involved in nodulation signal synthesis is a chitooligosaccharide deacetylase. PNAS 90:2625–29
    [Google Scholar]
  63. 63. 
    Kasprzewska A. 2003. Plant chitinases—regulation and function. Cell. Mol. Biol. Lett. 8:3809–24
    [Google Scholar]
  64. 64. 
    Kawase T, Yokokawa S, Saito A, Fujii T, Nikaidou N et al. 2006. Comparison of enzymatic and antifungal properties between family 18 and 19 chitinases from S. coelicolor A3(2). Biosci. Biotechnol. Biochem. 70:4988–98
    [Google Scholar]
  65. 65. 
    Kendra DF, Hadwiger LA. 1984. Characterization of the smallest chitosan oligomer that is maximally antifungal to Fusarium solani and elicits pisatin formation in Pisum sativum. Exp. Mycol. 8:3276–81
    [Google Scholar]
  66. 66. 
    Kevei Z, Lougnon G, Mergaert P, Horváth GV, Kereszt A et al. 2007. 3-Hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19:123974–89
    [Google Scholar]
  67. 67. 
    Khan W, Costa C, Souleimanov A, Prithiviraj B, Smith DL. 2011. Response of Arabidopsis thaliana roots to lipo-chitooligosaccharide from Bradyrhizobium japonicum and other chitin-like compounds. Plant Growth Regul 63:3243–49
    [Google Scholar]
  68. 68. 
    Kim HJ, Choi HS, Yang SY, Kim IS, Yamaguchi T et al. 2014. Both extracellular chitinase and a new cyclic lipopeptide, chromobactomycin, contribute to the biocontrol activity of Chromobacterium sp. C61. Mol. Plant Pathol. 15:2122–32
    [Google Scholar]
  69. 69. 
    Kim J-E, Lee H-J, Lee J, Kim KW, Yun S-H et al. 2009. Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity. Curr. Genet 55:4449–59
    [Google Scholar]
  70. 70. 
    Kim S, Zeng W, Bernard S, Liao J, Venkateshwaran M et al. 2019. Ca2+-regulated Ca2+ channels with an RCK gating ring control plant symbiotic associations. Nat. Commun. 10:13703
    [Google Scholar]
  71. 71. 
    Knack JJ, Wilcox LW, Delaux P-M, Ané J-M, Piotrowski MJ et al. 2015. Microbiomes of streptophyte algae and bryophytes suggest that a functional suite of microbiota fostered plant colonization of land. Int. J. Plant Sci. 176:5405–20
    [Google Scholar]
  72. 72. 
    Knight CD, Rossen L, Robertson JG, Wells B, Downie JA. 1986. Nodulation inhibition by Rhizobium leguminosarum multicopy nodABC genes and analysis of early stages of plant infection. J. Bacteriol. 166:2552–58
    [Google Scholar]
  73. 73. 
    Kuroki M, Okauchi K, Yoshida S, Ohno Y, Murata S et al. 2017. Chitin-deacetylase activity induces appressorium differentiation in the rice blast fungus Magnaporthe oryzae. Sci. Rep. 7:19697
    [Google Scholar]
  74. 74. 
    Langner T, Göhre V. 2016. Fungal chitinases: function, regulation, and potential roles in plant/pathogen interactions. Curr. Genet. 62:2243–54
    [Google Scholar]
  75. 75. 
    Lasudee K, Tokuyama S, Lumyong S, Pathom-Aree W. 2018. Actinobacteria associated with arbuscular mycorrhizal Funneliformis mosseae spores, taxonomic characterization and their beneficial traits to plants: evidence obtained from mung bean (Vigna radiata) and Thai jasmine rice (Oryza sativa). Front. Microbiol 9:1247
    [Google Scholar]
  76. 76. 
    Leake JR, Read DJ. 1990. Chitin as a nitrogen source for mycorrhizal fungi. Mycol. Res. 94:7993–95
    [Google Scholar]
  77. 77. 
    Lee CG, Da Silva CA, Lee J-Y, Hartl D, Elias JA 2008. Chitin regulation of immune responses: an old molecule with new roles. Curr. Opin. Immunol. 20:6684–89
    [Google Scholar]
  78. 78. 
    Lerouge P, Roche P, Faucher C, Maillet F, Truchet G et al. 1990. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344:6268781–84
    [Google Scholar]
  79. 79. 
    Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O et al. 2004. A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:56621361–64
    [Google Scholar]
  80. 80. 
    Liang Y, Cao Y, Tanaka K, Thibivilliers S, Wan J et al. 2013. Non-legumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341:61521384–87
    [Google Scholar]
  81. 81. 
    Li H-L, Wang W, Mortimer PE, Li R-Q, Li D-Z et al. 2015. Large-scale phylogenetic analyses reveal multiple gains of actinorhizal nitrogen-fixing symbioses in angiosperms associated with climate change. Sci. Rep. 5:14023
    [Google Scholar]
  82. 82. 
    Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R. 2003. LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:5645630–33
    [Google Scholar]
  83. 83. 
    Liu K, Ding H, Yu Y, Chen B 2019. A cold-adapted chitinase-producing bacterium from Antarctica and its potential in biocontrol of plant pathogenic fungi. Mar. Drugs 17:12695
    [Google Scholar]
  84. 84. 
    Liu Z, Gay LM, Tuveng TR, Agger JW, Westereng B et al. 2017. Structure and function of a broad-specificity chitin deacetylase from Aspergillus nidulans FGSC A4. Sci. Rep. 7:11746
    [Google Scholar]
  85. 85. 
    Li X, Roseman S. 2004. The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase. PNAS 101:2627–31
    [Google Scholar]
  86. 86. 
    Li X, Wang L-X, Wang X, Roseman S 2007. The chitin catabolic cascade in the marine bacterium Vibrio cholerae: characterization of a unique chitin oligosaccharide deacetylase. Glycobiology 17:121377–87
    [Google Scholar]
  87. 87. 
    Loh J, Stacey G. 2003. Nodulation gene regulation in Bradyrhizobium japonicum: a unique integration of global regulatory circuits. Appl. Environ. Microbiol. 69:110–17
    [Google Scholar]
  88. 88. 
    Loh JT, Stacey G. 2001. Feedback regulation of the Bradyrhizobium japonicum nodulation genes. Mol. Microbiol. 41:61357–64
    [Google Scholar]
  89. 89. 
    Long SR. 2001. Genes and signals in the rhizobium-legume symbiosis. Plant Physiol 125:169–72
    [Google Scholar]
  90. 90. 
    Loron CC, François C, Rainbird RH, Turner EC, Borensztajn S, Javaux EJ. 2019. Early fungi from the Proterozoic era in Arctic Canada. Nature 570:7760232–35
    [Google Scholar]
  91. 91. 
    Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB et al. 2010. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun. 1:110
    [Google Scholar]
  92. 92. 
    Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A et al. 2011. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:732858–63
    [Google Scholar]
  93. 93. 
    Malolepszy A, Kelly S, Sørensen KK, James EK, Kalisch C et al. 2018. A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis. eLife 7:e38874
    [Google Scholar]
  94. 94. 
    Mbengue M, Camut S, de Carvalho-Niebel F, Deslandes L, Froidure S et al. 2010. The Medicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22:103474–88
    [Google Scholar]
  95. 95. 
    Merzendorfer H. 2011. The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur. J. Cell Biol. 90:9759–69
    [Google Scholar]
  96. 96. 
    Messinese E, Mun J-H, Yeun LH, Jayaraman D, Rougé P et al. 2007. A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol. Plant-Microbe Interact. 20:8912–21
    [Google Scholar]
  97. 97. 
    Miller JB, Pratap A, Miyahara A, Zhou L, Bornemann S et al. 2013. Calcium/calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling. Plant Cell 25:125053–66
    [Google Scholar]
  98. 98. 
    Mornico D, Miché L, Béna G, Nouwen N, Verméglio A et al. 2011. Comparative genomics of aeschynomene symbionts: insights into the ecological lifestyle of nod-independent photosynthetic bradyrhizobia. Genes 3:135–61
    [Google Scholar]
  99. 99. 
    Mouyna I, Dellière S, Beauvais A, Gravelat F, Snarr B et al. 2020. What are the functions of chitin deacetylases in Aspergillus fumigatus?. Front. Cell. Infect. Microbiol. 10:28
    [Google Scholar]
  100. 100. 
    Mukherjee A, Ané J-M. 2011. Germinating spore exudates from arbuscular mycorrhizal fungi: molecular and developmental responses in plants and their regulation by ethylene. Mol. Plant-Microbe Interact. 24:2260–70
    [Google Scholar]
  101. 101. 
    Murakami E, Cheng J, Gysel K, Bozsoki Z, Kawaharada Y et al. 2018. Epidermal LysM receptor ensures robust symbiotic signalling in Lotus japonicus. eLife 7:e33506
    [Google Scholar]
  102. 102. 
    Muszkieta L, Aimanianda V, Mellado E, Gribaldo S, Alcàzar-Fuoli L et al. 2014. Deciphering the role of the chitin synthase families 1 and 2 in the in vivo and in vitro growth of Aspergillus fumigatus by multiple gene targeting deletion. Cell. Microbiol. 16:121784–805
    [Google Scholar]
  103. 103. 
    Nagahashi S, Sudoh M, Ono N, Sawada R, Yamaguchi E et al. 1995. Characterization of chitin synthase 2 of Saccharomyces cerevisiae: implication of two highly conserved domains as possible catalytic sites. J. Biol. Chem. 270:2313961–67
    [Google Scholar]
  104. 104. 
    Nguyen TV, Wibberg D, Battenberg K, Blom J, Vanden Heuvel B et al. 2016. An assemblage of Frankia Cluster II strains from California contains the canonical nod genes and also the sulfotransferase gene nodH. BMC Genom 17:1796
    [Google Scholar]
  105. 105. 
    Nguyen TV, Wibberg D, Vigil-Stenman T, Berckx F, Battenberg K et al. 2019. Frankia-enriched metagenomes from the earliest diverging symbiotic Frankia cluster: They come in teams. Genome Biol. Evol. 11:82273–91
    [Google Scholar]
  106. 106. 
    Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS et al. 2005. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:70711151–56
    [Google Scholar]
  107. 107. 
    Nishizawa Y, Kawakami A, Hibi T, He DY, Shibuya N, Minami E. 1999. Regulation of the chitinase gene expression in suspension-cultured rice cells by N-acetylchitooligosaccharides: differences in the signal transduction pathways leading to the activation of elicitor-responsive genes. Plant Mol. Biol. 39:5907–14
    [Google Scholar]
  108. 108. 
    Niu M, Steffan BN, Fischer GJ, Venkatesh N, Raffa NL et al. 2020. Fungal oxylipins direct programmed developmental switches in filamentous fungi. Nat. Commun. 11:15158
    [Google Scholar]
  109. 109. 
    Ohno M, Kimura M, Miyazaki H, Okawa K, Onuki R et al. 2016. Acidic mammalian chitinase is a proteases-resistant glycosidase in mouse digestive system. Sci. Rep. 6:37756
    [Google Scholar]
  110. 110. 
    Ohno N 2007. Yeast and fungal polysaccharides. Comprehensive Glycoscience, Vol. 2: Analysis of Glycans H Kamerling, JJ Barchi Jr., G-J Boons, YC Lee, A Suzuki , et. al., pp. 559–77 Oxford, UK: Elsevier
    [Google Scholar]
  111. 111. 
    Okazaki S, Kaneko T, Sato S, Saeki K 2013. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. PNAS 110:4217131–36
    [Google Scholar]
  112. 112. 
    Okazaki S, Tittabutr P, Teulet A, Thouin J, Fardoux J et al. 2016. Rhizobium-legume symbiosis in the absence of Nod factors: two possible scenarios with or without the T3SS. ISME J 10:164–74
    [Google Scholar]
  113. 113. 
    Orlean P, Funai D. 2019. Priming and elongation of chitin chains: implications for chitin synthase mechanism. The Cell Surface 5:100017
    [Google Scholar]
  114. 114. 
    Ovtsyna AO, Rademaker GJ, Esser E, Weinman J, Rolfe BG et al. 1999. Comparison of characteristics of the nodX genes from various Rhizobium leguminosarum strains. Mol. Plant-Microbe Interact. 12:3252–58
    [Google Scholar]
  115. 115. 
    Parniske M. 2018. Uptake of bacteria into living plant cells, the unifying and distinct feature of the nitrogen-fixing root nodule symbiosis. Curr. Opin. Plant Biol. 44:164–74
    [Google Scholar]
  116. 116. 
    Paschinger K, Wilson IBH. 2019. Comparisons of N-glycans across invertebrate phyla. Parasitology 146:141733–42
    [Google Scholar]
  117. 117. 
    Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riely BK et al. 2007. The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145:1192–203
    [Google Scholar]
  118. 118. 
    Persson T, Benson DR, Normand P, Vanden Heuvel B, Pujic P et al. 2011. Genome sequence of “Candidatus Frankia datiscae” Dg1, the uncultured microsymbiont from nitrogen-fixing root nodules of the dicot Datisca glomerata. J. Bacteriol. 193:247017–18
    [Google Scholar]
  119. 119. 
    Peters NK, Frost JW, Long SR. 1986. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:4767977–80
    [Google Scholar]
  120. 120. 
    Pimprikar P, Carbonnel S, Paries M, Katzer K, Klingl V et al. 2016. A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr. Biol. 26:8987–98 Erratum. 2016. Curr. Biol. 26(8):1126
    [Google Scholar]
  121. 121. 
    Poinsot V, Crook MB, Erdn S, Maillet F, Bascaules A, Ané J-M. 2016. New insights into Nod factor biosynthesis: analyses of chitooligomers and lipo-chitooligomers of Rhizobium sp. IRBG74 mutants. Carbohydr. Res. 434:83–93
    [Google Scholar]
  122. 122. 
    Prithiviraj B, Zhou X, Souleimanov A, Khan WM, Smith DL. 2003. A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants. Planta 216:3437–45
    [Google Scholar]
  123. 123. 
    Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y et al. 2003. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:6958585–92
    [Google Scholar]
  124. 124. 
    Redecker D, Kodner R, Graham LE. 2000. Glomalean fungi from the Ordovician. Science 289:54861920–21
    [Google Scholar]
  125. 125. 
    Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG 1986. Flavones induce expression of nodulation genes in Rhizobium. Nature 323:6089632–35
    [Google Scholar]
  126. 126. 
    Remy W, Taylor TN, Hass H, Kerp H. 1994. Four hundred-million-year-old vesicular arbuscular mycorrhizae. PNAS 91:2511841–43
    [Google Scholar]
  127. 127. 
    Rey T, André O, Nars A, Dumas B, Gough C et al. 2019. Lipo-chitooligosaccharide signalling blocks a rapid pathogen-induced ROS burst without impeding immunity. New Phytol 221:2743–49
    [Google Scholar]
  128. 128. 
    Ried MK, Antolín-Llovera M, Parniske M 2014. Spontaneous symbiotic reprogramming of plant roots triggered by receptor-like kinases. eLife 3:e03891
    [Google Scholar]
  129. 129. 
    Rinaudi LV, Giordano W 2010. An integrated view of biofilm formation in rhizobia. FEMS Microbiol. Lett. 304:11–11
    [Google Scholar]
  130. 130. 
    Roche P, Debellé F, Maillet F, Lerouge P, Faucher C et al. 1991. Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67:61131–43
    [Google Scholar]
  131. 131. 
    Roche P, Lerouge P, Ponthus C, Promé JC. 1991. Structural determination of bacterial nodulation factors involved in the Rhizobium meliloti-alfalfa symbiosis. J. Biol. Chem. 266:1710933–40
    [Google Scholar]
  132. 132. 
    Roche P, Maillet F, Plazanet C, Debellé F, Ferro M et al. 1996. The common nodABC genes of Rhizobium meliloti are host-range determinants. PNAS 93:2615305–10
    [Google Scholar]
  133. 133. 
    Rush TA, Puech-Pagès V, Bascaules A, Jargeat P, Maillet F et al. 2020. Lipo-chitooligosaccharides as regulatory signals of fungal growth and development. Nat. Commun. 11:13897
    [Google Scholar]
  134. 134. 
    Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher RA et al. 2000. Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Mol. Plant-Microbe Interact. 13:7763–77
    [Google Scholar]
  135. 135. 
    Savouré A, Magyar Z, Pierre M, Brown S, Schultze M et al. 1994. Activation of the cell cycle machinery and the isoflavonoid biosynthesis pathway by active Rhizobium meliloti Nod signal molecules in Medicago microcallus suspensions. EMBO J 13:51093–102
    [Google Scholar]
  136. 136. 
    Schultze M, Staehelin C, Brunner F, Genetet I, Legrand M et al. 1998. Plant chitinase/lysozyme isoforms show distinct substrate specificity and cleavage site preference towards lipochitooligosaccharide Nod signals. Plant J 16:5571–80
    [Google Scholar]
  137. 137. 
    Seidl V. 2008. Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biol. Rev. 22:136–42
    [Google Scholar]
  138. 138. 
    Shaw SL, Long SR. 2003. Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol 132:42196–204
    [Google Scholar]
  139. 139. 
    Singh S, Katzer K, Lambert J, Cerri M, Parniske M. 2014. CYCLOPS, a DNA-binding transcriptional activator, orchestrates symbiotic root nodule development. Cell Host Microbe 15:2139–52
    [Google Scholar]
  140. 140. 
    Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E et al. 2007. Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145:1183–91
    [Google Scholar]
  141. 141. 
    Sørbotten A, Horn SJ, Eijsink VGH, Vårum KM. 2005. Degradation of chitosans with chitinase B from Serratia marcescens: production of chito-oligosaccharides and insight into enzyme processivity. FEBS J 272:2538–49
    [Google Scholar]
  142. 142. 
    Souleimanov A, Prithiviraj B, Smith DL. 2002. The major Nod factor of Bradyrhizobium japonicum promotes early growth of soybean and corn. J. Exp. Bot. 53:3761929–34
    [Google Scholar]
  143. 143. 
    Stacey G, Shibuya N. 1997. Chitin recognition in rice and legumes. Plant Soil 194:1–2161–69
    [Google Scholar]
  144. 144. 
    Strullu-Derrien C, Selosse M-A, Kenrick P, Martin FM. 2018. The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytol 220:41012–30
    [Google Scholar]
  145. 145. 
    Subramanian S, Souleimanov A, Smith DL. 2016. Proteomic studies on the effects of lipo-chitooligosaccharide and Thuricin 17 under unstressed and salt stressed conditions in Arabidopsis thaliana. Front. Plant Sci. 7:1314
    [Google Scholar]
  146. 146. 
    Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E et al. 2015. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27:823–38
    [Google Scholar]
  147. 147. 
    Svistoonoff S, Benabdoun FM, Nambiar-Veetil M, Imanishi L, Vaissayre V et al. 2013. The independent acquisition of plant root nitrogen-fixing symbiosis in Fabids recruited the same genetic pathway for nodule organogenesis. PLOS ONE 8:5e64515
    [Google Scholar]
  148. 148. 
    Swanson JA, Mulligan JT, Long SR. 1993. Regulation of syrM and nodD3 in Rhizobium meliloti. Genetics 134:2435–44
    [Google Scholar]
  149. 149. 
    Tabata E, Kashimura A, Kikuchi A, Masuda H, Miyahara R et al. 2018. Chitin digestibility is dependent on feeding behaviors, which determine acidic chitinase mRNA levels in mammalian and poultry stomachs. Sci. Rep. 8:11461
    [Google Scholar]
  150. 150. 
    Tanaka K, Cho S-H, Lee H, Pham AQ, Batek JM et al. 2015. Effect of lipo-chitooligosaccharide on early growth of C4 grass seedlings. J. Exp. Bot. 66:195727–38
    [Google Scholar]
  151. 151. 
    Tedersoo L, Sánchez-Ramírez S, Kõljalg U, Bahram M, Döring M et al. 2018. High-level classification of the fungi and a tool for evolutionary ecological analyses. Fungal Divers 90:1135–59
    [Google Scholar]
  152. 152. 
    Tirichine L, Imaizumi-Anraku H, Yoshida S, Murakami Y, Madsen LH et al. 2006. Deregulation of a Ca2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441:70971153–56
    [Google Scholar]
  153. 153. 
    Tuveng TR, Rothweiler U, Udatha G, Vaaje-Kolstad G, Smalås A, Eijsink VGH. 2017. Structure and function of a CE4 deacetylase isolated from a marine environment. PLOS ONE 12:11e0187544
    [Google Scholar]
  154. 154. 
    Uchiyama T, Kaneko R, Yamaguchi J, Inoue A, Yanagida T et al. 2003. Uptake of N,N′-diacetylchitobiose [(GlcNAc)2] via the phosphotransferase system is essential for chitinase production by Serratia marcescens 2170. J. Bacteriol. 185:61776–82
    [Google Scholar]
  155. 155. 
    van Brussel AA, Bakhuizen R, van Spronsen PC, Spaink HP, Tak T et al. 1992. Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium. Science 257:506670–72
    [Google Scholar]
  156. 156. 
    van Velzen R, Doyle JJ, Geurts R. 2019. A resurrected scenario: Single gain and massive loss of nitrogen-fixing nodulation. Trends Plant Sci 24:149–57
    [Google Scholar]
  157. 157. 
    Veliz EA, Martínez-Hidalgo P, Hirsch AM. 2017. Chitinase-producing bacteria and their role in biocontrol. AIMS Microbiol 3:3689–705
    [Google Scholar]
  158. 158. 
    Venkateshwaran M, Cosme A, Han L, Banba M, Satyshur KA et al. 2012. The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24:62528–45
    [Google Scholar]
  159. 159. 
    Volk H, Marton K, Flajšman M, Radišek S, Tian H et al. 2019. Chitin-binding protein of Verticillium nonalfalfae disguises fungus from plant chitinases and suppresses chitin-triggered host immunity. Mol. Plant-Microbe Interact. 32:101378–90
    [Google Scholar]
  160. 160. 
    Wan J, Zhang X-C, Neece D, Ramonell KM, Clough S et al. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:2471–81
    [Google Scholar]
  161. 161. 
    Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF et al. 2009. Rosid radiation and the rapid rise of angiosperm-dominated forests. PNAS 106:103853–58
    [Google Scholar]
  162. 162. 
    Wang J, Wang L, Yu H, Zain-Ul-Abdin Chen Y et al. 2016. Recent progress on synthesis, property and application of modified chitosan: An overview. Int. J. Biol. Macromol. 88:333–44
    [Google Scholar]
  163. 163. 
    Xia G, Jin C, Zhou J, Yang S, Zhang S, Jin C 2001. A novel chitinase having a unique mode of action from Aspergillus fumigatus YJ-407. Eur. J. Biochem. 268:144079–85
    [Google Scholar]
  164. 164. 
    Yabe T, Yamada-Okabe T, Nakajima T, Sudoh M, Arisawa M, Yamada-Okabe H. 1998. Mutational analysis of chitin synthase 2 of Saccharomyces cerevisiae. Identification of additional amino acid residues involved in its catalytic activity. Eur. J. Biochem. 258:3941–47
    [Google Scholar]
  165. 165. 
    Yang J, Zhang K-Q 2019. Chitin synthesis and degradation in fungi: biology and enzymes. Targeting Chitin-Containing Organisms Q Yang, T Fukamizo 153–67 Singapore: Springer Singapore
    [Google Scholar]
  166. 166. 
    Zeng T, Rodriguez-Moreno L, Mansurkhodzaev A, Wang P, van den Berg W et al. 2020. A lysin motif effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. New Phytol 225:1448–60
    [Google Scholar]
  167. 167. 
    Zhao C, Fraczek MG, Dineen L, Lebedinec R, Macheleidt J et al. 2019. High-throughput gene replacement in Aspergillus fumigatus. Curr. Protoc. Microbiol. 54:1e88
    [Google Scholar]
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