Chitinases are essential for cell separation in Ustilago maydis

Eukaryotic Cell

Volumn 14, Issue 9, 2015, Pages 846-857

  Langner, Thorsten ^a   Öztürk, Merve ^a   Hartmann, Sarah ^a   Cord Landwehr, Stefan ^a,b   Moerschbacher, Bruno ^b   Walton, Jonathan D ^c   Göhrea, Vera ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITINASE; FUNGAL PROTEIN;

AMINO ACID SEQUENCE; CELL DIVISION; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; USTILAGO;

AMINO ACID SEQUENCE; CELL DIVISION; CHITINASES; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; USTILAGO;

EID: 84940642168     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00022-15     Document Type: Article

References (74)

1. Bowman SM, Free SJ. 2006. The structure and synthesis of the fungal cell wall. Bioessays 28:799-808. http://dx.doi.org/10.1002/bies.20441.
2. Klis FM, Boorsma A, De Groot PWJ. 2006. Cell wall construction in Saccharomyces cerevisiae. Yeast 23:185-202. http://dx.doi.org/10.1002/yea.1349.
3. Seidl V. 2008. Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biol Rev 22:36-42. http://dx.doi.org/10.1016/j.fbr.2008.03.002.
4. Karlsson M, Stenlid J. 2008. Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evol Bioinformatics 4:47-60.
5. Aam BB, Heggset EB, Norberg AL, Sorlie M, Varum KM, Eijsink VGH. 2010. Production of chitooligosaccharides and their potential applications in medicine. Mar Drugs 8:1482-1517. http://dx.doi.org/10.3390/md8051482.
6. Hermosa R, Viterbo A, Chet I, Monte E. 2012. Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17-25. http://dx.doi.org/10.1099/mic.0.052274-0.
7. Neeraja C, Anil K, Purushotham P, Suma K, Sarma P, Moerschbacher BM, Podile AR. 2010. Biotechnological approaches to develop bacterial chitinases as a bioshield against fungal diseases of plants. Crit Rev Biotechnol 30:231-241. http://dx.doi.org/10.3109/07388551.2010.487258.
8. Alcazar-Fuoli L, Clavaud C, Lamarre C, Aimanianda V, Seidl-Seiboth V, Mellado E, Latge JP. 2011. Functional analysis of the fungal/plant class chitinase family in Aspergillus fumigatus. Fungal Genet Biol 48:418-429. http://dx.doi.org/10.1016/j.fgb.2010.12.007.
9. Dünkler A, Jorde S, Wendland J. 2008. An Ashbya gossypii cts2 mutant deficient in a sporulation-specific chitinase can be complemented by Candida albicans CHT4. Microbiol Res 163:701-710. http://dx.doi.org/10.1016/j.micres.2008.08.005.
10. Dünkler A, Walther A, Specht CA, Wendland J. 2005. Candida albicans CHT3 encodes the functional homolog of the Cts1 chitinase of Saccharomyces cerevisiae. Fungal Genet Biol 42:935-947. http://dx.doi.org/10.1016/j.fgb.2005.08.001.
11. Kuranda MJ, Robbins PW. 1991. Chitinase is required for cell-separation during growth of Saccharomyces cerevisiae. J Biol Chem 266:19758-19767.
12. Hartl L, Zach S, Seidl-Seiboth V. 2012. Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93:533-543. http://dx.doi.org/10.1007/s00253-011-3723-3.
13. Vollmeister E, Schipper K, Baumann S, Haag C, Pohlmann T, Stock J, Feldbrügge M. 2012. Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev 36:59-77. http://dx.doi.org/10.1111/j.1574-6976.2011.00296.x.
14. Freitag J, Lanver D, Bohmer C, Schink KO, Bolker M, Sandrock B. 2011. Septation of infectious hyphae is critical for appressoria formation and virulence in the smut fungus Ustilago maydis. PLoS Pathog 7:e1002044. http://dx.doi.org/10.1371/journal.ppat.1002044.
15. Steinberg G, Schliwa M, Lehmler C, Bolker M, Kahmann R, McIntosh JR. 1998. Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J Cell Sci 111: 2235-2246.
16. Weber I, Assmann D, Thines E, Steinberg G. 2006. Polar localizing class V myosin chitin synthases are essential during early plant infection in the plant pathogenic fungus Ustilago maydis. Plant Cell 18:225-242. http://dx.doi.org/10.1105/tpc.105.037341.
17. Baumann S, Pohlmann T, Jungbluth M, Brachmann A, Feldbrugge M. 2012. Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J Cell Sci 125:2740-2752. http://dx.doi.org/10.1242/jcs.101212.
18. Koepke J, Kaffarnik F, Haag C, Zarnack K, Luscombe NM, König J, Ule J, Kellner R, Begerow D, Feldbrügge M. 2011. The RNA-binding protein Rrm4 is essential for efficient secretion of endochitinase Cts1. Mol Cell Proteomics 10:M111.011213.
19. Stock J, Sarkari P, Kreibich S, Brefort T, Feldbrügge M, Schipper K. 2012. Applying unconventional secretion of the endochitinase Cts1 to export heterologous proteins in Ustilago maydis. J Biotechnol 161:80-91. http://dx.doi.org/10.1016/j.jbiotec.2012.03.004.
20. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Terfrüchte M, Joehnk B, Fajardo-Somera R, Braus GH, Riquelme M, Schipper K, Feldbrügge M. 2014. Establishing a versatile Golden Gate cloning system for genetic engineering in fungi. Fungal Genet Biol 62:1-10. http://dx.doi.org/10.1016/j.fgb.2013.10.012.
22. Holliday R. 1974. Ustilago maydis, p 575-595. In King RC (ed), Handbook of genetics, vol 1. Plenum Press, New York, NY.
23. Brachmann A, König J, Julius C, Feldbrügge M. 2004. A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol Genet Genomics 272:216-226.
24. Kämper J. 2004. A PCR-based system for highly efficient generation of gene replacement mutants in Ustilago maydis. Mol Genet Genomics 271: 103-110. http://dx.doi.org/10.1007/s00438-003-0962-8.
25. Trudel J, Asselin A. 1989. Detection of chitinase activity after polyacrylamide gel electrophoresis. Anal Biochem 178:362-366. http://dx.doi.org/10.1016/0003-2697(89)90653-2.
26. Hamer SN, Cord-Landwehr S, Biarnés X, Planas A, Waegeman H, Moerschbacher BM, Kolkenbrock S. 2015. Enzymatic production of defined chitosan oligomers with a specific pattern of acetylation using a combination of chitin oligosaccharide deacetylases. Sci Rep 5:8716. http://dx.doi.org/10.1038/srep08716.
27. Mengerink Y, Deman HCJ, Vanderwal S. 1991. Use of an evaporative light-scattering detector in reversed-phase high-performance liquidchromatography of oligomeric surfactants. J Chromatogr 552:593-604. http://dx.doi.org/10.1016/S0021-9673(01)95975-8.
28. Decroos K, Vincken JP, Heng L, Bakker R, Gruppen H, Verstraete W. 2005. Simultaneous quantification of differently glycosylated, acetylated, and 2,3-dihydro-2,5-dihydroxy-6-methyl-4H-pyran-4-one-conjugated soyasaponins using reversed-phase high-performance liquid chromatography with evaporative light scattering detection. J Chromatogr A 1072: 185-193. http://dx.doi.org/10.1016/j.chroma.2005.03.021.
29. Remoroza C, Cord-Landwehr S, Leijdekkers AGM, Moerschbacher BM, Schols HA, Gruppen H. 2012. Combined HILIC-ELSD/ESI-MSn enables the separation, identification and quantification of sugar beet pectin derived oligomers. Carbohydr Polym 90:41-48. http://dx.doi.org/10.1016/j.carbpol.2012.04.058.
30. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Muller O, Perlin MH, Wosten HAB, de Vries R, Ruiz-Herrera J, Reynaga-Pena CG, Snetselaar K, McCann M, Perez-Martin J, Feldbrügge M, Basse CW, Steinberg G, Ibeas JI, Holloman W, Guzman P, Farman M, Stajich JE, Sentandreu R, Gonzalez-Prieto JM, Kennell JC, Molina L, Schirawski J, Mendoza-Mendoza A, Greilinger D, Munch K, Rossel N, Scherer M, Vranes M, Ladendorf O, Vincon V, Fuchs U, Sandrock B, Meng S, Ho ECH, Cahill MJ, Boyce KJ, Klose J, Klosterman SJ, Deelstra HJ, Ortiz-Castellanos L, Li W, Sanchez-Alonso P, Schreier PH, Häuser-Hahn I, Vaupel M, Koopmann E, Friedrich G, Voss H, Schlüter T, Margolis J, Platt D, Swimmer C, Gnirke A, Chen F, Vysotskaia V, Mannhaupt G, Güldener U, Münsterkötter M, Haase D, Oesterheld M, Mewes HW, Mauceli EW, DeCaprio D, Wade CM, Butler J, Young S, Jaffe DB, Calvo S, Nusbaum C, Galagan J, Birren BW. 2006. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444:97-101. http://dx.doi.org/10.1038/nature05248.
31. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490-D495. http://dx.doi.org/10.1093/nar/gkt1178.
32. Petersen TN, Brunak S, von Heijne G, Nielsen H. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785-786. http://dx.doi.org/10.1038/nmeth.1701.
33. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic Local Alignment Search Tool. J Mol Biol 215:403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2.
34. Brachmann A, Weinzierl G, Kamper J, Kahmann R. 2001. Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol Microbiol 42:1047-1063. http://dx.doi.org/10.1046/j.1365-2958.2001.02699.x.
35. Stöveken J, Singh R, Kolkenbrock S, Zakrzewski M, Wibberg D, Eikmeyer FG, Pühler A, Schlüter A, Moerschbacher BM. 2015. Successful heterologous expression of a novel chitinase identified by sequence analyses of the metagenome from a chitin-enriched soil sample. J Biotechnol 201:60-68. http://dx.doi.org/10.1016/j.jbiotec.2014.09.010.
36. Voth WP, Olsen AE, Sbia M, Freedman KH, Stillman DJ. 2005. ACE2, CBK1, and BUD4 in budding and cell separation. Eukaryot Cell 4:1018-1028. http://dx.doi.org/10.1128/EC.4.6.1018-1028.2005.
37. Weinzierl G, Leveleki L, Hassel A, Kost G, Wanner G, Bolker M. 2002. Regulation of cell separation in the dimorphic fungus Ustilago maydis. Mol Microbiol 45:219-231. http://dx.doi.org/10.1046/j.1365-2958.2002.03010.x.
38. Böhmer C, Böhmer M, Bölker M, Sandrock B. 2008. Cdc42 and the Ste20-like kinase Don3 act independently in triggering cytokinesis in Ustilago maydis. J Cell Sci 121:143-148. http://dx.doi.org/10.1242/jcs.014449.
39. Mahlert M, Leveleki L, Hlubek A, Sandrock B, Bolker M. 2006. Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol Microbiol 59:567-578. http://dx.doi.org/10.1111/j.1365-2958.2005.04952.x.
40. Heimel K, Scherer M, Vranes M, Wahl R, Pothiratana C, Schuler D, Vincon V, Finkernagel F, Flor-Parra I, Kamper J. 2010. The transcription factor Rbf1 is the master regulator for b-mating type controlled pathogenic development in Ustilago maydis. PLoS Pathog 6:e1001035. http://dx.doi.org/10.1371/journal.ppat.1001035.
41. Schink KO, Bolker M. 2009. Coordination of cytokinesis and cell separation by endosomal targeting of a Cdc42-specific guanine nucleotide exchange factor in Ustilago maydis. Mol Biol Cell 20:1081-1088.
42. Roncero C, Duran A. 1985. Effect of Calcofluor White and Congo Red on fungal cell-wall morphogenesis-in vivo activation of chitin polymerization. J Bacteriol 163:1180-1185.
43. Ram AF, Arentshorst M, Damveld RA, van Kuyk PA, Klis FM, van den Hondel CA. 2004. The cell wall stress response in Aspergillus niger involves increased expression of the glutamine: fructose-6-phosphate amidotransferase-encoding gene (gfaA) and increased deposition of chitin in the cell wall. Microbiology 150:3315-3326. http://dx.doi.org/10.1099/mic.0.27249-0.
44. Wan J, Zhang XC, Stacey G. 2008. Chitin signaling and plant disease resistance. Plant Signal Behav 3:831-833. http://dx.doi.org/10.4161/psb.3.10.5916.
45. Banuett F, Herskowitz I. 1996. Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122:2965-2976.
46. van den Burg HA, Harrison SJ, Joosten MHAJ, Vervoort J, de Wit PJGM. 2006. Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19:1420-1430. http://dx.doi.org/10.1094/MPMI-19-1420.
47. Feldbrügge M, Kamper J, Steinberg G, Kahmann R. 2004. Regulation of mating and pathogenic development in Ustilago maydis. Curr Opin Microbiol 7:666-672. http://dx.doi.org/10.1016/j.mib.2004.10.006.
48. Ruiz-Herrera J, Leon CG, Carabez-Trejo A, Reyes-Salinas E. 1996. Structure and chemical composition of the cell walls from the haploid yeast and mycelial forms of Ustilago maydis. Fungal Genet Biol 20:133-142. http://dx.doi.org/10.1006/fgbi.1996.0028.
49. Adams DJ. 2004. Fungal cell wall chitinases and glucanases. Microbiology 150:2029-2035. http://dx.doi.org/10.1099/mic.0.26980-0.
50. Colussi PA, Specht CA, Taron CH. 2005. Characterization of a nucleusencoded chitinase from the yeast Kluyveromyces lactis. Appl Environ Microbiol 71:2862-2869. http://dx.doi.org/10.1128/AEM.71.6.2862-2869.2005.
51. Baker LG, Specht CA, Lodge JK. 2009. Chitinases are essential for sexual development but not vegetative growth in Cryptococcus neoformans. Eukaryot Cell 8:1692-1705. http://dx.doi.org/10.1128/EC.00227-09.
52. Dekker N, Speijer D, Grun CH, van den Berg M, de Haan A, Hochstenbach F. 2004. Role of the alpha-glucanase Agn1p in fission-yeast cell separation. Mol Biol Cell 15:3903-3914. http://dx.doi.org/10.1091/mbc.E04-04-0319.
53. Alonso-Nunez ML, An HB, Martin-Cuadrado AB, Mehta S, Petit C, Sipiczki M, del Rey F, Gould KL, de Aldana CRV. 2005. Ace2p controls the expression of genes required for cell separation in Schizosaccharomyces pombe. Mol Biol Cell 16:2003-2017. http://dx.doi.org/10.1091/mbc.E04-06-0442.
54. Dekker N, de Haan A, Hochstenbach F. 2006. Transcription regulation of the alpha-glucanase gene agn1 by cell separation transcription factor Ace2p in fission yeast. FEBS Lett 580:3099-3106. http://dx.doi.org/10.1016/j.febslet.2006.04.061.
55. Colman-Lerner A, Chin TE, Brent R. 2001. Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates. Cell 107: 739-750. http://dx.doi.org/10.1016/S0092-8674(01)00596-7.
56. Doolin MT, Johnson AL, Johnston LH, Butler G. 2001. Overlapping and distinct roles of the duplicated yeast transcription factors Ace2p and Swi5p. Mol Microbiol 40:422-432. http://dx.doi.org/10.1046/j.1365-2958.2001.02388.x.
57. Sandrock B, Böhmer C, Bölker M. 2006. Dual function of the germinal centre kinase Don3 during mitosis and cytokinesis in Ustilago maydis. Mol Microbiol 62:655-666. http://dx.doi.org/10.1111/j.1365-2958.2006.05405.x.
58. Choi WJ, Sburlati A, Cabib E. 1994. Chitin synthase 3 from yeast has zymogenic properties that depend on both the CAL1 and the CAL3 genes. Proc Natl Acad Sci U S A 91:4727-4730. http://dx.doi.org/10.1073/pnas.91.11.4727.
59. Tao J, Ginsberg I, Banerjee N, Held W, Koltin Y, Bruenn JA. 1990. Ustilago maydis KP6 killer toxin: structure, expression in Saccharomyces cerevisiae, and relationship to other cellular toxins. Mol Cell Biol 10:1373-1381.
60. Sarkari P, Reindl M, Stock J, Muller O, Kahmann R, Feldbrügge M, Schipper K. 2014. Improved expression of single-chain antibodies in Ustilago maydis. J Biotechnol 191:165-175. http://dx.doi.org/10.1016/j.jbiotec.2014.06.028.
61. Lanver D, Berndt P, Tollot M, Naik V, Vranes M, Warmann T, Munch K, Rossel N, Kahmann R. 2014. Plant surface cues prime Ustilago maydis for biotrophic development. PLoS Pathog 10:e1004272. http://dx.doi.org/10.1371/journal.ppat.1004272.
62. Maddi A, Bowman SM, Free SJ. 2009. Trifluoromethanesulfonic acidbased proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genet Biol 46:768-781. http://dx.doi.org/10.1016/j.fgb.2009.06.005.
63. Tzelepis GD, Melin P, Jensen DF, Stenlid J, Karlsson M. 2012. Functional analysis of glycoside hydrolase family 18 and 20 genes in Neurospora crassa. Fungal Genet Biol 49:717-730. http://dx.doi.org/10.1016/j.fgb.2012.06.013.
64. Takaya N, Yamazaki D, Horiuchi H, Ohta A, Takagi M. 1998. Cloning and characterization of a chitinase-encoding gene chiA from Aspergillus nidulans, disruption of which decreases germination frequency and hyphal growth. Biosci Biotechnol Biochem 62:60-65. http://dx.doi.org/10.1271/bbb.62.60.
65. Yamazaki H, Tanaka A, Kaneko J, Ohta A, Horiuchi H. 2008. Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites. Fungal Genet Biol 45:963-972. http://dx.doi.org/10.1016/j.fgb.2008.02.008.
66. Jaques AK, Fukamizo T, Hall D, Barton RC, Escott GM, Parkinson T, Hitchcock CA, Adams DJ. 2003. Disruption of the gene encoding the ChiB1 chitinase of Aspergillus fumigatus and characterization of a recombinant gene product. Microbiology 149:2931-2939. http://dx.doi.org/10.1099/mic.0.26476-0.
67. de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MHAJ, Thomma BPHJ. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953-955. http://dx.doi.org/10.1126/science.1190859.
68. Hemetsberger C, Herrberger C, Zechmann B, Hillmer M, Doehlemann G. 2012. The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog 8:e1002684. http://dx.doi.org/10.1371/journal.ppat.1002684.
69. Rodriguez Estrada AE, Jonkers W, Corby Kistler H, May G. 2012. Interactions between Fusarium verticillioides, Ustilago maydis, and Zea mays: an endophyte, a pathogen, and their shared plant host. Fungal Genet Biol 49:578-587. http://dx.doi.org/10.1016/j.fgb.2012.05.001.
70. Teichmann B, Linne U, Hewald S, Marahiel MA, Bölker M. 2007. A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol Microbiol 66:525-533. http://dx.doi.org/10.1111/j.1365-2958.2007.05941.x.
71. Banuett F. 1995. Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu Rev Genet 29:179-208. http://dx.doi.org/10.1146/annurev.ge.29.120195.001143.
72. Gruber S, Seidl-Seiboth V. 2012. Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 158:26-34. http://dx.doi.org/10.1099/mic.0.052613-0.
73. Spellig T, Bottin A, Kahmann R. 1996. Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol Gen Genet 252:503-509.
74. Vollmeister E, Haag C, Zarnack K, Baumann S, König J, Mannhaupt G, Feldbrügge M. 2009. Tandem KH domains of Khd4 recognize AUACCC and are essential for regulation of morphology as well as pathogenicity in Ustilago maydis. RNA 15:2206-2218. http://dx.doi.org/10.1261/rna.1817609.