Wide distribution of the Ustilago maydis-bacterium endosymbiosis in naturally infected maize plants

References

• Arendt KR, Hockett KL, Araldi-Brondolo SJ, Baltrus DA, Arnold AE, Cullen D. Isolation of endohyphal bacteria from foliar ascomycota and in vitro establishment of their symbiotic associations. Appl Environ Microbiol. 2016;82:1–6. doi:10.1128/AEM.00452-16.
   Web of Science ®Google Scholar
• Bertaux J, Schmid M, Hutzler P, Hartmann A, Garbaye J, Frey-Klett P. Occurrence and distribution of endobacteria in the plant-associated mycelium of the ectomycorrhizal fungus Laccaria bicolor S238N. Environ Microbiol. 2005;7(11):1786–1795. doi:10.1111/j.1462-2920.2005.00867.x.
   PubMed Web of Science ®Google Scholar
• Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P. An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol. 1996;62(8):3005–3010. doi:10.1128/AEM.62.8.3005-3010.1996.
   PubMed Web of Science ®Google Scholar
• Desirò A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S, Faccio A, Kaech A, Pawlowska TE, Bonfante P. Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. Isme J. 2014;8:257–270. doi:10.1038/ismej.2013.151.
   PubMed Web of Science ®Google Scholar
• Fitzpatrick EE First bacterial endosymbionts found in the phylum Ascomycota. Dissertations and Theses. 2013; paper 675.
   Google Scholar
• Partida-Martínez LP, Monajembashi S, Greulich KO, Hertweck C. Endosymbiont-dependent host reproduction maintains bacterial-fungal mutualism. Curr Bio. 2007;17:773–777. doi:10.1016/j.cub.2007.03.039.
   PubMed Web of Science ®Google Scholar
• Sato Y, Narisawa K, Tsuruta K, Umezu M, Nishizawa T, Tanaka K, Yamaguchi K, Komatsuzaki M, Ohta H. Detection of betaproteobacteria inside the mycelium of the fungus Mortierella elongate. Microbes Environ. 2010;25:321–324. doi:10.1264/jsme2.ME10134.
   PubMed Web of Science ®Google Scholar
• Schüßmer A, Mollenhauer D, Schnepf E, Kluge M. Geosiphon pyriforme, an endosymbiotic association of fungus and cyanobacteria: the spore structure resembles that of arbuscular mycorrhizal [AM] fungi. Bot Acta. 1994;107:36–45. doi:10.1111/j.1438-8677.1994.tb00406.x.
   Google Scholar
• Sharma M, Schmid M, Rothballer M, Hause G, Zuccaro A, Imani J, Kämpfer P, Domann E, Schäfer P, Hartmann A, et al. Detection and identification of bacteria intimately associated with fungi of the order Sebacinales. Cell Microbiol. 2008;10:2235–2246. doi:10.1111/j.1462-5822.2008.01202.x.
   PubMed Web of Science ®Google Scholar
• Bonfante P, Desirò A. Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota. Isme J. 2017;11:1727–1735.
   PubMed Web of Science ®Google Scholar
• Deveau A, Bonito G, Uehling J, Paoletti M, Becker M, Bindschedler S, Hacquard S, Hervé V, Labbé J, Lastovetsky OA, et al. Bacterial–fungal interactions: ecology, mechanisms and challenges. FEMS Microbiol Rev. 2018;42:335–352.
   PubMed Web of Science ®Google Scholar
• Bianciotto V, Genre A, Jargeat P, Lumini E, Bécard G, Bonfante P. Vertical transmission of endobacteria in the arbuscular mycorrhizal fungus Gigaspora margarita through generation of vegetative spores. Appl Environ Microbiol. 2004;70(6):3600–3608. doi:10.1128/AEM.70.6.3600-3608.2004.
   PubMed Web of Science ®Google Scholar
• Hoffman MT, Gunatilaka MK, Wijeratne K, Gunatilaka L, Arnold AE, Corradi N. Endohyphal bacterium enhances production of indole-3-acetic acid by a foliar fungal endophyte. PLoS ONE. 2013;8:1–8. doi:10.1371/journal.pone.0073132.
   Web of Science ®Google Scholar
• Uehling J, Gryganskyi A, Hameed K, Tschaplinski T, Misztal PK, Wu S, Desirò A, Vande Pol N, Du Z, Zienkiewicz A, et al. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ Microbiol. 2017;19(8):2964–2983. doi:10.1111/1462-2920.13669.
   PubMed Web of Science ®Google Scholar
• Lackner G, Möbius N, Scherlach K, Partida-Martinez LP, Winkler R, Schmitt I, Hertweck C. Global distribution and evolution of a toxinogenic Burkholderia-Rhizopus symbiosis. MBio. 2009;75:2982–2986.
   Google Scholar
• Bianciotto V, Lumini E, Lanfranco L, Minerdi D, Bonfante P, Perotto S. Detection and identification of bacterial endosymbionts in arbuscular mycorrhizal fungi belonging to the family Gigasporaceae. MBio. 2000;66:4503–4509.
   Google Scholar
• Desirò A, Faccio A, Kaech A, Bidartondo MI, Bonfante P. Endogone, one of the oldest plant-associated fungi, host unique Mollicutes-related endobacteria. New Phytol. 2015;205:1464–1472. doi:10.1111/nph.13136.
   PubMed Web of Science ®Google Scholar
• Mondo SJ, Toomer KH, Morton JB, Lekberg Y, Pawlowska TE. Evolutionary stability in a 400-million-year-old heritable facultative mutualism. Evolution. 2012;66(8):2564–2576. doi:10.1111/j.1558-5646.2012.01611.x.
   Google Scholar
• Bölker M, Urban M, Kahmann R. The a mating type locus of U. maydis specifies cell signaling components. Cell. 1992;68:441–450. doi:10.1016/0092-8674(92)90182-C.
   PubMed Web of Science ®Google Scholar
• Müller P, Weinzierl G, Brachmann A, Feldbrügge M, Kahmann R. Mating and pathogenic development of the smut fungus Ustilago maydis are regulated by one mitogen-activated protein kinase cascade. Eukaryot Cell. 2003;2:1187–1199. doi:10.1128/EC.2.6.1187-1199.2003.
   PubMedGoogle Scholar
• Banuett F, Different HI. a alleles of Ustilago maydis are necessary for maintenance of filamentous growth but not for meiosis. Proc Natl Acad Sci USA. 1989;86:5878–5882. doi:10.1073/pnas.86.15.5878.
   PubMed Web of Science ®Google Scholar
• Banuett F, Herskowitz I. Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development. 1996;122:2965–2976.
   PubMed Web of Science ®Google Scholar
• Cabrera-Ponce JL, León-Ramírez CG, Verver-Vargas A, Palma-Tirado L, Ruiz- Herrera J. Metamorphosis of the Basidiomycota Ustilago maydis: transformation of yeast-like cells into basidiocarps. Fungal Genet Biol. 2012;49:765–771. doi:10.1016/j.fgb.2012.07.005.
   PubMed Web of Science ®Google Scholar
• Ruiz-Herrera J, León-Ramírez CG, Guevara-Olvera L, Cárabez-Trejo A. Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis. Microbiology. 1995;141:695–703. doi:10.1099/13500872-141-3-695.
   Web of Science ®Google Scholar
• Feldbrügge M, Bölker M, Steinberg G, Kämper J, Kahmann R. Regulatory and structural networks orchestrating mating, dimorphism, cell shape, and pathogenesis in Ustilago maydis. In: Kües U, Fischer R, editors. The mycota i growth, differentiation and sexuality. Heidelberg, GermanyBerlin: Heidelberg Springer-Verlag; 2006. p. 375–391.
   Google Scholar
• Heimel K, Scherer M, Schuler D, The KJ. Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. Plant Cell. 2010;22:2908–2922. doi:10.1105/tpc.110.076265.
   PubMed Web of Science ®Google Scholar
• Banuett F. History of the mating types in Ustilago maydis. In: Heitman J, JW K, JW T, LA C, editors. Sex in fungi: molecular determination and evolutionary implications. Washington DC, USA; ASM Press: 2007. p. 351–375.
   Google Scholar
• Ruiz-Herrera J, León-Ramírez C, Vera-Núñez A, Sánchez‐Arreguín A, Ruiz‐Medrano R, Salgado‐Lugo H, Sánchez‐Segura L, Peña‐Cabriales JJ. A novel intracellular nitrogen-fixing symbiosis made by Ustilago maydis and Bacillus spp. New Phytol. 2015;207:769–777. doi:10.1111/nph.13359.
   PubMed Web of Science ®Google Scholar
• Li W, Lee SY, Cho YJ, Ghim SY, Jung HY. Mediation of induced systemic resistance by the plant growth-promoting rhizobacteria Bacillus pumilus S2-3-2. Mol Biol Rep. 2020 Oct 10;47:8429–8438. PMID: 33037963. doi:10.1007/s11033-020-05883-9.
   PubMed Web of Science ®Google Scholar
• Masood S, Zhao XQ, Shen RF. Bacillus pumilus promotes the growth and nitrogen uptake of tomato plants under nitrogen fertilization. Sci Hortic (Amsterdam). 2020;272:109581. doi:10.1016/j.scienta.2020.109581.
   Web of Science ®Google Scholar
• Holliday R. The genetics of Ustilago maydis. Genet Res. 1961;2(2):204–230. doi:10.1017/S0016672300000719.
   Web of Science ®Google Scholar
• Kronstad JW, Leong SA. Isolation of two alleles of the b locus of Ustilago maydis. Proc Natl Acad Sci USA. 1989;86:978–982. doi:10.1073/pnas.86.3.978.
   PubMed Web of Science ®Google Scholar
• Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, Banuett F, Kronstad JW, Gold SE, Müller O, et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature. 2006;444:97–101. doi:10.1038/nature05248.
   PubMed Web of Science ®Google Scholar
• Burris RH. Methodology. In: Quispel A, editor. Biology of nitrogen fixation. Amsterdam, Netherlands: North-Holland Publishing Co Amsterdam; 1974. p. 3–42.
   Google Scholar
• Cavalcante VA, Dobereiner J. A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. Plant Soil. 1988;108:23–31. doi:10.1007/BF02370096.
   Web of Science ®Google Scholar
• Estrada-de Los Santos P, Bustillos-Cristales Y, Caballero-Mellado J. Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol. 2001;67:2790–2798. doi:10.1128/AEM.67.6.2790-2798.2001.
   PubMed Web of Science ®Google Scholar
• Tsukuda T, Carleton S, Fotheringham S, Holloman WK. Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol Cell Biol. 1988;8:3703–3709. doi:10.1128/MCB.8.9.3703.
   PubMed Web of Science ®Google Scholar
• Bracker CE, Ruiz-Herrera J, Bartnicki-Garcia S. Structure and transformation of chitin synthetase particles (chitosomes) during microfibril synthesis in vitro. Proc Natl Acad Sci USA. 1976;73(12):4570–4574. doi:10.1073/pnas.73.12.4570.
   PubMed Web of Science ®Google Scholar
• Klappenbach JA, Saxman PR, Cole JR, Schmidt TM. rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res. 2001;29:181–184.
   PubMed Web of Science ®Google Scholar
• Palacios R, Brom S, Davila G, Flores M, Girard ML, Romero D, Stepkowski T. Gene amplification in Rhizobium. In: Palacios R, Mora J, Newton WE, editors. New horizons in nitrogen fixation. Dordrecht, The Netherlands; Kluwer Academic Publishers: 1993. p. 581–585.
   Google Scholar
• FJ B. Biological nitrogen fixation. In: Lugtenberg B editor. Principles of plant-microbe interactions. Hoboken, New Jersey, USA: Springer, Cham; 2015. p. 215–224.
   Google Scholar
• Gomez NC, Kosheleva IA, Abraham WR, Smalla K. Effect of the inoculant strain Pseudomonas putida KT2442 (pNF142) and of naphthalene contamination on soil bacterial community. FEMS Microbiol Ecol. 2005;54:21–33. doi:10.1016/j.femsec.2005.02.005.
   PubMed Web of Science ®Google Scholar
• Heuer H, Krsek M, Baker P, Smalla K, Wellington EM. Analysis of actinomycete communities by specific amplification of genes encoding 16sRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol. 1997;63:3233–3241. doi:10.1128/AEM.63.8.3233-3241.1997.
   PubMed Web of Science ®Google Scholar