Advertisement

Arbuscular Mycorrhiza and Endophytic Fungi in Ruspestrian Grasslands

  • Yumi Oki
  • Bruno Tomio Goto
  • Khadija Jobim
  • Luiz Henrique Rosa
  • Mariana Costa Ferreira
  • Etiene Silva Coutinho
  • João Henrique de Azevedo Xavier
  • Fernanda Carvalho
  • Fatima Maria de Souza Moreira
  • Francisco Adriano de Souza
  • Ricardo Luís Louro Berbara
  • G. Wilson Fernandes
Chapter

Abstract

Rupestrian grasslands are a biodiversity hotspot for arbuscular mycorrhizal fungi (AMF) and endophytic fungi. These groups have major influence on the structure and dynamics of the plant community in this ecosystem. AMF are generalists, associating with a wide variety of host plants , while endophytic fungi tend to establish more specific relations with host plants. AMF distribution is mainly influenced by soil attributes, while the distribution of endophytic fungi is mostly driven by the host plant. Both fungal groups influence the host plant metabolism and ecology , enhancing the host plant survival in this harsh ecosystem. There are no studies relating both fungal groups in rupestrian grasslands. A strong relation may exist between them, and exploring this gap will contribute to the understanding of this unique ecosystem and the relations in it.

Keywords

Arbuscular Mycorrhizal Fungus Endophytic Fungus Arbuscular Mycorrhizal Fungus Species Arbuscular Mycorrhizal Fungus Community Arbuscular Mycorrhizal Fungus Diversity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank for CNPq, FAPEMIG and CAPES for grants and scholarships to the authors. We also thank for John Schroeder for careful reading the manuscript and for his helpful comments and suggestions.

References

  1. Arnold AE, Herre EA (2003) Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae). Mycol 95:388–398CrossRefGoogle Scholar
  2. Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hostpots? Ecology 88:541–549CrossRefPubMedGoogle Scholar
  3. Azevedo JL (1998) Microorganismos endofíticos. In: de Melo IS, Azevedo JL (eds) Ecologia microbiana. Embrapa, Jaguariúna, pp 117–137Google Scholar
  4. Belmiro MS (2010) Herbivoria e resinas - fatores mediadores da composição de fungos endofíticos em Baccharis dracunculifolia DC (Asteraceae). 2010. Monograph, Pontifícia Universidade Católica de Minas GeraisGoogle Scholar
  5. Berbara RLL, De Sousa FA, Fonseca HMA (2006) Fungos micorrízicos arbusculares: muito além da nutrição. In: Fernandes MS (ed) Nutrição mineral de plantas. SBCS, Viçosa, pp 53–88Google Scholar
  6. Bonfim JA, Vasconcellos RLF, Stürmer SL, Cardoso EJBN (2013) Arbuscular mycorrhizal fungi in the Brazilian Atlantic forest: a gradient of environmental restoration. Appl Soil Ecol 71:7–14CrossRefGoogle Scholar
  7. Bononi VLR, Trufem SFB (1983) Endomicorrizas vesículo-arbusculares do cerrado da Reserva Biológica de Moji-Guaçú, SP, Brasil. Rickia 10:55–84Google Scholar
  8. Breen JP (1994) Acremonium endophyte interactions with enhanced plant resistance to insect. Annu Ver Entomol 86:401–423CrossRefGoogle Scholar
  9. Carneiro MAC, Siqueira JO, Moreira FMS, Carvalho D, Botelho S (1998) Micorriza arbusculares em espécies arbóreas e arbustivas nativas de ocorrência no Sudeste do Brasil. Rev Cerne 4:129–145Google Scholar
  10. Carvalho F, Souza FA, Carrenho R, Moreira FMS, Jesus EC, Fernandes GW (2012) The mosaic of habitats in the high-altitude Brazilian rupestrian fields is a hotspot for arbuscular mycorrhizal fungi. Appl Soil Ecol 52:9–19CrossRefGoogle Scholar
  11. Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Evol Syst 21:275–297CrossRefGoogle Scholar
  12. Clay K (2004) Fungi and the food of the gods. Nature 427:401–402CrossRefPubMedGoogle Scholar
  13. Cordazo CV, Stürmer SL (2007) Ocorrência de fungos micorrízicos arbusculares em Panicum Racemosum (P. Beauv.) Spreng (Poaceae) em dunas costeiras do extremo sul do Brasil. Atlântica 29:65–68Google Scholar
  14. Cordoba AS, Mendonça MM, Stürmer SL, Rygiewicz PT (2001) Diversity of arbuscular mycorrhizal fungi along a sand dune stabilization gradient: a case study at Praia da Joaquina, Ilha de Santa Catarina, South Brasil. Mycoscience 42:379–387CrossRefGoogle Scholar
  15. Cota B, Rosa L, Caligiorne R, Rabello T, Rosa C, Zani C (2008) Altenusin, a biphenyl isolated from the endophytic fungus Alternaria sp. inhibits trypanothione reductase from Trypanosoma cruzi. FEMS Microbiol Lett 285:177–182CrossRefPubMedGoogle Scholar
  16. Coutinho ES, Fernandes GW, Berbara RLL, Valerio HM, Goto BT (2015) Variation of arbuscular mycorrhizal fungal communities along an altitudinal gradient in rupestrian fields in Brazil‏. Mycorrhiza 25:627–638Google Scholar
  17. Dantas ALA, Valente LMM, Morais LASD, Feliciano G, Bernardo-Filho M (2005) Vitro study of Vellozia pusilla pohl (Velloziaceae), a Brazilian plant species: antitumoral activity and labeling of blood elements. Braz Arch Bio Tech 48:63–67Google Scholar
  18. Dodd JC (2000) The role of arbuscular mycorrizal fungi in agro and natural ecosystems. Outlook Agri 29:55–62CrossRefGoogle Scholar
  19. Fernandes GW, Price PW (1992) The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecol 90:14–20CrossRefGoogle Scholar
  20. Fernandes GW, Oki Y, Sanchez-Azofeifa A, Faccion G, Amaro-Arruda HC (2011) Hail impact on leaves and endophytes of the endemic threatened Coccoloba cereifera (Polygonaceae). Plant Ecol 212:1687–1697CrossRefGoogle Scholar
  21. Gaylord ES, Preszler RW, Boecklen WJ (1996) Interaction between host plants, endophytic fungi and phytophagous insect in an oak (Quercus grisea × Quercus gambelli) hybrid zone. Oecol 105:336–342CrossRefGoogle Scholar
  22. Gene RM, Panizza S, Correa PL (1996) Anti-inflamatory and analgesic activity of Baccharis trimera: identification of its constituents. Planta Med 62:232–235CrossRefPubMedGoogle Scholar
  23. Gianinazzi S, Gollote A, Binet MN, Van Tuinen T, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530CrossRefPubMedGoogle Scholar
  24. Gomide PHO, Silva MLN, Soares CRFS, Cardoso EL, Carvalho F, Leal PL, Marques RM, Stürmer SL (2014) Fungos micorrízicos arbusculares em fitofisionomias do pantanal da Nhecolândia, Mato Grosso do Sul. Rev Bras Ci Solo 38:1114–1127CrossRefGoogle Scholar
  25. Goto BT, Silva GA, Yano-Melo AM, Maia LC (2010) Checklist of the arbuscular mycorrhizal fungi (Glomeromycota) in the Brazilian semiarid. Mycotaxon 113:251–254CrossRefGoogle Scholar
  26. Goto BT, Silva GA, Assis DM, Silva DKA, Souza RG, Ferreira ACA, Jobim K, Mello CMA, Vieira HEE, Maia LC, Oehl F (2012) Intraornatosporaceae: (Gigasporales), a new family with two new genera and two new species. Mycotaxon 119:117–132CrossRefGoogle Scholar
  27. Gupta V, Satyanarayana T, Garg S (2000) General aspects of mycorrhiza. In: Mukerji KG, Chamola BP, Singh J (eds) Mycorrhizal biology. Kluwer Academic/Plenum Publishers, New York, pp 27–44CrossRefGoogle Scholar
  28. Hawksworth DL (2001) The magnitude of fungal diversity: the 1.5 million species estimate revised. Mycol Res 105:1422–1432CrossRefGoogle Scholar
  29. Jacobi CM, Do Carmo FF, Vincent RC, Stehmann JR (2007) Plant communities on ironstone outcrops: a diverse and endangered Brazilian ecosystem. Biodiv Cons 16:2185–2200CrossRefGoogle Scholar
  30. Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303CrossRefGoogle Scholar
  31. Leal PL, Stürmer SL, Siqueira JO (2009) Occurrence and diversity of arbuscular mycorrhizal fungi in trap cultures from soils under different land use systems in the Amazon, Brazil. Braz J Microb 40:111–121CrossRefGoogle Scholar
  32. Leal PL, Siqueira JO, Stürmer SL (2013) Switch of tropical Amazon forest to pasture affects taxonomic composition but not species abundance and diversity of arbuscular mycorrhizal fungal community. Appl Soil Ecol 71:72–80CrossRefGoogle Scholar
  33. Lee EH, Eo JK, Ka KH, Eom AH (2013) Diversity of arbuscular mycorrhizal fungi and their roles in ecosystems. Mycobiology 41:121–125CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lima LL, Kozovits AR, Assis DMA, Silva GA, Oehl F (2014) Cetraspora auronigra, a new glomermycetes species from Ouro Preto, Minas Gerais (Brazil). Sydowia 66:299–308Google Scholar
  35. Liu H, Heckman JR, Murphy JA (1996) Screening fine fescues for aluminum tolerance. J Plant Nutr 19:677–688CrossRefGoogle Scholar
  36. Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 133:727–733CrossRefGoogle Scholar
  37. Mello CMA, Silva GA, Vieira HEE, Silva IR, Maia LC, Oehl F (2012) Fuscutata aurea, a new species in the Glomeromycetes from cassava and maize fields in the Atlantic rainforest zone in Northeastern Brazil. Nova Hedwigia 95:267–275CrossRefGoogle Scholar
  38. Miranda JCC (2008) Cerrado: micorriza arbuscular: ocorrência e manejo. Embrapa Cerrados, Planaltina 169pGoogle Scholar
  39. Moreira M, Baretta D, Tsai SM, Gomes-da-Costa SM, Cardoso EJBN (2007) Biodiversity and distribution of arbuscular mycorrhizal fungi in Araucaria angustifolia. Forest Sci Agric 64:393–399Google Scholar
  40. Nascimento IM (2010) Avaliação da atividade antipatogênica e enzimática de três fungos endofiticos de Baccharis dracunculifolia (Asteraceae). Monograph, Pontifícia Universidade Católica de Minas GeraisGoogle Scholar
  41. Novaes MRCG, Novaes LCG, Taveira VC (2007) Efeitos farmacológicos dos fungos Agaricales: uma revisão de evidência. Rev Cienc Med 16:87–95Google Scholar
  42. Novais CB, Borges WL, Jesus EC, Saggin Junior OJ, Siqueira JO (2014) Inter and intraspecific functional variability of tropical arbuscular mycorrhizal fungi isolates colonizing corn plants. Appl Soil Ecol 76:78–86CrossRefGoogle Scholar
  43. Oki Y, Fernandes GW, Correa Junior A (2008) Fungos: Amigos ou Inimigos? Cien Hoje 42:64–66Google Scholar
  44. Oki Y, Soares NR, Belmiro MS, Correa-Junior A, Fernandes GW (2009) The influence of the endophytic fungi on the herbivores from Baccharis dracunculifolia (Asteraceae). Neotrop Biol Cons 4:83–88CrossRefGoogle Scholar
  45. Oliveira JRG, Souza RG, Silva FSB, Mendes ASM, Yano-Melo AM (2009) O papel da comunidade de fungos micorrízicos arbusculares (FMA) autóctones no desenvolvimento de espécies vegetais nativas em área de dunas de restinga revegetadas no litoral do Estado da Paraíba. Rev Bras Bot 32:663–670CrossRefGoogle Scholar
  46. Pagano MC, Scotti MR (2009) A survey of the mycorrhiza occurrence in Paepalanthus bromelioids and Bulbostylis sp. in rupestrian fields, Brazil. Micol Appl Int 21:1–10Google Scholar
  47. Pereira CMR, Silva DKA, Ferreira ACA, Goto BT, Maia LC (2014) Diversity of arbuscular mycorrhizal fungi in Atlantic forest areas under different land uses. Agr Ecosyst Environ 185:245–252CrossRefGoogle Scholar
  48. Petrini O, Sieber TH, Toti L, Viret O (1992) Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat Tox 1:185–196CrossRefGoogle Scholar
  49. Prance GT (1994) A comparison of the efficacy of higher taxa and species numbers in the assessment of biodiversity in the Neotropics. Philos Trans R Soc Lond B Biol Sci 345:89–99CrossRefGoogle Scholar
  50. Preszler RW, Gaylord ES, Boecklen WJ (1996) Reduced parasitism of a leaf-mining moth on trees with high infection frequencies of an endophytic fungus. Oecol 108:159–166CrossRefGoogle Scholar
  51. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems–a journey towards relevance? New Phytol 157:475–492CrossRefGoogle Scholar
  52. Redman RS, Sheehan KB, Stout RG, Rodriguez JR, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581pCrossRefGoogle Scholar
  53. Rodrigues RL (2010) Fungos endofíticos associados à Vellozia compacta Mart. ex Schult. F. (Velloziaceae) presente em afloramentos rochosos nos estados de Minas Gerais e Tocantins. Dissertacion, Universidade Federal de Ouro PretoGoogle Scholar
  54. Rodriguez JR, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adap Strat Glob Chan 9:261–272CrossRefGoogle Scholar
  55. Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte–plant symbioses. Trends Plant Sci 9:275–280CrossRefPubMedGoogle Scholar
  56. Sanchez-Azofeifa A, Oki Y, Fernandes GW, Ball RA, Gamon J (2011) Relationships between endophyte diversity and leaf optical properties. Trees 26:291–299CrossRefGoogle Scholar
  57. Santiago IF (2008) Bioprospecção de fungos endofíticos associados à Vellozia graninea Pohl. presente em afloramentos rochosos da Cadeia do Espinhaço, Minas Gerais. Monograph, Universidade Federal de Ouro PretoGoogle Scholar
  58. Santos OM, Oliveira NC, Novais RF (1995) Observações preliminares sobre fungos micorrízicos vesículo-arbusculares em plantas crescendo em dunas na Bahia. Rev Ceres 42:191–202Google Scholar
  59. Schenck NCL, Siqueira JO, Oliveira E (1989) Changes in the incidence of VA mycorrhizal fungi with changes in ecosystems. Dev Soil Sci 18:125–129CrossRefGoogle Scholar
  60. Sette LD, Passarini MRZ, Delarmelina C, Salati F, Duarte MCT (2006) Molecular characterization and antimicrobial activity of endophytic fungi from coffee plants. World J Microb Biot 22:1185–1195CrossRefGoogle Scholar
  61. Silva DKA, Pereira CMR, Souza RG, Silva GA, Oehl F, Maia LC (2012) Diversity of arbuscular mycorrhizal fungi in resting and dunes areas in Brazilian Northeast. Biodiv Cons 21:2361–2373CrossRefGoogle Scholar
  62. Siqueira JO, Colozzi-Filho A, Oliveira E (1989) Ocorrência de micorrizas vesicular-arbusculares em agro e ecossistemas do estado de Minas Gerais. Pesq Agropec Bras 24:1499–1506Google Scholar
  63. Smith SE, Read D (2008) Mycorrhizal symbiosis, 3ª edn. Academic Press, San DiegoGoogle Scholar
  64. Soicke H, Almeida ER, Costa AF (1986) Characterisation of flavonoids from Baccharis trimera and their properties. Planta Med 52:37–39Google Scholar
  65. Sousa MP, Matos MO, Matos FJ (1991) Constituintes químicos de plantas medicinais brasileiras. UFC Edições, FortalezaGoogle Scholar
  66. Souza FA, Silva ICL, Berbara RLL (2007) Fungos micorrízicos arbusculares: muito mais diversos do que se imaginava. In: Moreira FMS, Siqueira JO, Brussard L (eds) Biodiversidade do solo em ecossistemas brasileiros. UFLA, Lavras, pp 483–536Google Scholar
  67. Souza FA, Stürmer SL, Carrenho R, Trufem SFB (2010) Classificação e taxonomia de fungos micorrízicos arbusculares e sua diversidade e ocorrência no Brasil. In: Siqueira JO, Souza FA, Cardoso EJBN, Tsai SM (eds) Micorrizas: 30 anos de pesquisas no Brasil. Editora UFLA, Lavras p, pp 15–73Google Scholar
  68. Strobel G (2002) Endophytes as sources of bioactive products. Microb Infect 5:535–544CrossRefGoogle Scholar
  69. Stürmer SL, Siqueira JO (2008) Diversidade de fungos micorrízicos arbusculares em ecossistemas brasileiros. In: Moreira FMS, Siqueira JO, Brussard L (eds) Biodiversidade do solo em ecossistemas brasileiros. UFLA, Lavras, pp 537–584Google Scholar
  70. Stürmer SL, Stürmer R, Pasqualini D (2013) Taxonomic diversity and community structure of arbuscular mycorrhizal fungi (Phylum Glomeromycota) in three maritime sand dunes in Santa Catarina State, South Brazil. Fungal Ecol 6:27–36CrossRefGoogle Scholar
  71. Sylvia DM, Williams SE (1992) Vesicular-arbuscular mycorrhizae and environmental stress. In: Bethlenfalvay GJ, Linderman RG (eds) Mycorrhizae in sustainable agriculture. Madison, J AM Soc Agron, pp 101–124Google Scholar
  72. Tejesvi MV, Kini KR, Prakash HS, Subbiah V, Shetty HS (2007) Genetic diversity and antifungal activity of species of Pestalotiopsis isolated as endophytes from medicinal plants. Fungal Divers 24:37–54Google Scholar
  73. Trufem SFB (1990) Aspectos ecológicos de fungos micorrízicos vesículo-arbusculares da mata tropica tropical úmida da Ilha do Cardoso, SP, Brasil. Acta Bot Bras 4:31–45CrossRefGoogle Scholar
  74. Trufem SFB (1995) Aspectos ecológicos de fungos micorrízicos arbusculares na rizosfera de plantas de restinga da Ilha do Cardoso, SP, Brasil. Rev Bras Bot 18:51–60Google Scholar
  75. Trufem SFB, Otomo HS, Malatinszky SMM (1989) Fungos micorrízicos vesículos arbusculares em rizosferas de plantas em dunas do Parque Estadual da Ilha do Cardoso, São Paulo, Brasil. Acta Bot Bras 3:141–152CrossRefGoogle Scholar
  76. Trufem SFB, Malatinszky SMM, Otomo HS (1994) Fungos micorrízicos arbusculares em rizosferas de plantas do litoral arenoso do Parque Estadual da Ilha do Cardoso, SP, Brasil. Acta Bot Bras 8:219–229Google Scholar
  77. Vaz ABM, Mota RC, Bomfim MRQ, Vieira MLA, Zani CL, Rosa CA, Rosa LH (2009) Antimicrobial activity of endophytic fungi associated with Orchidaceae in Brazil. Can J Microbiol 55:1381–1391CrossRefPubMedGoogle Scholar
  78. Ventura CP, Oliveira ABD, Braga FC (2007) Antimicrobial activity of Trembleya laniflora, Xyris platystachia and Xyris pterygoblephara. Rev Bras Farm 17:17–22CrossRefGoogle Scholar
  79. Vieira ML, Johann S, Hughes FM, Rosa CA, Rosa LH (2014) The diversity and antimicrobial activity of endophytic fungi associated with medicinal plant Baccharis trimera (Asteraceae) from the Brazilian savannah. Microbiol 60:847–856Google Scholar
  80. Wilson D (1993) Fungal endophytes: out of sight but should not be out of mind. Oikos 68:379–384CrossRefGoogle Scholar
  81. Zaurov DE, Bonos S, Murphy JA, Richardson M, Belanger FC (2001) Endophyte infection can contribute to aluminum tolerance in fine fescues. Crop Sci 41:1981–1984CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Yumi Oki
    • 1
  • Bruno Tomio Goto
    • 2
  • Khadija Jobim
    • 3
  • Luiz Henrique Rosa
    • 4
  • Mariana Costa Ferreira
    • 4
  • Etiene Silva Coutinho
    • 5
  • João Henrique de Azevedo Xavier
    • 5
  • Fernanda Carvalho
    • 6
  • Fatima Maria de Souza Moreira
    • 6
  • Francisco Adriano de Souza
    • 7
  • Ricardo Luís Louro Berbara
    • 8
  • G. Wilson Fernandes
    • 1
    • 9
  1. 1.Ecologia Evolutiva and Biodiversidade/DBG, CP 486, ICBUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  2. 2.Departamento de Botânica e Zoologia, CBUniversidade Federal do Rio Grande do NorteNatalBrazil
  3. 3.PPG em Sistemática e Evolução, CBUniversidade Federal do Rio Grande do NorteNatalBrazil
  4. 4.Departamento de Microbiologia, ICBUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  5. 5.PPG em Ecologia, Conservação da Vida Silvestre, ICBUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  6. 6.Departamento de Ciência do SoloUniversidade Federal de LavrasLavrasBrazil
  7. 7.Núcleo de Biologia Aplicada, Embrapa Milho e SorgoSete LagoasBrazil
  8. 8.Departamento de Solos, Instituto de AgronomiaUniversidade Federal Rural Do Rio de JaneiroSeropédicaBrazil
  9. 9.Department of BiologyStanford UniversityStanfordUSA

Personalised recommendations