Skip to main content

Advertisement

Log in

Fungal endophytes from cactus Cereus jamacaru in Brazilian tropical dry forest: a first study

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Endophytic fungi live within the healthy tissues of plants and can promote host species tolerance to different environmental stresses. However, most studies have been of plants in humid environments, and there are few reports of the benefits of such associations for plants of extreme environments. Our aims were to identify endophytic fungi using morphological taxonomy, to explore richness and estimate species frequency in a cactus, C. jamacaru, in Brazilian tropical dry forest (Caatinga). We thus identified 59 taxa, corresponding to 69.7 % of the total number of isolates; the other 30.3 % were sterile mycelia. Cladosporium cladosporioides and Fusarium oxysporum were the species most commonly isolated, followed by Acremonium implicatum, Aureobasidium pullulans, Trichoderma viride, Chrysonilia sitophila, and Aspergillus flavus. Forty-seven species are recorded for the first time as endophytic fungi of cacti, and 18 others as endophytes for Brazil; this suggests that C. jamacaru harbors a highly diverse fungal community as measured by a diversity index. However, species accumulation curves suggest that our study still underestimates endophyte diversity because it does not provide an exhaustive sample. To our knowledge, this is the first report of endophytic fungi from C. jamacaru in tropical dry forests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agra MF, Baracho GS, Basílio IJD, Nurit K, Coelho VP, Barbosa DA (2007) Sinopse da flora medicinal do cariri paraibano. Oecol Bras 11:323–330

    Article  Google Scholar 

  • Andrade CTS, Marques JGW, Zappi DC (2006) Utilização medicinal de cactáceas por sertanejos baianos. Rev Bras Pl Med 8:36–42

    Google Scholar 

  • Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecology 88(3):541–549

    Article  PubMed  Google Scholar 

  • Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274. doi:10.1046/j.1461-0248.2000.00159.x

    Article  Google Scholar 

  • Arnold AE, Maynard Z, Gilbert GS (2001) Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105(12):1502–1507

    Article  Google Scholar 

  • Azevedo JL, Araújo WL (2007) Diversity and applications of endophytic fungi isolated from tropical plants. In: Ganguli BN, Deshmukh SK (eds) Fungi: multifaceted microbes. CRC Press, Boca Raton, pp 189–207

    Google Scholar 

  • Azevedo JL, Maccheroni W Jr, Pereira JO, Araújo WL (2000) Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electron J Biotechnol 3(1):40–65

    Article  Google Scholar 

  • Barnett JA, Payne RW, Yarrow D (2000) Yeasts: characteristics and identification. Cambridge University Press, Cambridge

    Google Scholar 

  • Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247. doi:10.1007/s00572-003-0222-0

    Article  PubMed  CAS  Google Scholar 

  • Barrow JR, Lucero ME, Reyes-Vera I, Havstad KM (2008) Do symbiotic microbes have a role in plant evolution, performance and response to stress? Commun Integr Biol 1:69–73

    Article  PubMed  Google Scholar 

  • Bensch K, Braun U, Groenewald JZ, Crous PW (2012) The genus Cladosporium. Stud Mycol 72:1–401

    Article  PubMed  CAS  Google Scholar 

  • Bezerra JDP, Santos MGS, Svedese VM, Lima DMM, Fernandes MJS, Paiva LM, Souza-Motta CM (2012a) Richness of endophytic fungi isolated from Opuntia ficus-indica Mill. (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 28:1989–1995. doi:10.1007/s11274-011-1001-2

    Article  PubMed  CAS  Google Scholar 

  • Bezerra JDP, Lopes DHG, Santos MGS, Svedese VM, Paiva LM, Almeida-Cortez JS, Souza-Motta CM (2012b) Riqueza de micro-organismos endofíticos em espécies da família Cactaceae. Bol Soc Latin Carib Cact Suc 9(2):19–23

    Google Scholar 

  • Cavalcanti NB, Resende GM (2007) Efeito de Diferentes Substratos no Desenvolvimento de Mandacaru (Cereus jamacaru P. DC.), Facheiro (Pilosocereus pachycladus RITTER), Xiquexique (Pilosocereus gounellei (A. WEBWR EX K. SCHUM.) BLY. EX ROWL.) e Coroa-de-Frade (Melocactus bahiensis BRITTON & ROSE). Rev Caatinga 20(1):28–35

    Google Scholar 

  • Ceccon E, Huante P, Rincón E (2006) Abiotic factors influencing tropical dry forests regeneration. Braz Arch Biol Technol 49(2):305–312

    Article  Google Scholar 

  • Chandra S (2012) Endophytic fungi: novel sources of anticancer lead molecules. Appl Microbiol Biotechnol 95:47–59

    Article  PubMed  CAS  Google Scholar 

  • Clarke KR, Gorley RN (2006) Primer v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Costa IPMW, Assunção MMC, Lima TEF, Oliveira RJV, Cavalcanti MAQ (2012a) Checklist of endophytic fungi from tropical regions. Mycotaxon 119:494, http://www.mycotaxon.com/resources/checklists/costa_v119_checklist.pdf. Acessed 11 August 2012

    Google Scholar 

  • Costa IPMW, Maia LC, Cavalcanti MA (2012b) Diversity of leaf endophytic fungi in mangrove plants of Northeast Brazil. Braz J Microbiol 43(3):1165–1173. doi:10.1590/S1517-83822012000300044

    Article  Google Scholar 

  • Domsch KH, Gams W, Anderson TH (2007) Compendium of soil fungi. IHW-Verlag, Eching

    Google Scholar 

  • Ellis MB (1971) Dematiaceus hyphomycetes. Commonwealth Mycological Institute, Kew

    Google Scholar 

  • Embrapa (1997) Manual de métodos de análises do solo. Ministério da Agricultura e do Abastecimento, Rio de Janeiro

  • Fisher PJ, Sutton BC, Petrini LE, Petrini O (1994a) Fungal endophytes from Opuntia stricta: a first report. Nova Hedwigia 59:195–200

    Google Scholar 

  • Fisher PJ, Petrini O, Petrini LE, Sutton BC (1994b) Fungal endophytes from the leaves and twigs of Quercus ilex L. from England, Majorca an Switzerland. New Phytol 127:133–137. doi:10.1111/j.1469-8137.1994.tb04267.x

    Article  Google Scholar 

  • Girlanda M, Ghignone S, Luppi AM (2002) Diversity of sterile root-associated fungi of two Mediterranean plants. New Phytol 155:481–498

    Article  Google Scholar 

  • Guo LD, Hyde KD, Liew ECY (2000) Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytol 147:617–630

    Article  CAS  Google Scholar 

  • Hoog GS, Guarro J, Gené J, Figueras MJ (2000) Atlas of clinical fungi. Centraalbureau voor Schimmelcultures, Utrecht, The Netherlands

    Google Scholar 

  • Houbraken J, Frisvad JC, Samson RA (2011) Taxonomy of Penicillium section Citrina. Stud Mycol 70:53–138. doi:10.3114/sim.2011.70.02

    Article  PubMed  CAS  Google Scholar 

  • Kharwar RN, Verma VC, Strobel G, Ezra D (2008) The endophytic fungal complex of Catharanthus roseus (L.) G. Don. Curr Sci 95:228–233

    CAS  Google Scholar 

  • Khidir HH, Eudy DM, Porras-Alfaro A, Herrera J, Natvig DO, Sinsabaugh RL (2010) A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland. J Arid Environ 74:35–42. doi:10.1016/j.jaridenv.2009.07.014

    Article  Google Scholar 

  • Köppen W (1948) Climatologia: con un estudio de los climas de la tierra. Fondo de Cultura Econômica, México

    Google Scholar 

  • Kreger-Van Rij NJW (1984) The yeast–a taxonomic study. Elsevier Science, Amsterdam

    Google Scholar 

  • Kumaresan V, Suryanaraynan TS (2001) Occurrence and distribution of endophytic fungi in a mangrove community. Mycol Res 11(105):1388–1391

    Article  Google Scholar 

  • Kurtzman CP, Fell JW (1998) The yeasts, a taxonomic study. Elsevier Science, Amsterdam

    Google Scholar 

  • Kusari P, Kusari S, Spiteller M, Kayser O (2012) Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Divers. doi:10.1007/s13225-012-0216-3

  • Larran S, Perelló A, Simón MR, Moreno V (2002) Isolation and analysis of endophytic microorganisms in weat (Triticum aestivum L.) leaves. World J Microbiol Biotechnol 18:683–686

    Article  CAS  Google Scholar 

  • Leslie J, Summerell BA (2006) The Fusarium laboratory manual. Blackwell Publishing, Iowa

    Google Scholar 

  • Lima TEF, Oliveira RJV, Neves RP, Bezerra JL, Cavalcanti MAQ (2013) Endophytic yeast of Coffea Arabica and Vitis labrusca cv. Isabel from Pernambuco, Brazil. Nova Hedwigia 96

  • Linares-Palomino R (2006) Phytogeography and floristics of seasonally dry tropical forests in Peru. In: Pennington RT, Lewis GP, Ratter JA (eds) Neotropical savannas and dry forests: plant diversity, biogeography, and conservation. Taylor & Francis CRC Press, Oxford UK, pp 249–271

    Google Scholar 

  • Linnakoski R, Puhakka-Tarvainen H, Pappinen A (2012) Endophytic fungi isolated from Khaya anthotheca in Ghana. Fungal Ecol 5:298–308. doi:10.1016/j.funeco.2011.08.006

    Google Scholar 

  • Lodder J (1970) The yeast–a taxonomic study. North Holland Publishing Company, Amsterdam

    Google Scholar 

  • Lopez BR, Bashan Y, Bacilio M (2011) Endophytic bacteria of Mammillaria fraileana, an endemic rock-colonizing cactus of the southern Sonoran Desert. Arch Microbiol 193:527–541. doi:10.1007/s00203-011-0695-8

    Article  PubMed  CAS  Google Scholar 

  • Lopez BR, Tinoco-Ojanguren C, Bacilio M, Mendoza A, Bashan Y (2012) Endophytic bacteria of the rock-dwelling cactus Mammillaria fraileana affect plant growth and mobilization of elements from rocks. Environ Exp Bot 81:26–36. doi:10.1016/j.envexpbot.2012.02.014

    Article  CAS  Google Scholar 

  • Loro M, Valero-Jiménez CA, Nozawac S, Márquez LM (2012) Diversity and composition of fungal endophytes in semiarid Northwest Venezuela. J Arid Environ 85:46–55. doi:10.1016/j.jaridenv.2012.04.009

    Article  Google Scholar 

  • Magan N (2007) Fungi in extreme environments. In: Kubicek CP, Druzhinina IS (eds) Environmental and microbial relationships: The Micota IV, 2nd edn. Springer, Berlin Heidelberg, pp 85–103

  • Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected coolseason grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940

    Article  CAS  Google Scholar 

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189

    Article  Google Scholar 

  • Morsy MR, Oswald J, He J, Tang Y, Roossinck MJ (2010) Teasing apart a three-way symbiosis: transcriptome analyses of Curvularia protuberata in response to viral infection and heat stress. Biochem Biophys Res Commun 401:225–230. doi:10.1016/j.bbrc.2010.09.034

    Article  PubMed  CAS  Google Scholar 

  • Murali TS, Suryanarayanan TS, Venkatesan G (2007) Fungal endophytes communities in two tropical forest of southern India: diversity and host affiliation. Mycol Prog 6:191–199

    Article  Google Scholar 

  • Murphy PG, Lugo AE (1986) Ecology of tropical dry forest. Annu Rev Ecol Syst 17:67–88

    Article  Google Scholar 

  • Newsham KK (2012) Fungi in extreme environments. Fungal Ecol 5:379–380. doi:10.1016/j.funeco.2012.04.003

    Article  Google Scholar 

  • Oldfield S (comp) (1997) Cactus and succulent plants–status survey and conservation action plant. IUCN/SSC Cactus and Succulent Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp 212

  • Posada F, Aime M, Peterson SW, Rehner SA, Vega F (2007) Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycol Res 111:748–757

    Article  PubMed  CAS  Google Scholar 

  • Postma J, Rattink H (1992) Biological control of Fusarium wilt of carnation with a non-pathogenic isolate of Fusarium oxysporum. Can J Bot 70:1199–1205

    Article  Google Scholar 

  • Puente ME, Bashan Y, Li CY, Lebsky VK (2004a) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. I. Root colonization and weathering of igneous rocks. Plant Biol 6:629–642

    Article  PubMed  CAS  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2004b) Microbial populations and activities in the rhizoplane of rock-weathering desert plants. II. Growth promotion of cactus seedlings. Plant Biol 6:643–649

    Article  PubMed  CAS  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2009a) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401

    Article  CAS  Google Scholar 

  • Puente ME, Li CY, Bashan Y (2009b) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408

    Article  CAS  Google Scholar 

  • Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JN (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581

    Article  PubMed  CAS  Google Scholar 

  • Rêgo MM, Araújo ER, Rêgo ER, Castro JP (2009) In vitro seed germination of mandacaru (Cereus jamacaru DC.). Rev Caatinga 22(4):34–38

    Google Scholar 

  • Rodrigues KF, Petrini O (1997) Biodiversity of endophytic fungi in tropical regions. In: Biodiversity of tropical microfungi. Hong Kong University Press, Hong Kong, pp 57–69

  • Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9(6):275–280

    Article  PubMed  CAS  Google Scholar 

  • Samson RA, Frisvad JC (2004) Penicillium subgenus Penicillium: new taxonomics schemes, mycotoxins and other extrolites. Stud Mycol 49:1–260

    Google Scholar 

  • Sánchez-Azofeifa GA, Quesada M, Rodriguez JP, Nassar JM, Stoner KE, Castillo A, Garvin T, Zent EL, Calvo-Alvarado JC, Kalacska MER, Fajardo L, Gamon JA, Cuevas-Reyes P (2005) Research priorities for neotropical dry forests. Biotropica 37(4):477–485

    Google Scholar 

  • Santos RM, Oliveira-Filho AT, Eisenlohr PV, Queiroz LP, Cardoso DBOS, Rodal MJN (2012) Identity and relationships of the Arboreal Caatinga among other floristic units of seasonally dry tropical forests (SDTFs) of north-eastern and Central Brazil. Ecol Evol 2(2):409–428

    Article  PubMed  Google Scholar 

  • Siqueira Filho JA et al (2012) Flora das Caatingas do Rio São Francisco. In: Siqueira Filho JA (org) A Flora das Caatingas do Rio São Francisco: história natural e conservação. Andrea Jakobsson Estúdio Editorial, Rio de Janeiro, pp 446–542

  • Siqueira VM, Conti R, Araújo JM, Souza-Motta CM (2011) Endophytic fungi from the medicinal plant Lippia sidoides Cham. and their antimicrobial activity. Symbiosis 53:89–95

    Article  CAS  Google Scholar 

  • Souza AEF, Nascimento LC, Araújo E, Lopes EB, Souto FM (2010) Ocorrência e identificação dos agentes etiológicos de doenças em palma forrageira (Opuntia ficus-indica Mill.) no semiárido paraibano. Biotemas 23(3):11–20

    Google Scholar 

  • Stone JK, Polishook JD, White JF (2004) Endophytic fungi. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi. Inventory and monitoring methods. Elsevier Academic Press, San Diego, pp 241–270

    Chapter  Google Scholar 

  • Strobel GA, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67(4):491–502

    Article  PubMed  CAS  Google Scholar 

  • Summerbell RC (2005) Root endophyte and mycorrhizosphere fungi of black spruce, Picea mariana, in a boreal forest habitat: influence of site factors on fungal distributions. Stud Mycol 53:121–145

    Article  Google Scholar 

  • Sun Y, Wang Q, Lu X, Okane I, Kakishima M (2012) Endophytic fungal community in stems and leaves of plants from desert areas in China. Mycol Prog 11:781–790

    Article  Google Scholar 

  • Suryanarayanan TS, Kumaresan V, Johnson JA (1998) Foliar fungal endophytes from two species of the mangrove Rhizophora. Can J Microbiol 44:1003–1006

    CAS  Google Scholar 

  • Suryanarayanan TS, Murali TS, Venkatesan G (2002a) Occurrence and distribution of fungal endophytes in tropical forest across a rainfall gradient. Can J Bot 80:818–826

    Article  Google Scholar 

  • Suryanarayanan TS, Venkatesan G, Murali TS (2002b) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr Sci 85:489–494

    Google Scholar 

  • Suryanarayanan TS, Venkatesan G, Murali TS (2003) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr Sci 85:489–493

    Google Scholar 

  • Suryanarayanan TS, Wittlinger SK, Faeth SH (2005) Endophytic fungi associated with cacti in Arizona. Mycol Res 109:635–639

    Article  PubMed  Google Scholar 

  • Suryanarayanan TS, Murali TS, Thirunavukkarasu N, Rajulu MBG, Venkatesan G, Sukumar R (2011) Endophytic fungal communities in woody perennials of three tropical forest types of the Western Ghats, southern India. Biodivers Conserv 20:913–928

    Article  Google Scholar 

  • Suryanaraynan TS, Kumaresan V (2000) Endophytic fungi of some halophytes from an estuarine mangrove forest. Mycol Res 12(104):1465–1567

    Article  Google Scholar 

  • Sutton BC (1980) The Coelomycetes: fungi imperfecti with pycnidia, acervuli and stromata. Commonwealth Mycological Institute, Kew

    Google Scholar 

  • Tadych M, Bergen MS, Johnson-Cicalese J, Polashock JJ, Vorsa N, White JF Jr (2012) Endophytic and pathogenic fungi of developing cranberry ovaries from flower to mature fruit: diversity and succession. Fungal Divers 54:101–116

    Article  Google Scholar 

  • Tan RX, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459

    Article  PubMed  CAS  Google Scholar 

  • Taylor NP, Zappi DC (2004) Cacti of Eastern Brazil. Royal Botanic Gardens, Kew, Kew

    Google Scholar 

  • Unterseher M, Reiher A, Finstermeier K, Otto P, Morawetz W (2007) Species richness and distribution patterns of leaf-inhabiting endophytic fungi in a temperate forest canopy. Mycol Prog 6:201–212

    Article  Google Scholar 

  • Vieira PDS, Souza-Motta CM, Lima D, Torres JB, Quecine MC, Azevedo JL, Oliveira NT (2011) Endophytic fungi associated with transgenic and non-transgenic cotton. Mycology 2(2):91–97

    Google Scholar 

  • Vieira MLA, Hughes AFS, Gil VB, Vaz ABM, Alves TMA, Zani CL, Rosa CA, Rosa LH (2012) Diversity and antimicrobial activities of the fungal endophyte community associated with the traditional Brazilian medicinal plant Solanum cernuum Vell. (Solanaceae). Can J Microbiol 58:54–66

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Guo LD, Hyde KD (2005) Taxonomic placement of sterile morphotypes of endophytic fungi from Pinus tabulaeformis (Pinaceae) in northeast China based on rDNA sequences. Fungal Divers 20:235–260

    CAS  Google Scholar 

  • Wang Q-X, Li S-F, Zhao F, Dai H-Q, Bao L, Ding R, Gao H, Zhang L-X, Wen H-A, Liu H-W (2011) Chemical constituents from endophytic fungus Fusarium oxysporum. Fitoterapia 82:777–781

    Article  PubMed  CAS  Google Scholar 

  • Xing X, Guo S, Fu J (2010) Biodiversity and distribution of endophytic fungi associated with Panax quinquefolium L. cultivated in a forest reserve. Symbiosis 51:161–166

    Article  Google Scholar 

  • Yuan ZL, Zhang CL, Lin FC, Kubicek CP (2010) Identity, diversity, and molecular phylogeny of the endophytic mycobiota in the roots of rare wild rice (Oryza granulate) from a nature reserve in Yunnan, China. Appl Environ Microbiol 76:1642–1652. doi:10.1128/AEM.01911-09

    Article  PubMed  CAS  Google Scholar 

  • Zappi DC, Taylor NP, Machado MC (2010) Cactaceae. In: Forzza RC et al (eds) Catálogo de Plantas e Fungos do Brasil, Jardim Botânico do Rio de Janeiro, 1:822–832

Download references

Acknowledgments

We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Financiadora de Estudos e Projetos (FINEP-01.08.0392.00), Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG, CRA-APQ 00001–11), Fundação de Amparo a Ciência e Tecnologia de Pernambuco (FACEPE APQ-0290-2.12/10), Sistema Nacional de Pesquisa em Biodiversidade – SISBIOTA Brasil (Process 563304/2010-3) of Brazil for financial support of this project. We extend our thanks to the Instituto Fazenda Tamanduá (Tamanduá Farm), Danielle Karla Silva (MSc.), Dra. Neiva Tinti de Oliveira, Dr. João Lúcio de Azevedo, and two anonymous reviewers for suggestions regarding the manuscript. We also thank the students of the Laboratório de Citologia e Genética de Fungos/UFPE for their technical help and processing of samples.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jadson D. P. Bezerra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bezerra, J.D.P., Santos, M.G.S., Barbosa, R.N. et al. Fungal endophytes from cactus Cereus jamacaru in Brazilian tropical dry forest: a first study. Symbiosis 60, 53–63 (2013). https://doi.org/10.1007/s13199-013-0243-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-013-0243-1

Keywords

Navigation