Abstract
In the terrestrial ecosystems, soil is an important component, characterized by holding high diversity of microorganisms which play a key role for productivity and vegetal composition. The group of symbionts microorganisms stands out for contributing directly to the growth and plant nutrition, and among them, the arbuscular mycorrhizal fungi form one of the oldest and well established associations. In order to increase the knowledge and contribute for further research with AMF and plants of Caatinga, in this review we compile data from previous studies on the effects of symbiosis between arbuscular mycorrhizal fungi (AMF) and plants of the Caatinga, a type of dry tropical forest found in the northeast of Brazil. These studies collected data under various experimental conditions, emphasizing fungal efficiency and host responsiveness in soils with varied fertility. From our analysis we conclude that in general the symbiotic efficiency on these plants depends on many factors, such as the plant-fungi combination, fertility and soil type. Furthermore, in leguminosae the impact of a joint inoculation with nitrogen fixing bacteria must be taken into account. Claroideoglomus etunicatum was the most tested AMF species benefiting almost all plants tested. Approximately 30 plant species were studied regarding possible benefits provided by AMF and of these only Hymenea courbaril and Aspidosperma pyrifolium did not respond to mycorrhization. Higher efficiency of the mycorrhizal symbiosis can be obtained in soils with low P levels, emphasizing the essential role of these microorganisms in the growth and survival of plant species from the Caatinga biome.
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References
Albuquerque UP, Medeiros PM, Almeida ALS, Monteiro JM, Neto EMDFL, Melo JG, Santos JP (2007) Medicinal plants of the caatinga (semi-arid) vegetation of NE Brazil: a quantitative approach. J Ethnopharmacol 114:325–354
Albuquerque UP, Araújo LE, El-Deir ACA et al (2012) Caatinga revisited: ecology and conservation of an important seasonal dry forest. Sci World J 205182:1–18
Araim G, Saleem A, Arnason JT, Charest C (2009) Root colonization by an arbuscular mycorrhizal (AM) fungus increases growth and secondary metabolism of purple coneflower, Echinacea purpurea (L.) Moench. J Agric Food Chem 57:2255–2258
Araújo RSL (2012) Fungo micorrízico arbuscular e biofertilizantes no crescimento e nutrição da sabiá (Mimosa cesalpiniaefolia Benth.). Dissertation, Federal University of Pernambuco
Bagyaraj DJ (2014) Mycorrhizal fungi. Proc Indian Natl Sci Acad 80:415–428
Bever JD (2002) Negative feedback within a mutualism: host–specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond B Biol Sci 269:2595–2601
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
Buainain AM, Garcia JR (2015) Polos de Irrigação no Nordeste do Brasil: desenvolvimento recente e perspectivas. Confins. Revue franco-brésilienne de géographie/Revista franco-brasilera de geografia: 23. http://confins.revues.org/10031. Acessed 5 Feb 2017
Burity HA, Lyra MCCP, Souza ED, Mergulhão ACES, Silva MLRB (2000) Efetividade da inoculação com rizóbio e fungos micorrízicos arbusculares em mudas de sabiá submetidas a diferentes níveis de fósforo. Pesq Agropec Bras 35:801–807
Carneiro MAC, Siqueira JO, Davide AC, Gomes LJ, Curi N, Vale FD (1996) Fungo micorrízico e superfosfato no crescimento de espécies arbóreas tropicais. Sci For 50:21–36
Carneiro MAC, Siqueira JO, Davide AC (2004) Fósforo e inoculação com fungos micorrízicos arbusculares no estabelecimento de mudas de embaúba (Cecropia pachystachya Trec). Pesq Agropec Trop 34:119–125
Carrenho R, Trufem SFB, Bononi VLR, Silva ES (2007) The effect of different soil properties on arbuscular mycorrhizal colonization of peanuts, sorghum and maize. Acta Bot Bras 21:723–730
Córdula E, Morim MP, Alves M (2014) Morfologia de frutos e sementes de Fabaceae ocorrentes em uma área prioritária para a conservação da Caatinga em Pernambuco, Brasil. Rodriguésia-Instituto de Pesquisas Jardim Botânico do Rio de Janeiro 65:505–516
Degáspari CH, Waszczynskyj N (2004) Propriedades antioxidantes de compostos fenólicos. Visão Acadêmica 5:33–40
Dias PC, Pereira MDSF, MegumiKasuya MC, Paiva HN, Oliveira LS, Xavier A (2012) Micorriza arbuscular e rizóbios no enraizamento e nutrição de mudas de angico-vermelho. Rev Árvore 36:1027–1037
Forzza RC, Costa A, Walter BMT, Pirani JR, Morim MP, Queiroz LP, Martinelli G, Peixoto AL, Coelho, MAN, Baumgratz JFA, Stehmann JR, Lohmann LG (2015) Angiospermas in Lista de Espécies da Flora do Brasil. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB128482. Acessed 16 Aug 2015
Gariglio MA, Sampaio EVDSB, Cestaro LA, Kageyama PY (2010) Uso sustentável e conservação dos recursos florestais da caatinga. Serviço Florestal Brasileiro-SFB, Brasília, 368pp
Gattai GS, Pereira SV, Costa C, Lima CE, Maia LC (2011) Microbial activity, arbuscular mycorrhizal fungi and inoculation of woody plants in lead contaminated soil. Braz J Microbiol 42:859–867
Giulietti AM, Bocage Neta AL, Castro AAJF, Gamarra-Rojas CFL, Sampaio EVSB, Virgínio JF, Queiroz LP, Figueiredo MA, Rodal MJN, Barbosa MRV, Harley RM (2004) Diagnóstico da vegetação nativa do bioma Caatinga. Biodiversidade da Caatinga: áreas e ações prioritárias para a conservação, pp 48–90
Goto BT, Silva GA, Yano-Melo AM, Maia LC (2010) Checklist of the arbuscular mycorrhizal fungi (Glomeromycota) in the Brazilian semiarid. Mycotaxon 113:251–154
Gross E, Cordeiro L, Caetano FH (2004) Nodulação e micorrização em Anadenanthera peregrina var. falcata em solo de cerrado autoclavado e não autoclavado. Rev Bras Ciênc Solo 28:95–101
Hacquard S, Schadt CW (2015) Towards a holistic understanding of the beneficial interactions across the Populus microbiome. New Phytol 205:1424–1430
Huang Z, Zou Z, He C, He Z, Zhang Z, Li J (2011) Physiological and photosynthetic responses of melon (Cucumis melo L.) seedlings to three Glomus species under water deficit. Plant Soil 339:391–399
INPE (2016) Centro do INPE avança no mapeamento da Caatinga. http://www.inpe.br/noticias/noticia.php?Cod_Noticia=4157. Acessed 03 May 2016
Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91
Khaosaad T, Vierheilig H, Nell M, Zitterl-Eglseer K, Novak J (2006) Arbuscular mycorrhiza alter the concentration of essential oils in oregano (Origanum sp., Lamiaceae). Mycorrhiza 16:443–446
Koziol L, Bever JD (2016) AMF, phylogeny, and succession: specificity of response to mycorrhizal fungi increases for late-successional plants. Ecosphere 7:1–11
Lacerda KAP, Silva MMDS, Carneiro MAC, Reis EFD, Saggin Júnior OJ (2011) Fungos micorrízicos arbusculares e adubação fosfatada no crescimento inicial de seis espécies arbóreas do cerrado. Cerne 17:377–386
Leite TS, Freitas RMO, Dombroski JLD, Leite MS, Rodrigues MRO (2014) Crescimento e partição da biomassa de mudas de mulungu sob adubação fosfatada e inoculação micorrízica. Pesquisa Florestal Brasileira 34:407–415
Lekberg Y, Rosendahl S, Olsson PA (2015) The fungal perspective of arbuscular mycorrhizal colonization in ‘nonmycorrhizal’ plants. New Phytol 205:1399–1403
Maia LC, Silva GA, Yano-Melo AM, Goto BT (2010) Fungos micorrízicos arbusculares no bioma Caatinga. In: Siqueira JO, Souza FA, Cardoso EJBN, Tsai SM (eds) Micorrizas: 30 anos de pesquisas no Brasil. Editora UFLA, Lavras, pp 311–339
Maia LC, Carvalho Júnior AA, Cavalcanti LH et al (2015) Diversity of Brazilian fungi. Rodriguésia 66:1033–1045
Marinho F, Silva GA, Ferreira AC, Veras JSN, Sousa NMF, Goto BT, Maia LC, Oehl F (2014) Bulbospora minima, a new genus and a new species in the Glomeromycetes from semi-arid Northeast Brazil. Sydowia 66:313–323
Martínez-García LB, Pugnaire FI (2011) Arbuscular mycorrhizal fungi host preference and site effects in two plant species in a semiarid environment. Appl Soil Ecol 48:313–317
Mello CMA, Silva IR, Pontes JS, Goto BT, Silva GA, Maia LC (2012) Diversidade de fungos micorrízicos arbusculares em área de Caatinga, PE, Brasil. Acta Bot Bras 26:938–943
Mendes MMC, Chaves LFC, Neto TPP, Silva JAA, Figueiredo MDVB (2013) Crescimento e sobrevivência de mudas de sabiá (Mimosa caesalpiniaefolia Benth.) inoculadas com micro-organismos simbiontes em condições de campo. Cienc Florest 23:309–320
Mergulhão ACES, Silva MLRB, Burity HA, Stamford NP (2001) Influência da dupla inoculação rizóbio e fungos micorrizas-arbusculares em plantas de sabiá sob solos de diferentes texturas. Ecossistema 26(1):42–47
Miranda JCC, Miranda LN (2001) Produção de mudas inoculadas com fungos micorrizicos arbusculares em viveiros. Brasília: Embrapa Cerrados. Recomendação Técnica. www.cpac.embrapa.br/baixar/790/t
MMA (2011) Monitoramento do desmatamento nos biomas brasileiros por satélite – Acordo de cooperação técnica MMA/IBAMA - Monitoramento do bioma caatinga 2008-2009. http://www.mma.gov.br/estruturas/sbf_chm_rbbio/_arquivos/relatorio_tecnico_caatinga_2008_2009_72.pdf. Acessed 02 Apr 2015
Nascimento JM, Moraes TA, Silva EM, Melo NF, Melo AM (2014) Crescimento de plantas de Bauhinia cheilanta micorrizadas em dois tipos de solo do bioma Caatinga. Revista Brasileira de Ciências Agrárias 9:570–576
Oehl F, Sieverding E, Palenzuela J, Ineichen K (2011) Advances in Glomeromycota taxonomy and classification. IMA fungus 2:191–199
Oliveira JJF, Alixandre TF (2013) Parâmetros biométricos de mudas de sabiá micorrizadas sob níveis de fósforo em Latossolo Amarelo. Pesquisa Florestal Brasileira 33:159–167
Oliveira MS, Campos MAS, Albuquerque UP, Silva FSB (2013) Arbuscular mycorrhizal fungi (AMF) affects biomolecules content in Myracrodruon urundeuva seedlings. Ind Crop Prod 50:244–247
Oliveira JRG, Teixeira-Rios T, Melo NFD, Yano-Melo AM (2015a) Response of an endangered tree species from Caatinga to mycorrhization and phosphorus fertilization. Acta Bot Bras 29:94–102
Oliveira PTF, Alves GD, Silva FA, Silva FSB (2015b) Foliar bioactive compounds in Amburana cearensis (Allemao) AC Smith seedlings: increase of biosynthesis using mycorrhizal technology. J Med Plant Res 9:712–718
Oliveira JRG, Resende GM, Melo NF, Yano-Melo AM (2017) Symbiotic compatibility between arbuscular mycorrhizal fungi (autoctone or exotic) and three native species of the Caatinga in different phosphorus levels. Acta Scientiarum Biological Sciences. https://doi.org/10.4025/actascibiolsci.v39i1.33486
Öpik M, Davison J (2016) Uniting species- and community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecol 24:106–113
Pagano MC, Cabello MN, Bellote AF, Sá NM, Scotti MR (2008) Intercropping system of tropical leguminous species and Eucalyptus camaldulensis, inoculated with rhizobia and/or mycorrhizal fungi in semiarid Brazil. Agrofor Syst 74:231–242
Pagano MC, Zandavalli RB, Araújo FS (2013) Biodiversity of arbuscular mycorrhizas in three vegetational types from the semiarid of Ceará State, Brazil. Appl Soil Ecol 67:37–46
Pasqualini D, Uhlmann A, Stürmer SL (2007) Arbuscular mycorrhizal fungal communities influence growth and phosphorus concentration of woody plants species from the Atlantic rain forest in South Brazil. For Ecol Manag 245:148–155
Patreze CM, Cordeiro L (2004) Nitrogen-fixing and vesicular–arbuscular mycorrhizal symbioses in some tropical legume trees of tribe Mimoseae. Forest Ecol Manag 196:275–285
Pedone-Bonfim MV, Lins MA, Coelho IR, Santana AS, Silva FS, Maia LC (2013) Mycorrhizal technology and phosphorus in the production of primary and secondary metabolites in cebil (Anadenanthera colubrina (Vell.) Brenan) seedlings. J Sci Food Agric 93:1479–1484
Pereira Filho JM, Bakke OA (2010) Produção de Forragem de espécies herbáceas da caatinga. In: Gariglio MA, Sampaio EVSB, Cestaro LA, Kageyama PY (eds) Uso sustentável e conservação dos recursos florestais da Caatinga. Serviço Florestal Brasileiro, Brasília, pp 145–159
Pereira CM, Goto BT, Silva DKA, Ferreira ACA, Souza FA, Silva GA, Maia LC, Oehl F (2015) Acaulospora reducta sp. nov. and A. excavata — two glomeromycotan fungi with pitted spores from Brazil. Mycotaxon 130:983–995
Pontes JSD, Sánchez-Castro I, Palenzuela J, Maia LC, Silva GAD, Oehl F (2013) Scutellospora alterata, a new gigasporalean species from the semi-arid Caatinga biome in northeastern Brazil. Mycotaxon 125:169–181
Pralon AZ, Martins MA (2001) Utilização do resíduo industrial ferkal na produção de mudas de Mimosa caesalpiniaefolia, em estéril de extração de argila, inoculadas com fungos micorrízicos arbusculares e rizóbio. Rev Bras Cienc Solo 25:55–63
Ratti N, Verma HN, Gautam SP (2010) Effect of Glomus species on physiology and biochemistry of Catharantus roseus. Indian J Microbiol 50:355–360
Rimington WR, Pressel S, Duckett JG, Bidartondo MI (2015) Fungal associations of basal vascular plants: reopening a closed book? New Phytol 205:1394–1398
Sampaio EVSB, Araújo MSB, Gamarra-Rojas CFL (2008) Espacialização do uso da vegetação nativa no semiárido nordestino. Rev Geogr 1:115–154
Santana AS (2010) Eficiência micorrízica em espécies de plantas medicinais da Caatinga em diferentes substratos. Dissertation, Federal University of Pernambuco
Santos DR, Costa MCS, Miranda JRP, Santos RV (2008) Micorriza e rizóbio no crescimento e nutrição em N e P de mudas de angico-vermelho. Rev Caatinga 21:76–82
Scotti MR, Corrêa EJA (2004) Growth and litter decomposition of woody species inoculated with rhizobia and arbuscular mycorrhizal fungi in Semiarid Brazil. Ann Forest Sci 61:87–95
Silva EM (2008) Condição micorrízica em espécies de Passiflora e efeito da simbiose na promoção do crescimento. Dissertation, Federal University of Pernambuco
Silva JL (2013) Crescimento de mudas de Myracrodruon urundeuva Allemão (Aroeira) e Anadenanthera colubrina (Vell.) Brenan (Angico-vermelho) submetidas a fertilização fosfatada e inoculação com fungo micorrízico arbuscular. Dissertation, Rural Federal University of Pernambuco
Silva FA, Silva FSB (2016) Is the application of arbuscular mycorrhizal fungi an alternative to increase foliar phenolic compounds in seedlings of Mimosa tenuiflora (Wild.) Poir., Mimosoideae? Braz J Bot. https://doi.org/10.1007/s40415-016-0320-9
Silva GA, Santos BA, Alves MV, Maia LC (2001) Arbuscular mycorrhiza in species of Commelinidae (Liliopsida) in the state of Pernambuco (Brazil). Acta Bot Bras 15:155–165
Silva MF, Pescador R, Rebelo RA, Stürmer SL (2008) The effect of arbuscular mycorrhizal fungal isolates on the development and oleoresin production of micropropagated Zingiber officinale. Braz J Plant Physiol 20:119–130
Silva FA, Ferreira MR, Soares LA, Sampaio EV, Maia LC (2014a) Arbuscular mycorrhizal fungi increase gallic acid production in leaves of field grown Libidibia ferrea (Mart. ex Tul.) LP Queiroz. J Med Plant Res 8:1110–1115
Silva IR, Mello CMA, Neto RAF, Silva DKA, Melo AL, Oehl F, Maia LC (2014b) Diversity of arbuscular mycorrhizal fungi along an environmental gradient in the Brazilian semiarid. Appl Soil Ecol 84:166–175
Silva DKA, Goto BT, Oehl F et al (2014c) Arbuscular mycorrhizal fungi: new records in northeast of Brazil. Boletim do Museu de Biologia Mello Leitão 36:35–50
Silva FA, Silva FAS, Maia LC (2014d) Biotechnical application of arbuscular mycorrhizal fungi used in the production of foliar biomolecules in ironwood seedlings [Libidibia ferrea (Mart. ex Tul.) LP Queiroz var. ferrea]. J Med Plant Res 8:814–819
Silva PCG, Moura MSB, Kiill LHP et al (2015a) Characterization of the Brazilian semi-arid region: natural and human factors. In: Sá IB, Silva PG (eds) Brazilian semi-arid: research, development and innovation, 1st edn. Embrapa Informação Tecnológica, Brasília, pp 17–54
Silva EM, Melo NF, Mendes AMS, Araújo FP, Maia LC, Yano-Melo AM (2015b) Response of Passiflora setacea to Mycorrhization and phosphate fertilization in a semiarid region of Brazil. J Plant Nutr 38:431–442
Siqueira JO, Saggin-Júnior OJ (2001) Dependency on arbuscular mycorrhizal fungi and responsiveness of some Brazilian native woody species. Mycorrhiza 11:245–255
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250
Smith SE, Smith FA (2012) Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia 104:1–13
Smith SE, Jakobsen I, Grolund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057
Sousa CDS, Menezes RSC, Sampaio EVDSB, Lima FDS, Oehl F, Maia LC (2013) Arbuscular mycorrhizal fungi within agroforestry and traditional land use systems in semi-arid Northeast Brazil. Acta Sci-Agron 35(3):307–314
Souza RG, Goto BT, Silva DKA, Silva FSB, Sampaio EV, Maia LC (2010) The role of arbuscular mycorrhizal fungi and cattle manure in the establishment of Tocoyena selloana Schum. in mined dune areas. Eur J Soil Biol 46:237–242
Spatafora JW, Chang Y, Benny GL et al (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046
Stamford NP, Ortega AD, Temprano F, Santos DR (1997) Effects of phosphorus fertilization and inoculation of Bradyrhizobium and mycorrhizal fungi on growth of Mimosa caesalpiniaefolia in an acid soil. Soil Biol Biochem 29:959–964
Sugai MAA, Collier LS, Saggin-Júnior OJ (2011) Inoculação micorrízica no crescimento de mudas de angico em solo de cerrado. Bragantia 70:416–423
Teixeira-Rios T, Souza RGD, Maia LC, Oehl F, Lima CEP (2013) Arbuscular mycorrhizal fungi in a semi-arid, limestone mining-impacted area of Brazil. Acta Bot Bras 27:688–693
Teixeira-Rios T, Oliveira JRG, Yano-Melo AM (2016) Arbuscular mycorrhizal fungi and phosphorus in the initial development of Mimosa tenuiflora (Willd.) Poir. Braz J Bot 39:997–1004
Torrecillas E, Alguacil MM, Roldán A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid Mediterranean prairies. Appl Environ Microbiol 78:6180–6186
Toussaint J-P, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297
Van der Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423
Vandresen J, Nishidate FR, Torezan JMD, Zangaro W (2007) Inoculação de fungos micorrízicos arbusculares e adubação na formação e pós-transplante de mudas de cinco espécies arbóreas nativas do sul do Brasil. Acta Bot Bras 21:753–765
Zangaro W, Nishidate FR, Camargo FRS, Romagnoli GG, Vandressen J (2005) Relationships among arbuscular mycorrhizas, root morphology and seedling growth of tropical native woody species in southern Brazil. J Trop Ecol 21:529–540
Zangaro W, Nishidate FR, Vandresen J, Andrade G, Nogueira MA (2007) Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil. J Trop Ecol 23:53–62
Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735
Acknowledgements
The authors acknowledge the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) by providing a PhD scholarship to M.V.L. Pedone-Bonfim and research grants provided to A.M. Yano-Melo (Proc. 0393-5.01/15) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for postdoctoral scholarship to D.K.A. Silva and research grants provided to L.C. Maia (Proc.446.144/2014-2, Proc. 307.129/2015-2).
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Pedone-Bonfim, M.V.L., da Silva, D.K.A., Maia, L.C. et al. Mycorrhizal benefits on native plants of the Caatinga, a Brazilian dry tropical forest. Symbiosis 74, 79–88 (2018). https://doi.org/10.1007/s13199-017-0510-7
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DOI: https://doi.org/10.1007/s13199-017-0510-7