Potencial Simbiótico de Microrganismos do Solo na Promoção do Crescimento de Espécies Arbóreas da Mata Atlântica

Autores/as

DOI:

https://doi.org/10.21664/2238-8869.2024v13i1.p105-129

Palabras clave:

ecological restoration, topsoil, root symbionts, nitrogen-fixing bacteria, arbuscular mycorrhizal fungi

Resumen

The objective of this study was to evaluate the potential of topsoil obtained from a natural forest fragment in the Brazilian Atlantic Forest to serve as a source of symbiotic microorganisms capable of promoting the growth of native tree species in ecological restoration projects. In greenhouse conditions, 14 experiments in a completely randomized design were conducted in 1,700 cm³ pots filled with sterilized substrate. The effect of adding 80 g of topsoil, either in natura or sterilized, to the substrate was tested on the growth of 14 tree species. Plant height, stem diameter, mycorrhizal colonization and dry masses of shoot, roots, and nodules of tree species were measured. Applying the topsoil to the pots generally resulted in significant increases in height and stem diameter of seedlings compared to the control group during the four to six-month evaluation period. This effect was particularly greater in the nodulating species Plathymenia reticulata, Dalbergia nigra and Mimosa bimucronata, with increases in height and stem diameter of up to 328% and 484%, respectively. Forest topsoil also had a positive impact on the growth of shoot, roots, and nodules of the plants, significantly differing from the control groups. Only the plants that received the topsoil in natura exhibited mycorrhizal colonization and the formation of nodules in nitrogen-fixing species. These plants that established mycorrhizas and nodules presented higher concentrations of phosphorous and nitrogen in their biomass, respectively. Under controlled conditions, the use of forest topsoil proved to be a promising strategy for the introduction of microorganisms that can enhance the growth of tree species, thereby holding potential for implementation in nurseries and field settings.

 

 

Citas

Afkhami ME, Almeida BK, Hernandez DJ, Kiesewetter KN, Revillini DP 2020. Tripartite mutualisms as models for understanding plant–microbial interactions. Curr Opin Plant Biol 56:28-36. https://doi.org/10.1016/j.pbi.2020.02.003

Alvares AC, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G 2013. Koppen’s climate classification map for Brazil. Meteorol Z 22(6):711-728. http://dx.doi.org/10.1127/0941-2948/2013/0507

Arnhold E 2022. Easyanova: Analysis of Variance and Other Important Complementary Analyses. Version 4.0.0, https://cran.r-project.org/web/packages/easyanova/easyanova

Averill C, Anthony MA, Baldrian P, Finkbeiner F, Van den Hoogen J, Kiers T, Kohout P, Hirt E, Smith GR, Crowther TW 2022. Defending Earth’s terrestrial microbiome. Nat Microbiol 7(11):1717-1725. http://dx.doi.org/10.1038/s41564-022-01228-3

Barros JA, Medeiros EV, Costa DP, Duda GP, Lima JRS, Santos UJ, Antonino ACD, Hammecker, C 2019. Human disturbance affects enzyme activity, microbial biomass and organic carbon in tropical dry sub-humid pasture and forest soils. Arch Agron Soil Sci 66:458-472. https://doi.org/10.1080/03650340.2019.1622095

Berkelmann D, Schneider D, Meryandini A, Daniel R 2020. Unravelling the effects of tropical land use conversion on the soil microbiome. Environmental Microbiome 15(5). https://doi.org/10.1186/s40793-020-0353-3

Borges WL, Prin Y, Ducousso M, Le Roux C, Faria SM 2016. Rhizobial characterization in revegetated areas after bauxite mining. Braz J Microbiol 47(2):314-321. https://doi.org/10.1016/j.bjm.2016.01.009

Bournaud C, James EK, Faria, SM, Lebrun M, Melkonian R, Duponnois R, Tisseyre P, Moulin L, Prin Y 2018. Interdependency of efficient nodulation and arbuscular mycorrhization in Piptadenia gonoacantha, a Brazilian legume tree. Plant Cell Environ 41(9). https://doi.org/10.1111/pce.13095

Brancalion, PHS, Meli P, Tymus JRC, Lenti FEB, Benini RM, Silva APM, Isernhagen I, Holl KD 2019 What makes ecosystem restoration expensive? A systematic cost assessment of projects in Brazil. Biol Conserv 240:108274. https://doi.org/10.1016/j.biocon.2019.108274

Busby PE, Newcombe G, Neat AS, Averill C 2022. Facilitating reforestation through the plant microbiome: Perspectives from the phyllosphere. Annu. Rev. Phytopathol. 60:337-356. https://doi.org/10.1146/annurev-phyto-021320-010717

Carneiro MAC, Siqueira JO, Moreira FMS, Carvalho D, Botelho SA, Saggin Júnior, OJ 1998. Micorriza arbuscular em espécies arbóreas e arbustivas nativas de ocorrência no sudoeste do Brasil. Cerne 4(1):129-145

Carvalho NM, Nakagawa J 2000. Sementes: Ciência, tecnologia e produção. Funep, Jaboticabal

Castro DS, Amaro HTR, Araujo EF, Borges EEL, Martins Filho S 2019. Superação de dormência em sementes de garapa ((Apuleia leiocarpa (VOGEL)) JF MACBR. Colloq Agrariae 15(4):51-59. https://doi.org/10.5747/ca.2019.v15.n4.a311

Cipriani VB, Garlet J, Lima BM 2019. Quebra de dormência em sementes de Chloroleucon acacioides e Senna macranthera. Revista de Ciências Agrárias 42(1):49-54. https://doi.org/10.19084/RCA18238

Dwivedi SL, Sahrawat KL, Upadhyaya HD, Mengoni A, Galardini M, Bazzicalupo M, Biondi EG, Hungria M, Kaschuk G, Blair MW, Ortiz R 2015. Advances in host plant and rhizobium genomics to enhance symbiotic nitrogen fixation in grain legumes. Adv Agron 129:1-116. https://doi.org/10.1016/bs.agron.2014.09.001

Ferguson M, Ihrie J. Cran.r-project.org [homepage on the Internet]. MPN: Most Probable Number and Other Microbial Enumeration Techniques; 2019 [updated 2022 Oct 12; cited 2022 Nov 19]. Available from: https://cran.r-project.org/web/packages/MPN.

Fierer N 2017. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Rev Microbiol 15(10):579-590. https://doi.org/10.1038/nrmicro.2017.87

Freire JM, Faria SMD, Zilli JE, Saggin Júnior OJ, Camargo IS, Rouws JRC, Jesus EC 2020. Symbiotic efficiency of inoculation with nitrogen-fixing bacteria and arbuscular mycorrhizal fungi in Tachigali vulgaris seedlings. Rev Árvore 44. https://doi.org/10.1590/1806-908820200000024

Gerdermann JN, Nicolson TH 1963. Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46(2):235-244. https://doi.org/10.1016/S0007-1536(63)80079-0

Giovannetti M, Mosse B 1980. An evaluation of techniques to measure vesicular-arbuscular mycorrhizal infection in roots. New Phytol 84(3):484-500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x

Gossner MM, Lewinsohn TM, Kahl T, Grassein F, Boch S, Prati D, Birkhofer K, Renner SC, Sikorski J, Wubet T, Arndt H, Baumgartner V, Blaser S, Blüthgen N, Börschig C, Buscot F, Diekötter T, Jorge LR, Jung K, Keyel AC, Klein AM, Klemmer S, Krauss J, Lange M, Müller J, Overmann J, Pašalić E, Penone C, Perović DJ, Purschke O, Schall P, Socher SA, Sonnemann I, Tschapka M, Tscharntke T, Türke M, Venter PC, Weiner CN, Werner M, Wolter V, Wurst S, Westphal C, Fischer M, Weisser WW, Allan E 2016. Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540(7632):266-269. https://doi.org/10.1038/nature20575

Grace C, Stribley DP 1991. A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol. Res.95:11160-1162. https://doi.org/10.1016/S0953-7562(09)80005-1

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 Cienc Solo 28:95-101. https://doi.org/10.1590/S0100-06832004000100010

Guzmán I, Döbereiner J 1968. Effectiveness and efficiency in the symbiosis of your cross inoculated tropical legumes. In: Anais da 4º Reunião Latino Americana sobre inoculantes para leguminosas, Universidade Federal do Rio Grande do Sul, Porto Alegre 81-91.

Instituto Brasileiro de Geografia e Estatística – IBGE 2012. Manual técnico da vegetação brasileira, 2nd ed. IBGE, Rio de Janeiro (Manuais Técnicos em Geociências, 1)

Instituto Nacional de Meteorologia - INMET 2021. Dados históricos anuais. bdmep.inmet.gov.br Accessed 25 March 2021

Ivanova EA, Pershinaa EV, Kutovayab OV, Sergalieva NK, Nagievad AG, Zhiengalievd AT, Provorova N A, Andronova EE 2018. Comparative analysis of microbial communities of contrasting soil types in different plant communities. Russ J Ecol 49(1):30-39. https://doi.org/10.1134/S106741361801006X

Jakovac CC, Junqueira AB, Crouzeilles R, Peña‐Claros M, Mesquita RC, Bongers F 2021. The role of land‐use history in driving successional pathways and its implications for the restoration of tropical forests. Biol Rev 96(4):1114-1134. https://doi.org/10.1111/brv.12694

Jarvis B, Wilrich C, Wilrich PT 2010. Reconsideration of the derivation of Most Probable Numbers, their standard deviations, confidence bounds and rarity values. J Appl Microbiol 109(5):1660-1667. https://doi.org/10.1111/j.1365-2672.2010.04792.x

Jenkins WR 1964. A rapid centrifugal-flotation technique for separating nematodes from soil. Plant Dis Rep 48:692.

Kestring D, Klein J, de Menezes LCCR, Rossi MN 2009. Imbibition phases and germination response of Mimosa bimucronata (Fabaceae: Mimosoideae) to water submersion. Aquatic Botany 91(2):105-109. https://doi.org/10.1016/j.aquabot.2009.03.004

Koske RE, Gemma JN 1989. A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92(4):486-488. https://doi.org/10.1016/S0953-7562(89)80195-9

Koziol L, Schultz PA, House GL, Bauer JT, Middleton EL, Bever JD 2018. The plant microbiome and native plant restoration: the example of native mycorrhizal fungi. BioScience 68(12):996-1006. https://doi.org/10.1093/biosci/biy125

Koziol L, Bauer JT, Duell EB, Hickman K, House GL, Schultz PA, Tipton AG, Wilson GWT, Bever JD 2022. Manipulating plant microbiomes in the field: Native mycorrhizae advance plant succession and improve native plant restoration. J Appl Ecol 59:1976-1985. https://doi.org/10.1111/1365-2664.14036

Lima KDRD, Correia MEF, Campello EFC, Resende AS 2021. Regeneração natural após 13 anos de plantio com espécies arbóreas fixadoras de nitrogênio em Valença, no estado do Rio de Janeiro. Ciênc Florest 31:830-845. https://doi.org/10.5902/1980509844460

Lobo CB, Tomás MSJ, Viruel E, Ferrero MA, Lucca ME 2019. Development of low-cost formulations of plant growth-promoting bacteria to be used as inoculants in beneficial agricultural technologies. Microbiological research 219:12-25. https://doi.org/10.1016/j.micres.2018.10.012

Machado RL, Resende AS, Pitard R, Faria SM 2004. Obtenção e seleção de estirpes de rizóbio para leguminosas florestais com potencial de uso em áreas degradadas. Embrapa Agrobiologia, Seropédica

Martins EM, Silva ERD, Campello EFC, Lima SSD, Nobre CP, Correia MEF, Resende AS 2019. O uso de sistemas agroflorestais diversificados na restauração florestal na Mata Atlântica. Ciênc Florest 29:632-648. https://doi.org/10.5902/1980509829050

McMahen K, Lavkulich LM, Grayston SJ, Simard SW 2022. Small-volume additions of forest topsoil improve root symbiont colonization and seedling growth in mine reclamation. Appl Soil Ecol 180:104622, 2022. https://doi.org/10.1016/j.apsoil.2022.104622

Nasto MK, Alvarez‐Clare S, Lekberg Y, Sullivan BW, Townsend AR, Cleveland CC 2014. Interactions among nitrogen fixation and soil phosphorus acquisition strategies in lowland tropical rain forests. Ecol Lett 17(10):1282-1289. https://doi.org/10.1111/ele.12335

Nogueira ARA, Souza GB 2005. Manual de laboratórios: solo, água, nutrição vegetal, nutrição animal e alimentos. Embrapa Pecuária Sudeste, São Carlos

Novais CB, Sbrana C, Jesus EC, Rouws LFM, Giovannetti M, Avio L, Siqueira JO, Saggin Júnior OJ, Silva EMR, Faria SM 2020. Mycorrhizal networks facilitate the colonization of legume roots by a symbiotic nitrogen-fixing bacterium. Mycorrhiza 30:389-396. https://doi.org/10.1007/s00572-020-00948-w

Oliveira Júnior JQ, Jesus EC, Lisboa FJ, Berbara RLL, Faria SM 2017. Nitrogen-fixing bacteria and arbuscular mycorrhizal fungi in Piptadenia gonoacantha (Mart.) Macbr. Braz J Microbiol 48(1):95-100. https://doi.org/10.1016/j.bjm.2016.10.013

Paiva Sobrinho SD, Siqueira AG, Morais PDB, Silva SJD 2012. Superação da dormência em sementes de mutamba (Guazuma ulmifolia Lam. -Sterculiaceae). Rev Árvore 36(5):797-802. https://doi.org/10.1590/S0100-67622012000500001

Pedone-Bonfim MVL, Silva DKA, Maia LC 2018. Mycorrhizal benefits on native plants of the Caatinga, a Brazilian dry tropical forest. Symbiosis 74:79-88. https://doi.org/10.1007/s13199-017-0510-7

Piveta G, Menezes VO, Pedroso DC, Muniz MFB, Blume E, Wielewicki AP 2010. Superação de dormência na qualidade de sementes e mudas: influência na produção de Senna multijuga (LC Rich.) Irwin & Barneby. Acta Amaz 40(2):281-288. https://doi.org/10.1590/S0044-59672010000200006

Rahman MH, Khatun S, Ali SR, Yasmin S, Kamruzzaman M, Rashid MH 2018. Morpho-physiological diversity of root nodule rhizobia from Mimosa (Mimosa pudica L.) and water Mimosa (Neptunia oleracea L.). J Bacteriol Mycol 5(1):1061, 2018

Redford KH 2023. Extending conservation to include Earth's microbiome. Conserv Biol e14088. https://doi.org/10.1111/cobi.14088

Santos RS, Scoriza RN, Silva EMR, Saggin Júnior OJS 2016. Selection of mycorrhizal fungi for the initial growth of Albizia polycephala. Rev Bras Cienc Agrar 11(2):98-103. https://doi.org/10.5039/agraria.v11i2a5362

Schenck NC, Perez Y 1988. A manual for identification of vesicular-arbuscular mycorrhizal fungi, 2nd ed. University of Florida, Gainesville

Silva CF, Pereira MG, Santos VL, Miguel DL, Silva EMR 2016. Arbuscular mycorrhizal fungi: Composition, length extraradical mycelium and glomalin in areas of Atlantic Forest, Rio de Janeiro. Cienc Florest 26(2):419-433. https://doi.org/10.5902/1980509822743

Silva MM, Ataíde GM, Ribeiro LP, Catarina A, Cunha MC, Silva LBJ 2013. Superação da dormência e germinação de sementes de Plathymenia reticulata (Fabaceae) em diferentes temperaturas. In: III Semana de Engenharia Florestal da Bahia, Universidade Estadual do Sudoeste da Bahia, Vitória da Conquista 1214-1219

Silva FF 2018. Uso de topsoil como fonte de inóculo de microrganismos simbiontes para leguminosas florestais usadas na recuperação de áreas degradadas na Caatinga. Dissertation, Universidade Federal Rural do Rio de Janeiro

Silva, FF 2022. Avaliação da associação simbiótica entre bactérias fixadoras de nitrogênio, fungos micorrízicos arbusculares e leguminosas arbóreas nativas da Caatinga. Thesis, Universidade Federal do Rio de Janeiro

Sun Y, Luo C, Jiang L, Song M, Zhang D, LI J, Ostle NJ, Zhang G 2020. Land-use changes alter soil bacterial composition and diversity in tropical forest soil in China. Sci Total Environ 712. https://doi.org/10.1016/j.scitotenv.2020.136526

Teixeira PC, Donagemma GK, Fontana A, Teixeira WG 2017. Manual de métodos de análise de solo, 3rd ed. Embrapa, Brasília, DF

Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A 2015. The importance of the microbiome of the plant holobiont. New Phytol. 206(4):1196-1206. https://doi.org/10.1111/nph.13312

Wubs ERJ, van der Putten WH, Bosch M, Bezemer TM 2016. Soil inoculation steers restoration of terrestrial ecosystems. Nature Plants 2:16107. https://doi.org/10.1038/nplants.2016.107

Zhang W, Li XG, Sun K, Tang MJ, Xu FJ, Zhang M, Dai CC 2020. Mycelial network-mediated rhizobial dispersal enhances legume nodulation. ISME J 14(4):1015-1029. https://doi.org/10.1038/s41396-020-0587-5

Descargas

Publicado

2024-04-05

Cómo citar

SANTOS, Thainá Alves dos; SILVA, Felipe Ferreira da; FARIA, Sergio Miana de; CHAER, Guilherme Montandon. Potencial Simbiótico de Microrganismos do Solo na Promoção do Crescimento de Espécies Arbóreas da Mata Atlântica. Fronteira: Journal of Social, Technological and Environmental Science, [S. l.], v. 13, n. 1, p. 105–129, 2024. DOI: 10.21664/2238-8869.2024v13i1.p105-129. Disponível em: https://periodicos.unievangelica.edu.br/index.php/fronteiras/article/view/7147. Acesso em: 21 nov. 2024.