Synergistic potential of nitrogen fertilization and endophytic microorganisms on initial growth of Sorghum bicolor

Keywords: Poaceae, Arbuscular mycorrhizal fungi, Seed

Abstract

Endophytic microorganisms such as arbuscular mycorrhizal fungi (AMF) and dark septate fungi (DSF) may influence plant development according to soil microbial interaction and fertility. The purpose of the work was to evaluate the effect of nitrogen levels on the interaction of AMF and DSF on initial sorghum growth. The experimental design was completely randomized in a 4 x 4 factorial scheme, corresponding to sorghum cultivation in four treatments (Control - without inoculation of AMF and three mycorrhizal isolates: UFLA351 - Rhizoglomus clarum, UFLA372 - Claroideoglomus etunicatum, and UFLA401 - Acaulospora morrowiae) and four nitrogen levels (N): 0, 100, 300, and 600 mg Kg-1 of N. The sorghum seeds presented the filamentous fungi Rhizoctonia, Colletotrichum, Curvularia, Fusarium, Helminthosporium and Mucor; and the bacterium Bacillus subtillis, which may have interfered with plant growth. In the UFLA351 and UFLA372 treatments, the increase in nitrogen levels reduces the initial growth of sorghum, but does not influence the colonization rate of endophytic fungi DSE. The UFLA401 isolate favors the initial growth of sorghum, but without nitrogen fertilization. The endophytic fungi “dark septate” can influence the rate of mycorrhizal colonization and, therefore, the initial growth of sorghum, depending on the microbial interaction.

Author Biographies

Jéssica Silva Santos, Universidade Federal de Sergipe - UFS
Doutoranda do Programa de Pós-graduação em Agricultura e Biodiversidade (PPGAGRI) da Universidade Federal de Sergipe (UFS), São Cristóvão (SE), Brasil.
Larissa de Souza Gois, Universidade Federal de Sergipe - UFS
Doutoranda do Programa de Pós-graduação em Agricultura e Biodiversidade (PPGAGRI) da Universidade Federal de Sergipe (UFS), São Cristóvão (SE), Brasil.
Johny de Jesus Mendonça, Universidade Federal do Rio Grande do Sul - UFRGS
Doutorando do Programa de Pós-graduação em Ciência do Solo (PPGCS) da Universidade Federal do Rio Grande do Sul (UFRGS), Faculdade de Agronomia, Porto Alegre (RS), Brasil.
Pedro Rabelo de Oliveira, Universidade Federal de Sergipe - UFS
Engenheiro Agrônomo da Universidade Federal de Sergipe (UFS), São Cristóvão (SE), Brasil.
Regina Helena Marino, Universidade Federal de Sergipe - UFS
Doutora em Biotecnologia e Docente permanente do Departamento de Engenharia Agronômica da Universidade Federal de Sergipe (UFS), São Cristóvão (SE), Brasil.

References

AMORIM, L.; BERGAMIN FILHO, A.; REZENDE, J. A. M. Manual de Fitopatologia. 5. ed. Ouro Fino: Agronômica Ceres, 2018.

BAMISILE, B. S.; DASH, C. K.; AKUTSE, K. S.; KEPPANAN, R.; Fungal Endophytes: Beyond Herbivore Management. Frontier in Microbiology, Lausana, v. 9, n. 544, p. 1-11, mar. 2018. DOI: https://doi.org/10.3389/fmicb.2018.00544.

BERNAOLA, L.; CANGE, G.; WAY, M. O.; GORE, J.; HARDKE, J.; STOUT, M. Natural colonization of rice by arbuscular mycorrhizal fungi in different production areas. Rice Science, Zhejiang, v. 25, n. 3, p. 169-174, mai. 2018. DOI: https://doi.org/10.1016/j.rsci.2018.02.006.

CAULIER, S.; NANNAN, C.; GILLIS, A.; LICCIARDI, F.; BRAGARD, C.; MAHILLON, J. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Frontier in Microbiology, Lausana, v. 10, n. 302, p. 1-19, fev. 2019. DOI: https://doi.org/10.3389/fmicb.2019.00302.

COBB, A. B.; WILSON, G. W. T.; GOAD, C. L.; BEAN, S. R., KAUFMAN, R. C.; HERALD, T. J.; WILSON, J. D. The role of arbuscular mycorrhizal fungi in grain production and nutrition of sorghum genotypes: Enhancing sustainability through plant-microbial partnership. Agriculture, Ecosystems and Environment, Amsterdam, v. 233, n. 1, p. 432-440, oct. 2016. DOI: https://doi.org/10.1016/j.agee.2016.09. 024.

EHTESHAMI, S. M. R.; KHAVAZI, K.; ASGHARZADEH, A. Forage sorghum quantity and quality as affected by biological phosphorous fertilization. Grass and Forage Science, Hoboken, v. 73, n. 4, p. 926–937, set. 2018. DOI: https://doi.org/10.1111/gfs.12388.

GIOVANNETTI, M.; MOSSE, B. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist, Cambridge, v. 84, n. 3, p. 489-500, mar. 1980. DOI: http://dx.doi.org/10.1111/j.1469-8137.1980.tb04556.x.

GOIS, L. S.; SANTOS, J. S.; SANTOS, J. F. S.; BARBOSA, A.V.G.; VIÉGAS, P. R. A.; MARINO, R. H. Endophytic microorganisms and nitrogen levels on rice plant growth. Ciência e Agrotecnologia, Lavras, v. 43, n. 2, p. 1-10, 2019. DOI: http://dx.doi.org/10.1590/1413-7054201943001519.

GOMIDE, P. H. O.; SANTOS, J. G. D.; SIQUEIRA, O.; SOARES, C. R. F. S. Diversidade e função de fungos micorrízicos arbusculares em sucessão de espécies hospedeiras. Pesquisa Agropecuária Brasileira, Brasília, v. 44, n. 11, p. 1483-1490, nov. 2009. DOI: https://doi.org/10.1590/S0100-204X2009001100016.

HADEBE, S. T.; MABHAUDHI, T.; MODI, A. Water use of sorghum (Sorghum bicolor L. Moench) in response to varying planting dates evaluated under rainfed conditions. Water SA, Gezina, v. 43, n. 1, p. 91-113, jan. 2017. DOI: https://doi.org/10.4314/wsa.v43i1.12.

JALONEN, R.; TIMONEN, S.; SIERRA, J.; NYGREN, P. Arbuscular mycorrhizal symbioses in a cut-and-carry forage production system of legume tree Gliricidia sepium and fodder grass Dichanthium aristatum. Agroforest System, Dordrecht-Netherlands, v. 87, n. 2, p. 319-330, jul. 2013. DOI: https://doi.org/10.1007/s10457-012-9553-1.

KISHOR, K.; KUMAR, Y. V.; GAUTAM, P.; CHUGH, A.; KAUSHAL, K. Effect of fertility levels on Yield and Yield attribute of different Sorghum [Sorghum bicolar (L.) Moench] genotypes. Journal of Pharmacognosy and Phytochemistry, New Delhi, v. 6, n. 4, p. 541–543, 2017. Disponível em: https://www.phytojournal.com/archives/2017/vol6issue4/PartH/6-4-51-354.pdf. Acesso em 08 ago. 2022.

LESSA, B. F. T.; DUTRA, A. S.; SILVA, T. M.; SANTOS, C. C.; SOUSA, W. N. Physiological maturation in seeds of sweet sorghum for foliar fertilization with silicate. Revista Caatinga, Mossoró, v. 30, n. 3, p. 718–729, jul./sept. 2017. DOI: https://doi.org/10.1590/1983-21252017v30n320rc.

LOPES, L. J. O.; SANTOS, G. M.; SANTOS, J. S.; SANTOS, J. F. S.; MENDONÇA, J. J.; FAGUNDES, J. L.; MARINO, R. H. Produção de propágulos micorrízicos em sorgo e/ou em braquiária. Scientia Plena, São Cristóvão, v. 14, n. 8, p .1-8, ago. 2018.

DOI: https://doi.org/10.14808/sci.plena.2018.086201.

MACHINESKI, O.; BALOTA, E. L.; SOUZA, J. R. P. Resposta da mamoneira a fungos micorrízicos arbusculares e a níveis de fósforo. Semina: Ciências Agrárias, Londrina, v. 32, n. 4, p. 1855-1862, abr. 2011. DOI: https://doi.org/10.5433/1679-0359.2011v32n4Sup1p1855.

MANDYAM, K.; JUMPPONEN, A. Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza, Londres, v. 18, n. 1, p. 145-155, jan. 2008. DOI: https://doi.org/10.1007/s00572-008-0165-6.

MENDONÇA, J. J.; LIRA-JUNIOR, M. A.; CARVALHO, E. X.; FRACETTO, G. G. M.; FRACETTO, F .J. C.; ALVES, M. J. G.; OLIVEIRA, J. P. Diversidade, mecanismos de atuação e potencial agrícola de bactérias promotoras de crescimento de plantas, usando milho como cultura exemplo. Pesquisa Agropecuária Pernambucana, Recife, v. 25, n. 2, p. 1–10, jun./dez. 2020. DOI: https://doi.org/10.12661/pap.2020.010.

MENDONÇA, J. J.; GOIS, L. S.; SANTOS, J. F. S.; SANTOS, T. A. C.; HOLANDA, F. S. R.; MARINO, R. H. Native microbiota and arbuscular mycorrhizal fungi on growth of Paspalum millegrana Schrad. Revista Caatinga, Mossoró, v. 32, n. 2, p. 345-353, fev. 2019. DOI: https://doi.org/10.1590/1983-21252019v32n207rc.

NAKMEE, P. S.; TECHAPINYAWAT, S.; NGAMPRASITC, S. Comparative potentials of native arbuscular mycorrhizal fungi to improve nutrient uptake and biomass of Sorghum bicolor Linn. Agriculture and Natural Resources, Amsterdam, v. 50, n. 3, p. 173-178, may. 2016. DOI: https://doi.org/10.1016/j.anres.2016.06.004.

NDINGA-MUNIANIA, C.; MUELLER, R. C.; KUSKE, C. R.; PORRAS-ALFARO, A. Seasonal variation and potential roles of dark septate fungi in an arid grassland. Mycologia, Londres, v. 113, n. 6, p. 1181-1198, oct. 2021. DOI: https://doi.org/10.1080/00275514.2021.1965852.

PANDEY, A. Are dark septate endophytic bioindicators of climate in mountain ecosystems? Rhizosphere, Amsterdã, v. 9, n. 1, p. 110-111, mar. 2019. DOI: https://doi.org/10.1016/j.rhisph.2019.01.001.

PEREIRA, G. M. D.; RIBEIRO, K,G.; JÚNIOR, P. I. F.; VITAL, M. J. S.; KASUYA, M. C. M.; ZILLI, J. E. Ocorrência de fungos endofíticos “dark septate” em raízes de Oryza glumaepatula na Amazônia. Pesquisa Agropecuária Brasileira, Brasília, v. 46, n. 3, p. 331-334, mar. 2011. DOI: https://doi.org/10.1590/S0100-204X2011000300015.

PÜSCHEL, D.; JANOUŠKOVÁ, M.; HUJSLOVÁ, M.; SLAVÍKOVÁ, R.; GRYNDLEROVÁ, H.; JANSA, J. Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecology e Evolution, Nova Jersey, v. 6, n. 13, p. 4332-4346, may. 2016. DOI: https://doi.org/10.1002/ece3.2207.

QIAO, Y.; BAI, Y.; SHE, W.; LIU, L.; MIAO, C.; ZHU, G.; QIN. S.; ZHANG, Y. Arbuscular mycorrhizal fungi outcompete fine roots in determining soil multifunctionality and microbial diversity in a desert ecosystem. Applied Soil Ecology, Amsterdã, v. 171, n. 1, p. 1-12, mar. 2022. DOI: https://doi.org/10.1016/j.apsoil.2021.104323.

RASHWAN, A. K.; YONES, H. A.; KARIM, N.; TAHA, E. M.; CHEN, W. Potential processing technologies for developing sorghum-based food products: An update and comprehensive review. Trends in Food Science and Technology, Amsterdam, v. 110, p. 168-182, apr. 2021. DOI: https://doi.org/10.1016/j.tifs.2021.01.087.

SANTANA-SANTOS, I. V.; CHAVES-SILVA, N. E.; AMÂNCIO, L. H. S.; SANTOS, W. B.; VIÉGAS, P. R. A.; MARINO, R. H. Fungos comestíveis e microbiota nativa no controle do nematoide formador de galhas. Revista em Agronegócio e Meio Ambiente – RAMA, Maringá, v. 15, n. 2, e9086, abr./jun. 2022. DOI: https://doi.org/10.17765/2176-9168.2022v15n2e9301.

SANTOS, J. S.; SANTOS, J. F. S.; LOPES, L. J. O.; MENDONÇA, J. J.; HOLANDA, F. S. R.; MARINO, R. H. Arbuscular mycorrhizal fungi and dark septate endophytic fungi on the biomass development of vetiver grass. Revista Caatinga, Mossoró, v. 31, n. 3, p. 602-611, mar. 2018a. DOI: https://doi.org/10.1590/1983-21252018v31n308rc.

SANTOS, T. A. C.; MENEZES, G. S.; SANTOS, J. S.; GOIS, L. S.; NASCIMENTO, S. L. M.; MARINO, R. H. Microbial Interactions in the development of biomass of gliricidia. Revista Caatinga, Mossoró, v. 31, n. 3, p. 612-621, mar. 2018b. DOI: https://doi.org/10.1590/1983-21252018v31n309rc.

SYMANCZIK, S.; LEHMANN, M.; WIEMKEN, A.; BOLLER, T.; COUTRY, P. Effects of two contrasted arbuscular mycorrhizal fungal isolates on nutrient uptake by Sorghum bicolor under drought. Mycorrhiza, Londres, v. 28, n. 8, p. 779-785, ago. 2018. DOI: https://doi.org/10.1007/s00572-018-0853-9.

TEUTSCHEROVA, N.; VASQUEZ, E.; ARANGO, J.; AREVALO, A.; BENITO, M.; PULLEMAN, M Native arbuscular mycorrhizal fungi increase the abundance of ammonia-oxidizing bacteria but suppress nitrous oxide emissions shortly after urea application. Geoderma, Amsterdã, v. 338, n. 1, p. 493-501, mar. 2019. DOI: https://doi.org/10.1016/j.geoderma.2018.09.023.

VAN HEIJDEN, M. G. A.; MARIN, F. M.; SELOSSE, M. A.; SANDRES, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist, Cambridge, v. 205, n. 4, p. 406-1423, fev. 2015. DOI: https://doi.org/10.1111/nph.13288.

YAN, J. F.; BROUGHTON, S. J.; YANG, S. L.; GANGE, A. C. Do endophytic fungi grow through their hosts systemically? Fungal Ecology, Amsterdã, v. 13, n. 1, p. 53-59, fev. 2015. DOI: https://doi.org/10.1016/j.funeco.2014.07.005.

ZHANG, X.; WANG, L.; M. A. F.; YANG, J.; SU, M. Effects of arbuscular mycorrhizal fungi inoculation on carbon and nitrogen distribution and grain yield and nutritional quality in rice (Oryza sativa L.). J. Science of Food and Agriculture, Hoboken, v. 97, n. 9, p. 2919–2925, nov. 2017. DOI: https://doi.org/10.1002/jsfa.8129.

ZUBEK, S.; KAPUSTA, P.; ROŻEK, K.; BŁASZKOWSKI, J.; GIELAS I,; NOBIS, M.; NOWAK, A. Fungal root colonization and arbuscular mycorrhizal fungi diversity in soils of grasslands with different mowing intensities. Applied Soil Ecology, Amsterdã, v. 172, n. 1, p. 1-10, apr. 2021. DOI: https://doi.org/10.1016/j.apsoil.2021.104358.

Published
2023-08-22
Section
Agrobusiness