Physiological changes in tomato colonized by dark septate endophytic fungi
DOI:
https://doi.org/10.33448/rsd-v12i4.41188Keywords:
Root colonization; Tomato; Nitrogen fraction; Soluble sugars; pH.Abstract
As is customary in mycorrhizae, the interaction between plant and dark septate endophytic (DSE) fungi can result in physiological changes in the host plant, which are still poorly understood. This study aimed to evaluate the physiological changes in tomato plants colonized by DSE fungi. Four DSE isolates previously identified through ITS phylogeny were inoculated on tomato seeds and compared to non-inoculated plants (control). Kinetic parameters (Vmax and Km) were calculated measuring the nitrate content in the nutrient solution. The contents of NO3--N, NH4+-N, amino-N, soluble sugars in the root, petiole, stem and leaf, and the contents of macronutrients in the shoot were determined. The plants inoculated with A101 and A105 exhibited (i) significant increases in the soluble sugar contents; (ii) increases in the contents of P, K, Mg and S; and (iii) increased dry biomass compared to control. The A103 inoculation was antagonistic when compared to the other treatments, leading to a higher influx of NO3--N in the plants, resulting in a higher amino-N and the lower soluble sugar content in the shoot. The physiological parameters of tomato varied depending on the inoculation, and the changes ranged from positive to negative depending on each isolate involved in the interaction.
References
Addy, H. D., Piercey, M. M., & Currah, R. S. (2005). Microfungal endophytes in roots. Canadian Journal of Botany, 83(1), 1-13. DOI: https://doi.org/10.1139/b04-171
Alaburda, J., & Nishihara, L. (1998). Presença de compostos de nitrogênio em águas de poços. Revista de Saúde Pública, 32(2), 160-165.
Alberton, O., Kuyper, T. W., & Summerbell, R. C. (2010). Dark septate root endophytic fungi increase growth of Scots pine seedlings under elevated CO2 through enhanced nitrogen use efficiency. Plant and Soil, 328, 459-470.
Alves, L. S., Torres-Junior, C. V., Fernandes, M. S., Santos, A. M., & Souza, S. R. d. (2016). Soluble fractions and kinetics parameters of nitrate and ammonium uptake in sunflower (“Neon” Hybrid). Revista Ciência Agronômica, 47, 13-21.
Andrade-Linares, D. R., Grosch, R., Restrepo, S., Krumbein, A., & Franken, P. (2011). Effects of dark septate endophytes on tomato plant performance. Mycorrhiza, 21(5), 413-422. DOI: https://doi.org/10.1007/s00572-010-0351-1
Baptista, J. A., Fernandes, M. S., & Souza, S. R. d. (2000). Cinética de absorção de amônio e crescimento radicular das cultivares de arroz Agulha e Bico Ganga. Pesquisa Agropecuária Brasileira, 35(7), 1325-1330.
Barrow, J. R., & Aaltonen, R. E. (2001). A method of evaluating internal colonization of Atriplex canescens (Pursh) Nutt. Roots by dark septate fungi and how they are influenced by host physiological activity. Mycorrhiza, 11, 199-205.
Borges, E. d. A., Fernades, M. S., Loss, A., Silva, E. E. d., & Souza, S. R. d. (2006). Acúmulo e remobilização de nitrogênio em variedades de milho. Revista Caatinga, 19(3), 278-286.
Bucher, C. A. (2007). Avalição através de RT-PCR da expressão dos genes que codificam para enzimas de assimilação de nitrogênio em variedades de arroz [Dissertation, Universidade Federal Rural do Rio de Janeiro].
Bucher, C. A. (2011). Expressão de genes relacionados à absorção e metabolismos de nitrogênio em Arroz sob alto e baixo suprimento de nitrato [Dissertation, Universidade Federal Rural do Rio de Janeiro].
Cerri, C. E. P., Sparovek, G., Bernoux, M., Easterling, W. E., Melillo, J. M., & Cerri, C. C. (2007). Tropical agriculture and global warming: impacts and mitigation options. Scientia Agricola, 64(1), 83-99. DOI: https://doi.org/10.1590/S0103-90162007000100013
Cometti, N. N., Furlani, P. R., Ruiz, H. A., & Filho, E. I. F. (2006). Soluções nutritivas: formulações e aplicações. In M. S. Fernandes (Ed.), (pp. 89-144).
Crawford, N. M., & Glass, A. D. M. (1998). Molecular and physiological aspects of nitrate uptake in plants. TRENDS in Plant Science, 3(10), 389-395.
De Angeli, A., Monachello, D., Ephritikhine, G., Frachisse, J. M., Thomine, S., Gambale, F., & Barbier-Brygoo, H. (2006). The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature, 442, 939-942.
Felker, P. (1977). Micro determination of nitrogen in seed protein extracts. Analytical Chemistry, 49(7), 1080-1080.
Fernandes, M. S. (1984). Carriers, light and temperature influences on the free amino acid pool composition of Rice plants. Turrialba, 33(3), 297-301.
Filgueira, F. A. R. (2008). Novo manual de Olericultura: agrotecnologia moderna na produção e comercialização de hortaliças (3rd ed.). UFV Viçosa-MG.
Furlani, A. M. C., & Furlani, P. R. (1988). Composição e pH de soluções nutritivas para estudos fisiológicos e seleção de plantas em condições nutricionais adversas. Campinas. In. Gaxiola, R. A., Palmgren, M. G., & Schumacher, K. (2007). Plant proton pumps. FEBS Letters, 581, 2204-2214.
Hirel, B., Bertin, P., Quilleré, I., Bourdoncle, W., Attagnant, C., Dellay, C., . . . Gallais, A. (2001). Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiology, 125, 1258-1270.
Hoagland, D. R., & Arnon, D. I. (1950). The water-culture method for growing plants without soil. California Agricultural of Experimental Stn. Bull, 347, 1-32.
Jumpponen, A., & Trappe, J. M. (1998). Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytologist, 140(2), 295-310. DOI: https://doi.org/10.1046/j.1469-8137.1998.00265.x
Kohout, P., Sýkorová, Z., Čtvrtlíková, M., Rydlová, J., Suda, J., Vohník, M., & Sudová, R. (2012). Surprising spectra of root-associated fungi in submerged aquatic plants. FEMS Microbiology Ecology, 80, 216-235.
Lee, R. B., & Rudge, R. A. (1986). Effects of nitrogen deficiency on the absorption of nitrate and ammonium by barley plants. Annals of Botany, 57, 471-486.
Li, Y., Luo, A., Wei, X., & Yao, X. (2007). Genotypic variation of rice in phosphorus acquisition from iron phosphate: contributions of root morphology and phosphorus uptake kinetics. Russian Journal of Plant Physiology, 54(2), 230-236. DOI: https://doi.org/10.1134/S102144370
Lucini, T. (2013). Mecanismos de resistência ao ácaro rajado em genótipos de tomateiro com altos teores de acil-açúcares [Dissertation, Universidade Estadual Do Centro-Oeste, Unicentro-PR].
Lukešová, T., Kohout, P., Větrovský, T., & Vohník, M. (2015). The Potential of Dark Septate Endophytes to Form Root Symbioses with Ectomycorrhizal and Ericoid Mycorrhizal Middle European Forest Plants. PLoS ONE, 10(4).
Mahmoud, R. S., & Narisawa, K. (2013). A New Fungal Endophyte, Scolecobasidium humicola, Promotes Tomato Growth under Organic Nitrogen Conditions. PLoS ONE, 8(11), e78746-e78746. DOI: https://doi.org/10.1371/journal.pone.0078746
Mandyam, K., & Jumpponen, A. (2005). Abundance and possible functions of the root-colonizing dark septate endophytic fungi. Studies in Mycology, 53, 173-190.
Mandyam, K., & Jumpponen, A. (2008). Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment. Mycorrhiza, 18, 145-155.
Mandyam, K., Loughin, T., & Jumpponen, A. (2010). Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia, 102(4), 813-821. DOI: https://doi.org/10.3852/09-212
McGonigle, T. P., Miller, M. H., Evans, D. G., Fairchild, G. L., & Swan, J. A. (1990). A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist, 115, 495-501.
Miranda, K. M., Espey, M. G., & Wink, D. A. (2001). A Rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. NITRIC OXIDE: Biology and Chemistry, 5(1), 62-71.
Newsham, K. K. (1999). Phialophora graminicola , a dark septate fungus, is a beneficial associate of the grass Vulpia ciliata ssp. ambigua. New Phytologist, 144(3), 517-524. DOI: https://doi.org/10.1046/j.1469-8137.1999.00537.x
Newsham, K. K. (2011). A meta-analysis of plant responses to dark septate root endophytes. New Phytologist, 190(3), 783-793. DOI: https://doi.org/10.1111/j.1469-8137.2010.03611.x
Oliveira, S. A. S. d., Stark, E. M. L. M., Epifânio, J. A., Berbara, R. L. L., & Souza, S. R. d. (2011). Partição de nitrogênio em variedades de milho (Zea mays L.) com a aplicação foliar de microorganismos eficazes e nitrato. Revista Universidade Rural. Série Ciências da Vida, 31(1), 57-69.
Paixão, C. F. C. d., Vidal, V. M., Gomes, L. F., Lira, L. C. d., Soares, J. A. B., Moraes, G. S., . . . Soares, F. A. L. (2020). Crescimento de plantas e qualidade de frutos de tomate tipo sweet grape sob efeitos de doses de nitrogênio e reposições hídricas. Research, Society and Development, 9(7), e917974784. DOI: https://doi.org/10.33448/rsd-v9i7.4784
Pereira, A. S., Shitsuka, D., Parreira, F., & Shitsuka, R. (2018). Metodologia da pesquisa científica [recurso eletrônico]. Santa Maria, BR: UFSM, NTE.
Peterson, R. L., Wagg, C., & Pautler, M. (2008). Associations between microfungal endophytes and roots: do structural features indicate function? Botany, 86, 445-456.
Phillips, J. M., & Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. The British Mycological Society, 55(1), 157-160. DOI: https://doi.org/10.1016/S0007-1536(70)80110-3
R: A language and environment for statistical computing. (2017). In. Vienna: R Foundation for Statistical Computing.
Ribeiro, K. G. (2011). Fungos endofíticos dark septates em arroz silvestre Oryza glumaepatula Steund [Dissertation, Universidade Federal de Roraima]. Boa Vista,RO.
Rocha, J. G. d., Ferreira, L. M., Tavares, O. C. H., Santos, A. M. d., & Souza, S. R. d. (2014). Cinética de absorção de nitrogênio e acúmulo de frações solúveis nitrogenadas e açúcares em girassol. Pesquisa Agropecuária Tropical, 44(4), 381-390.
Santi, S., Locci, G., Pinton, R., Cesco, S., & Varanini, Z. (1995). Plasma membrane H+ATPase in maize roots induced for NO3- uptake. Plant Physiology, 109, 1277-1283.
Santos, L. A. (2006). Absorção e Remobilização de NO3- em arroz (Orysa sativa L.): atividade das bombas de prótons e a dinâmica do processo [Dissertation, Universidade Federal Rural do Rio de Janeiro].
Santos, L. A., Bucher, C. A., Souza, S. R. d., & Fernandes, M. S. (2005). Metabolismo de nitrogênio em arroz sob níveis decrescentes de nitrato. Agronomia, 39(1-2), 28-33.
Santos, L. A., Bucher, C. A., Souza, S. R. d., & Fernandes, M. S. (2009). Effects of nitrogen stress on proton-pumping and nitrogen metabolism in rice. Journal of Plant Nutrition, 32, 549-564.
Santos, L. A., Santos, W. A., Sperandio, M. V. L., Bucher, C. A., Souza, S. R. d., & Fernandes, M. S. (2011). Nitrate uptake kinetics and metabolic parameters in two rice varieties grown in high and low nitrate. Journal of Plant Nutrition, 34(7), 988-1002.
Souza, S. R. d., Stark, E. M. L. M., & Fernandes, M. S. (1998). Nitrogen remobilization during the reproductive period in two Brazilian rice varieties. Journal of Plant Nutriton(21), 2049-2063.
Sperandio, M. V. L. (2011). Expressão gênica de transportadores de nitrato e amônio, proteína reguladora de NAR e bombas de prótons em Arroz (Oryza sativa L.) e seus efeitos na eficiência de absorção de nitrogênio [Dissertation, Universidade Federal Rural do Rio de Janeiro].
Sperandio, M. V. L., Santos, L. A., Bucher, C. A., Fernandes, M. S., & Souza, S. R. d. (2011). Isoforms of plasma membrane H+-ATPase in rice root and shoot are differentially induced by starvation and resupply of NO3- or NH4+. Plant Science, 180, 251-258.
Tedesco, M. J. (1982). Extração simultânea de N, P, K, Ca, e Mg em tecido de plantas por disgestão com H2O2-H2SO4. UFRGS, Porto Alegre, RS, 23-23p.
Upson, R., Read, D. J., & Newsham, K. K. (2009). Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza, 20(1), 1-11. DOI: https://doi.org/10.1007/s00572-009-0260-3
Usuki, F., & Narisawa, K. (2007). A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia, 99(2), 175-184. DOI: https://doi.org/10.3852/mycologia.99.2.175
Vergara, C., Araujo, K. E. C., Alves, L. S., Souza, S. R. d., Santos, L. A., Santa-Catarina, C., . . . Zilli, J. É. (2018). Contribution of dark septate fungi to the nutrient uptake and growth of rice plants. Brazilian Journal of Microbiology, 49(1), 67-78. DOI: https://doi.org/10.1016/j.bjm.2017.04.010
Vergara, C., Araujo, K. E. C., Souza, S. R. d., Schultz, N., Jaggin Júnior, O. J., Sperandio, M. V. L., & Zilli, J. É. (2019). Plant-mycorrhizal fungi interaction and response to inoculation with different growth-promoting fungi. Pesquisa Agropecuária Brasileira, 54. http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0100-204X2019000103301&nrm=iso
Vergara, C., Araujo, K. E. C., Sperandio, M. V. L., Santos, L. A., Urquiaga, S., & Zilli, J. É. (2019). Dark septate endophytic fungi increase the activity of proton pumps, efficiency of 15N recovery from ammonium sulphate, N content, and micronutrient levels in rice plants. Brazilian Journal of Microbiology. DOI: https://doi.org/10.1007/s42770-019-00092-4
Vergara, C., Araujo, K. E. C., Urquiaga, S., Santa-Catarina, C., Schultz, N., da Silva Araújo, E., . . . Zilli, J. É. (2018). Dark Septate Endophytic Fungi Increase Green Manure-(15)N Recovery Efficiency, N Contents, and Micronutrients in Rice Grains. Frontiers in Plant Science, 9, 613. DOI: https://doi.org/10.3389/fpls.2018.00613
Vergara, C., Araujo, K. E. C., Urquiaga, S., Schultz, N., Balieiro, F. d. C., Medeiros, P. S., . . . Zilli, J. E. (2017). Dark Septate Endophytic Fungi Help Tomato to Acquire Nutrients from Ground Plant Material [Original Research]. Frontiers in microbiology, 8(2437). DOI: https://doi.org/10.3389/fmicb.2017.02437
Wilcox, H. E., & Ganmore-Neumann, R. (1974). Ectendomycorrhizae inPinus resinosaseedlings. I. Characteristics of mycorrhizae produced by a black imperfect fungus. Canadian Journal of Botany, 52, 2145-2153.
Wilcox, H. E., & Wang, C. J. K. (1987). Mycorrhizal and pathological associations of dematiaceous fungi in roots of 7-month-old tree seedlings. Canadian Journal of Forest Research, 17(8), 884-899. DOI: https://doi.org/10.1139/x87-140
Xu, G., Fan, X., & Miller, A. J. (2012). Plant Nitrogen Assimilation and Use Efficiency. Annual Review of Plant Biology, 63(1), 153-182.
Yemm, E. W., & Cocking, E. C. (1955). The determination of amino-acid with ninhydrin. Analytical Biochemistry, 80, 209-213.
Yemm, E. W., & Willis, A. J. (1954). The estimation of carbohydrate in plants extracts by anthrone. Biochemistry, 57, 508-514.
Yu, T., Nassuth, A., & Peterson, R. L. (2001). Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Canadian Journal of Microbiology, 47, 741-753.
Zhang, H.-h., Tang, M., Chen, H., & Wang, Y.-j. (2012). Effects of a dark-septate endophytic isolate LBF-2 on the medicinal plant Lycium barbarum L. The Journal of Microbiology, 50(1), 91-96. DOI: https://doi.org/10.1007/s12275-012-1159-9
Zhang, Y., Li, T., & Zhao, Z.-W. (2013). Colonization Characteristics and Composition of Dark Septate Endophytes (DSE) in a Lead and Zinc Slag Heap in Southwest China. Soil and Sediment Contamination, 22, 532-545.
Zhang, Z., Rengel, Z., & Meney, K. (2009). Kinetics of ammonium, nitrate and phosphorus uptake by Canna indica and Schoenoplectus validus. Aquatic Botany, 91(2), 71-74.
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