Mycorrhization of strawberry plantlets potentiates the synthesis of phytochemicals during ex vitro acclimatization
Resumo
Ex vitro strawberry plantlets from micropropagation and coinoculated with arbuscular mycorrhizal fungi (AMF) and biochar can provide beneficial health effects. In the present study, we evaluated the effects of different proportions of biochar in the presence and absence of AMF on the production of secondary metabolites in the leaves and roots of strawberry plantlets during ex vitro acclimatization. Additionally, the enzymatic activity of the substrate enriched with AMF and biochar was analyzed. The experiment consisted of the control (absence of the mycorrhizal community) and four biochar proportions (0, 3, 6, and 9% of the volume of the container) coinoculated with AMF. Plantlets produced on substrates enriched with AMF showed higher levels of polyphenols, flavonoids, phenolic acids, and tannins in the tissues analyzed than control plantlets. The combination of AMF and 9% biochar increased the content of total flavonoids in the leaves of strawberry plantlets and increased the activity of phosphatase. The substrate with up to 6% biochar and mycorrhizae showed increased β-glucosidase activity. In conclusion, mycorrhizae are excellent tools to improve the phytochemical quality of strawberry plantlets acclimatized ex vitro. The association between host plants, mycorrhizal symbionts, and bioactivators of these fungi potentiates properties beneficial to health, which can be exploited efficiently in sustainable agriculture.
Downloads
Referências
Adolfsson, L., Nziengui, H., Abreu, I. N., Šimura, J., Beebo, A., Herdean, A., … Spetea, C. (2017). Enhanced secondary and hormone metabolism in leaves of arbuscular mycorrhizal Medicago truncatula. Plant Physiology, 175(1), 392-411. DOI: https://doi.org/10.1104/pp.16.01509
Besbes, F., Habegger, R., & Schwab, W. (2019). Induction of PR-10 genes and metabolites in strawberry plants in response to Verticillium dahliae infection. BMC Plant Biology, 19, 1-17. DOI: https://doi.org/10.1186/s12870-019-1718-x
Björkman, M., Klingen, I., Birch, A. N. E., Bones, A. M., Bruce, T. J. A., Johansen, T. J., … Stewart, D. (2011). Phytochemicals of Brassicaceae in plant protection and human health Influences of climate, environment and agronomic practice. Phytochemistry, 72(7), 538-556. DOI: https://doi.org/10.1016/j.phytochem.2011.01.014
Borkowska, B. (2002). Growth and photosynthetic activity of micropropagated strawberry plants inoculated with endomycorrhizal fungi (AMF) and growing under drought stress. Acta Physiologiae Plantarum, 24, 365-370. DOI: https://doi.org/10.1007/s11738-002-0031-7
Brasil. (2017). Ministério da Saúde. Agência Nacional de Vigilância Sanitária (ANVISA). Resolução da Diretoria Colegiada - RDC Nº 166, de 24 de Julho de 2017. Dispõe sobre a validação de métodos analíticos e dá outras providências.
Campanelli, A., Ruta, C., Tagarelli, A., Morone-Fortunato, I., & De Mastro, G. (2014). Effectiveness of mycorrhizal fungi on globe artichoke (Cynara cardunculus L. var. scolymus) micropropagation. Journal of Plant Interactions., 9(1), 100-106. DOI: https://doi.org/10.1080/17429145.2013.770928
Cavallaro, V. A., Tringali, S., & Patanè, C. (2011). Large-scale in vitro propagation of giant reed (Arundo donax L.), a promising biomass species. The Journal of Horticultural Science and Biotechnology, 86(5), 452-456. DOI: https://doi.org/10.1080/14620316.2011.11512787
Cecatto, A. P., Ruiz, F. M., Calvete, E. O., Martínez, J., & Palencia, P. (2016). Mycorrhizal inoculation affects the phytochemical content in strawberry fruits. Acta Scientiarum. Agronomy, 38(2), 227-237. DOI: https://doi.org/10.4025/actasciagron.v38i2.27932
Ceccarelli, N., Curadi, M., Martelloni, L., Sbrana, C., Picciarelli, P., & Giovannetti, M. (2010). Mycorrhizal colonization impacts on phenolic content and antioxidant properties of artichoke leaves and flower heads two years after field transplant. Plant and Soil, 335(1), 311-323. DOI: https://doi.org/10.1007/s11104-010-0417-z
Chaves, V. C., Calvete, E. O., & Reginatto, F.H. (2017). Quality properties and antioxidant activity of seven strawberry (Fragaria x ananassa Duch.) cultivars. Scientia Horticulturae, 225, 293-298. DOI: https://doi.org/10.1016/j.scienta.2017.07.013
Chiomento, J. L. T., Stürmer, S. L., Carrenho, R., Costa, R. C., Scheffer-Basso, S. M., Antunes, L. E. C., ... Calvete, E. O. (2019a). Composition of arbuscular mycorrhizal fungi communities signals generalist species in soils cultivated with strawberry. Scientia Horticulturae, 253, 286-294. DOI: https://doi.org/10.1016/j.scienta.2019.04.029
Chiomento, J. L. T., Costa, R. C., De Nardi, F. S., Trentin, N. S., Nienow, A. A., & Calvete, E. O. (2019b). Arbuscular mycorrhizal fungi communities improve the phytochemical quality of strawberry. The Journal of Horticultural Science and Biotechnology, 94(5), 653-663. DOI: https://doi.org/10.1080/14620316.2019.1599699
Cvetković, D. J, Stanojević, L. P., Stanković, M. Z., Cakić, M. D., Savić, S. R., & Miljković, M. D. (2017). Antioxidant activity of strawberry (Fragaria x ananassa Duch.) leaves. Separation Science and Technology, 52(6), 1039-1051. DOI: https://doi.org/10.1080/01496395.2017.1281305
De Tender, C. A., Debode, J., Vandecasteele, B., D’hose, T., Cremelie, P., Haegeman, A., … Maes, M. (2016). Biological, physicochemical and plant health responses in lettuce and strawberry in soil or peat amended with biochar. Applied Soil Ecology, 107, 1-12. DOI: https://doi.org/10.1016/j.apsoil.2016.05.001
Duarte, L. J., Chaves, V. C., Nascimento, M. V. P. S., Calvete, E. O., Li, M., Ciraolo, E., … Dalmarco, E. M. (2018). Molecular mechanism of action of Pelargonidin-3-O-glucoside, the main anthocyanin responsible for the anti-inflammatory effect of strawberry fruits. Food Chemistry, 247, 56-65. DOI: https://doi.org/10.1016/j.foodchem.2017.12.015
Ferlemi, A. V., & Lamari, F. N. (2016). Berry leaves: an alternative source of bioactive natural products of nutritional and medicinal value. Antioxidants, 5(2), 1-20. DOI: https://doi.org/10.3390/antiox5020017
Ferrari, M. P. S., Queiroz, M. S., Andrade, M. M., Alberton, O., Gonçalves, J. E., Gazim, Z. C., & Magalhães, H. M. (2020). Substrate-associated mycorrhizal fungi promote changes in terpene composition, antioxidant activity, and enzymes in Curcuma longa L. acclimatized plants. Rhizosphere, 13. DOI: https://doi.org/10.1016/j.rhisph.2020.100191
Giampieri, F., Forbes-Hernandez, T. Y., Gasparrini, M., Alvarez-Suarez, J. M., Afrin, S., Bompadre, S., ... Battino, M. (2015). Strawberry as a health promoter: an evidence based review. Food & Function, 6(5), 1386-1398. DOI: https://doi.org/10.1039/C5FO00147A
Gianfreda, L. (2015). Enzymes of importance to rhizosphere processes. Journal of Soil Science and Plant Nutrition, 15(2), 283-306. DOI: https://doi.org/10.4067/S0718-95162015005000022
Gómez, J. D., Denef, K., Stewart, C. E., Zheng, J., & Cotrufo, M. F. (2014). Biochar addition rate influences soil microbial abundance and activity in temperate soils. European Journal of Soil Science, 65(1), 28-39. DOI: https://doi.org/10.1111/ejss.12097
Guerra, P. A. M., Sanjúan, M. D. C. S., & López, M. J. (2018). Evaluation of physicochemical properties and enzymatic activity of organic substrates during four crop cycles in soilless containers. Food Science & Nutrition, 6(8), 2066-2078. DOI: https://doi.org/10.1002/fsn3.757
Gutteridge, J. M., & Halliwell, B. (2010). Antioxidants: molecules, medicines, and myths. Biochemical and Biophysical Research, 393(4), 561-564. DOI: https://doi.org/10.1016/j.bbrc.2010.02.071
International Conference on Harmonization [ICH]. (2005). Guideline on the validation of analytical procedures: Text and methodology Q2 (R1). London, UK: ICH.
Kapoor, R., Sharma, D., & Bhatnagar, A.K. (2008). Arbuscular mycorrhizae in micropropagation systems and their potential applications. Scientia Horticulturae, 116(3), 227-239. DOI: https://doi.org/10.1016/j.scienta.2008.02.002
Koron, D., Sonjak, S., & Regvar, M. (2014). Effects of non-chemical soil fumigant treatments on root colonisation with arbuscular mycorrhizal fungi and strawberry fruit production. Crop Protection, 55, 35-41. DOI: https://doi.org/10.1016/j.cropro.2013.09.009
Lingua, G., Bona, E., Manassero, P., Marsano, F., Todeschini, V., Cantamessa, S., ... Berta, G. (2013). Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads increases anthocyanin concentration in strawberry fruits (Fragaria x ananassa var. Selva) in conditions of reduced fertilization. International Journal of Molecular Sciences, 14(8), 16207-16225. DOI: https://doi.org/10.3390/ijms140816207
Liu, L., Wang, Y. F., Yan, X. W., Li, J. W., Jiao, N. Y., & Hu, S. J. (2017). Biochar amendments increase the yield advantage of legume-based inter cropping systems over monoculture. Agriculture, Ecosystems & Environment, 237, 16-23. DOI: https://doi.org/10.1016/j.agee.2016.12.026
López-Ráez, J. A., Flors, V., Garcia, J. M., & Pozo, M. J. (2010). AM symbiosis alters phenolic acid content in tomato roots. Plant Signaling & Behavior, 5(9), 1138-1140. DOI: https://doi.org/10.4161/psb.5.9.12659
Miliauskas, G., Venskutonis, P. R., & Van Beek, T. A. (2004). Screening of radical scavenging activity of some medicinal and aromatic plant extracts. Food Chemistry, 85(2), 231-237. DOI: https://doi.org/10.1016/j.foodchem.2003.05.007
Mirjani, L., Salimi, A., Matinizadeh, M., Razavi, K., & Shahbazi, M. (2019). The role of arbuscular mycorrhizal fungi on acclimatization of micropropagated plantlet Satureja khuzistanica Jam. by ameliorating of antioxidant activity and expression of PAL gene. Scientia Horticulturae, 253(1), 364-370. DOI: https://doi.org/10.1016/j.scienta.2019.04.060
Murashige, T., & Skoog, F. A. (1962). Revised medium for rapid growth and bio assays with tobacco tissue cultures. Plant Physiology, 15(3), 473-497. DOI: https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Palei, S., Das, A. K., & Rout, G. R. (2015). In vitro studies of strawberry - an important fruit crop: a review. The Journal of Plant Science Research, 31(2), 115-131.
Paz-Ferreiro, J., Fu, S. L., Mendez, A., & Gasco, G. (2014). Interactive effects of biochar and the earthworm Pontoscolex corethrurus on plant productivity and soil enzyme activities. Journal of Soils and Sediments, 14(3), 483-494. DOI: https://doi.org/10.1007/s11368-013-0806-z
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. Transactions of the British Mycological Society, 55(1), 158-161. DOI: https://doi.org/10.1016/S0007-1536(70)80110-3
Raghuwanshi, R., & Sinha, S. (2014). Linking mycorrhizal technology with medicinal plant secondary metabolites. In R. N. Kharwar, R. S. Upadhyay, N. K. Dubey, & R. Raghuwanshi (Eds.), Microbial diversity and biotechnology in food security (p. 121-132.). Cham, SW: Springer.
Redecker, D., Schubler, A., Stockinger, H., Stürmer, S. L., Morton, J. B., & Walker, C. (2013). An evidence based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza, 23, 515-531. DOI: https://doi.org/10.1007/s00572-013-0486-y
Rouphael, Y., Franken, P., Schneider, C., Schwarz, D., Giovannetti, M., Agnolucci, M., … Colla, G. (2015). Arbuscular mycorrhizal fungi act as biostimulants in horticultural crops. Scientia Horticulturae, 196, 91-108. DOI: https://doi.org/10.1016/j.scienta.2015.09.002
Singleton, V. L., Orthofer, R., & Lamuela-Raventos, R. M. (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology, 299, 152-178. DOI: https://doi.org/10.1016/S0076-6879(99)99017-1
Tabatabai, M. A. (1982). Soil enzyme. In A. L. Page (Ed.), Methhods of soil analysis (p. 903-948.), part 2. Madison, US: American Society of Agromony.
Tabatabai, M. A., & Bremmer, J. M. (1969). Use of p-nitrophenyl phosphate in assay of soil phosphatase activity. Soil Biology and Biochemistry, 1(4), 301-307. DOI: https://doi.org/10.1016/0038-0717(69)90012-1
Trouvelot, A., Kouch, J., & Gianinazzi-Pearson, V. (1986). Mesure du taux de mycorhization VA d’un système radiculaire: recherche of method d’estimation ayant une signification fonctionelle. In V. Gianinazzi-Pearson, & S. Gianinazzi (Eds.), Aspects physiologiques et génétiques des mycorhizes (p. 217–221). Paris, FR: Inra Press.
Umaru, I. J., Samling, B., & Umaru, H. A. (2018). Phytochemical screening of Etlingera elatior (torch ginger) cultivated on different dosage of biochar. Asian Journal of Biochemistry, Genetics and Molecular Biology, 1(4), 1-6.
Villarreal, T. C., Medina, M. E., Ulloa, S. M., Darwin, R. O., Bangeppagari, M., Selvaraj, T., & Sikandar, I. M. (2016). Effect of arbuscular mycorrhizal fungi (AMF) and Azospirillum on growth and nutrition of banana plantlets during acclimatization phase. Journal of Applied Pharmaceutical Science, 6(6), 131-138. DOI: https://doi.org/10.7324/JAPS.2016.60623
Warnock, D. D., Lehmann, J., Kuyper, T. W., & Rillig, M. C. (2007). Mycorrhizal responses to biochar in soil - concepts and mechanisms. Plant and Soil, 300, 9-20. DOI: https://doi.org/10.1007/s11104-007-9391-5
Zayova, E., Nikolova, M., Dimitrova, L., & Petrova, M. (2016). Comparative study of in vitro, ex vitro and in vivo propagated Salvia hispanica (Chia) plants: morphometric analysis and antioxidant activity. AgroLife Scientific Journal, 5(2), 166-174.
Zhu, Q. Y., Hackman, R. M., Ensunsa, J. L., Holt, R. R., & Keen, C. L. (2002). Antioxidative activities of oolong tea. Journal of Agricultural and Food Chemistry, 50(23), 6929-6934. DOI: https://doi.org/10.1021/jf0206163
Zhu, X., Chen, B., Zhu, L., & Xing, B. (2017). Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: a review. Environmental Pollution, 227, 98-115. DOI: https://doi.org/10.1016/j.envpol.2017.04.032
DECLARAÇÃO DE ORIGINALIDADE E DIREITOS AUTORAIS
Declaro que o presente artigo é original, não tendo sido submetido à publicação em qualquer outro periódico nacional ou internacional, quer seja em parte ou em sua totalidade.
Os direitos autorais pertencem exclusivamente aos autores. Os direitos de licenciamento utilizados pelo periódico é a licença Creative Commons Attribution 4.0 (CC BY 4.0): são permitidos o compartilhamento (cópia e distribuição do material em qualqer meio ou formato) e adaptação (remix, transformação e criação de material a partir do conteúdo assim licenciado para quaisquer fins, inclusive comerciais.
Recomenda-se a leitura desse link para maiores informações sobre o tema: fornecimento de créditos e referências de forma correta, entre outros detalhes cruciais para uso adequado do material licenciado.