Rol de los brasinoesteroides en frutales con énfasis en condiciones de estrés abiótico: Una revisión
Resumen
El cambio climático puede causar eventos de estrés en los cultivos, principalmente por los cambios generados sobre la precipitación y la temperatura. Dentro de los cultivos que se ven afectados se encuentran los frutales, un grupo de especies de gran importancia por su valor nutritivo en la dieta humana. Estas especies se pueden ver afectados por condiciones de estrés abiótico debido a cambios en la disponibilidad hídrica, la temperatura y la radiación. Por esta razón se han generado distintas alternativas que podrían mitigar dicha afectación, como la aplicación exógena de brasinoesteroides (BR). Los BR desempeñan un papel importante en el crecimiento y desarrollo de las plantas, además está involucrado en la respuesta de las plantas al estrés abiótico por medio de la regulación en la concentración de solutos, apertura estomática, protección del aparato fotosintético y el aumento de la capacidad antioxidante, principalmente. Este artículo de revisión busca sintetizar el papel de los brasinoesteroides en el crecimiento y desarrollo de los frutales, así como la función que desempeñan en la respuesta a condiciones de estrés abiótico, expresión génica y balance hormonal.
Palabras clave
Cambio climático, Estrés oxidativo, Fotosíntesis, Regulación génica, Fisiología vegetal
Citas
- Ahammed, G. J., Li, X., Liu, A., & Chen, S. (2020). Brassinosteroids in plant tolerance to abiotic stress. Journal of Plant Growth Regulation, 39(4), 1451-1464. https://doi.org/10.1007/s00344-020-10098-0
- Ahammed, G. J., Ruan, Y. P., Zhou, J., Xia, X. J., Shi, K., Zhou, Y. H., & Yu, J. Q. (2013). Brassinosteroid alleviates polychlorinated biphenyls-induced oxidative stress by enhancing antioxidant enzymes activity in tomato. Chemosphere, 90(11), 2645-2653. https://doi.org/10.1016/j.chemosphere.2012.11.041
- Ali, B. (2017). Practical applications of brassinosteroids in horticulture—some field perspectives. Scientia Horticulturae, 225, 15-21. https://doi.org/10.1016/j.scienta.2017.06.051
- Aly, M. A., Ezz, T. M., Mahmoud, G., & Khadeejah, H. N. (2021). Effect of some Growth Regulators on Productivity, Fruit Quality and Storability of Sugar Apple Anona squamosa, L. Nveo-natural volatiles & essential oils Journal| NVEO, 12298-12316
- Anjum, S. A., Xie, X. Y., Wang, L. C., Saleem, M. F., Man, C., & Lei, W. (2011). Morphological, physiological and biochemical responses of plants to drought stress. African journal of agricultural research, 6(9), 2026-2032. https://doi.org/10.5897/AJAR10.027
- Arantes, M. B. D. S., Marinho, C. S., Gomes, M. D. M. D. A., Santos, R. F. D., Galvão, S. P., & Vaz, G. P. (2021). Brassinosteroid accelerates the growth of Psidium hybrid during acclimatization of seedlings obtained from minicuttings. Pesquisa Agropecuária Tropical, 50, e64743. https://doi.org/10.1590/1983-40632020v5064743
- Arunanondchai, P., Fei, C., Fisher, A., McCarl, B. A., Wang, W., & Yang, Y. (2018). How does climate change affect agriculture? (pp. 191-210). Abingdon-on-Thames, UK: Routledge. https://doi.org/10.4324/9781315623351
- Caño-Delgado, A., Yin, Y., Yu, C., Vafeados, D., Mora-García, S., Cheng, J. C., ... & Chory, J. (2004). BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development, 131 (21), 5341–5351 https://doi.org/10.1242/dev.01403
- Cao, X., Khaliq, A., Lu, S., Xie, M., Ma, Z., Mao, J., & Chen, B. (2020). Genome‐wide identification and characterization of the BES1 gene family in apple (Malus domestica). Plant Biology, 22(4), 723–733. https://doi.org/10.1111/plb.13109
- Castañeda-Murillo, C. C., Rojas-Ortiz, J. G., Sánchez-Reinoso, A. D., Chávez-Arias, C. C., & Restrepo-Díaz, H. (2022). Foliar brassinosteroid analogue (DI-31) sprays increase drought tolerance by improving plant growth and photosynthetic efficiency in lulo plants. Heliyon, 8(2), e08977. https://doi.org/10.1016/j.heliyon.2022.e08977
- Champa, WH, Gill M, Mahajan B, Aror N, Bedi S (2015) Brassinosteroids improve quality of table grapes (Vitis vinifera L.) cv. fame seedless. Trop Agric Res 26, 368–379 http://doi.org/10.4038/tar.v26i2.8099
- Chaudhry, S., & Sidhu, G. P. S. (2021). Climate change regulated abiotic stress mechanisms in plants: a comprehensive review. Plant Cell Reports, 41, 1-31. https://doi.org/10.1007/s00299-021-02759-5
- Chen, Z. Y., Wang, Y. T., Pan, X. B., & Xi, Z. M. (2019). Amelioration of cold-induced oxidative stress by exogenous 24-epibrassinolide treatment in grapevine seedlings: toward regulating the ascorbate–glutathione cycle. Scientia Horticulturae, 244, 379-387. https://doi.org/10.1016/j.scienta.2018.09.062
- Damghan, I. R. (2009). Exogenous application of brassinosteroid alleviates drought-induced oxidative stress in Lycopersicon esculentum L. Gen. Appl. Plant Physiol, 35, 22-34.
- Eid, F. S., El-Kholy, M. F., & Hosny, S. S. (2016). Effect of Foliar Sprays Application of Milagrow on Yield and Fruit Quality of Avocado Tree cv. Journal of Plant Production, 7(12), 1495-1499. https://doi.org/10.21608/JPP.2016.47106
- Fang, P., Yan, M., Chi, C., Wang, M., Zhou, Y., Zhou, J., ... & Yu, J. (2019). Brassinosteroids act as a positive regulator of photoprotection in response to chilling stress. Plant physiology, 180(4), 2061-2076. https://doi.org/10.1104/pp.19.00088
- Furlan, V., & Garramuño, M. P. (2022). Yo las espero todo el año... Las frutas cultivadas por mujeres en jardines domésticos. Sus aportes a la diversidad alimentaria y nutricional en Puerto Iguazú, Argentina. Boletim Do Museu Paraense Emílio Goeldi. Ciências Humanas, 17(1), e20200092. https://doi.org/10.1590/2178-2547-BGOELDI-2020-0092
- Gomes, M. D. M. A., Campostrini, E., Leal, N. R., Viana, A. P., Ferraz, T. M., do Nascimento Siqueira, L., ... & Zullo, M. A. T. (2006). Brassinosteroid analogue effects on the yield of yellow passion fruit plants (Passiflora edulis f. flavicarpa). Scientia Horticulturae, 110(3), 235-240. https://doi.org/10.1016/j.scienta.2006.06.030
- Goraya, G. K., Kaur, B., Asthir, B., Bala, S., Kaur, G., & Farooq, M. (2017). Rapid injuries of high temperature in plants. Journal of Plant Biology, 60(4), 298-305. https://doi.org/10.1007/s12374-016-0365-0
- Gou, X., Yin, H., He, K., Du, J., Yi, J., Xu, S., ... & Li, J. (2012). Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS genetics, 8(1), e1002452. https://doi.org/10.1371/journal.pgen.1002452
- Hassan, H., Amin, M., Rajwana, I. A., Ullah, S., Razzaq, K., Faried, H. N., Akhtar, G., Naeem-Ullah, U., Qayyum, M. A., Aslam, M. M., Ali, K., Asghar, Z., Nayab, S., Naz, A., & Sahar, H. W. (2022). Nutritional functions and antioxidative enzymes in juice extract from two different maturity stages of low temperature stored phalsa (Grewia subinaequalis D.C.) fruit. LWT, 153, 112552. https://doi.org/10.1016/j.lwt.2021.112552
- He, Z. , Wang, Z.Y. , Li, J. , Zhu, Q. , Lamb, C. , Ronald, P. , Chory, J. (2000). Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288, 2360–2363 https://doi.org/10.1126/science.288.5475.2360
- Helaly, M. N., El-Hoseiny, H. M., Elsheery, N. I., Kalaji, H. M., de Los Santos-Villalobos, S., Wróbel, J., ... & Alam-Eldein, S. M. (2022). 5-aminolevulinic acid and 24-epibrassinolide improve the drought stress resilience and productivity of banana plants. Plants, 11(6), 743. https://doi.org/10.3390/plants11060743
- Hernández, I., Uarrota, V., Fuentealba, C., Paredes, D., Defilippi, B. G., Campos-Vargas, R., Nuñez, G., Carrera, E., Meneses, C., Hertog, M., & Pedreschi, R. (2022). Transcriptome and hormone analyses reveals differences in physiological age of ′Hass′ avocado fruit. Postharvest Biology and Technology, 185, 111806. https://doi.org/10.1016/j.postharvbio.2021.111806
- Holá, D. (2011). Brassinosteroids and photosynthesis. In: Hayat, S., Ahmad, A. (eds) Brassinosteroids: A Class of Plant Hormone. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0189-2
- Hu, C., Zheng, Y., Tong, C., & Zhang, D. (2022). Effects of exogenous melatonin on plant growth, root hormones and photosynthetic characteristics of trifoliate orange subjected to salt stress. Plant Growth Regulation, 97, 551–558. https://doi.org/10.1007/s10725-022-00814-z
- Hu, S., Ding, Y., and Zhu, C. (2020). Sensitivity and responses of Chloroplasts to heat stress in plants. Front. Plant Sci. 11, 375. https://doi.org/10.3389/fpls.2020.00375
- Islam, M., Ali, S., Nawaz, A., Naz, S., Ejaz, S., Shah, A. A., & Razzaq, K. (2022). Postharvest 24-epibrassinolide treatment alleviates pomegranate fruit chilling injury by regulating proline metabolism and antioxidant activities. Postharvest Biology and Technology, 188, 111906. https://doi.org/10.1016/j.postharvbio.2022.111906
- Karlidag, H., Yildirim, E., & Turan, M. (2011). Role of 24-epibrassinolide in mitigating the adverse effects of salt stress on stomatal conductance, membrane permeability, and leaf water content, ionic composition in salt stressed strawberry (Fragaria× ananassa). Scientia horticulturae, 130(1), 133-140. https://doi.org/10.1016/j.scienta.2011.06.025
- Khatoon, F., Kundu, M., Mir, H., & Nahakpam, S. (2021). Efficacy of foliar feeding of brassinosteroid to improve growth, yield and fruit quality of strawberry (Fragaria× ananassa Duch.) grown under subtropical plain. Communications in Soil Science and Plant Analysis, 52(8), 803-814. https://doi.org/10.1080/00103624.2020.1869765
- Kinoshita, T. , Caño-Delgado, A. , Seto, H. , Hiranuma, S. , Fujioka, S. , Yoshida, S. , Chory, J. (2005). Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433, 167–171. https://doi.org/10.1038/nature03227
- Krishna, P., Prasad, B. D., & Rahman, T. (2017). Brassinosteroid action in plant abiotic stress tolerance. In Brassinosteroids (pp. 193-202). Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6813-8_16
- Kumari, S., & Thakur, A. (2019a). Morphological and Physio-biochemical Changes in Response to Foliar Application of Brassinosteroid and Water Stress in Apple Plants Under Pot Culture Study. International Journal of Bio-resource and Stress Management, 10(1), 39-45. https://doi.org/10.23910/IJBSM/2019.10.1.1944
- Kumari, S., & Thakur, A. (2019b). The Effects of Water Stress and Brassinosteroid on Apple Varieties. International Journal of Economic Plants, 6(1), 1-6. https://doi.org/10.23910/IJEP/2019.6.1.0278
- Kumari, S., Thakur, A., Singh, N., Chandel, J. S., & Rana, N. (2020). Influence of drought stress and brassinosteroid on growth and physio-biochemical characteristics of apple plants. Indian Journal of Horticulture, 77(1), 88-93. https://doi.org/10.5958/0974-0112.2020.00007.9
- Li, B. B., Fu, Y. S., Li, X. X., Yin, H. N., & Xi, Z. M. (2022a). Brassinosteroids alleviate cadmium phytotoxicity by minimizing oxidative stress in grape seedlings: Toward regulating the ascorbate-glutathione cycle. Scientia Horticulturae, 299, 111002. https://doi.org/10.1016/j.scienta.2022.111002
- Li, N., Euring, D., Cha, J. Y., Lin, Z., Lu, M., Huang, L. J., & Kim, W. Y. (2021a). Plant hormone-mediated regulation of heat tolerance in response to global climate change. Frontiers in Plant Science, 11, 2318. https://doi.org/10.3389/fpls.2020.627969
- Li, S., Zheng, H., Lin, L., Wang, F., & Sui, N. (2021b). Roles of brassinosteroids in plant growth and abiotic stress response. Plant Growth Regulation, 93(1), 29-38. https://doi.org/10.1007/s10725-020-00672-7
- Li, T., Shi, Y., Zhu, B., Zhang, T., Feng, Z., Wang, X., Li, X., & You, C. (2022b). Genome-Wide Identification of Apple Atypical bHLH Subfamily PRE Members and Functional Characterization of MdPRE4.3 in Response to Abiotic Stress. Frontiers in Genetics, 13, 13, 846559. https://doi.org/10.3389/fgene.2022.846559
- Liao, Z., Dong, F., Liu, J., Xu, L., Marshall-Colon, A., & Ming, R. (2022). Gene regulation network analyses of pistil development in papaya. BMC Genomics, 23(1), 8. https://doi.org/10.1186/s12864-021-08197-7
- Lippmann, R., Babben, S., Menger, A., Delker, C., and Quint, M. (2019). Development of wild and cultivated plants under global warming conditions. Curr. Biol. 29, R1326–R1338. https://doi.org/10.1016/j.cub.2019.10.016
- Liu, Y.-J., An, J.-P., Wang, X.-F., Gao, N., Wang, X., Zhang, S., Gao, W.-S., Hao, Y.-J., & You, C.-X. (2021). MdBZR1 regulates ABA response by modulating the expression of MdABI5 in apple. Plant Cell Reports, 40(7), 1127–1139. https://doi.org/10.1007/s00299-021-02692-7
- Mao, J., Zhang, D., Li, K., Liu, Z., Liu, X., Song, C., ... & Han, M. (2017). Effect of exogenous Brassinolide (BR) application on the morphology, hormone status, and gene expression of developing lateral roots in Malus hupehensis. Plant Growth Regulation, 82(3), 391-401. https://doi.org/10.1007/s10725-017-0264-5
- Market Data Forecast (2021). Global Processed Superfruits Market. https://www. marketdataforecast.com/market-reports/processed-superfruits-market (Último acceso Junio 2022).
- Mostafa, L. Y., & Kotb, H. R. (2018). Effect of brassinosteroids and gibberellic acid on parthenocarpic fruit formation and fruit quality of sugar apple Annona squamosa L. Middle East J, 7(4), 1341-1351.
- Mutum, B., Maity, U., Basak, S., Laya, B., & Singh, S. D. (2018). Effect of Plant Growth Regulator on Flowering and Yield Attributes of Papaya. Biological Forum. 13(3), 627-630
- Nolan, T. M., Vukašinović, N., Liu, D., Russinova, E., & Yin, Y. (2019). Brassinosteroids: multidimensional regulators of plant growth, development, and stress responses. The Plant Cell, 32(2), 295-318. https://doi.org/10.1105/tpc.19.00335
- Nolan, T., Chen, J., & Yin, Y. (2017). Cross-talk of Brassinosteroid signaling in controlling growth and stress responses. Biochemical Journal, 474(16), 2641-2661. https://doi.org/10.1042/BCJ20160633
- Ogweno, J. O., Song, X. S., Shi, K., Hu, W. H., Mao, W. H., Zhou, Y. H., ... & Nogués, S. (2008). Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. Journal of Plant Growth Regulation, 27(1), 49-57. https://doi.org/10.1007/s00344-007-9030-7
- Pino, M. T., Mc Leod B., C., Domínguez D., E., Zamora V., O., Álvarez M., F., Águila M., K., & Pérez Díaz, R. (2022). Potencial de frutales nativos chilenos como fuente de antioxidantes y colorantes. In M. Teresa Pino & C. Vergara H. (Eds.), Colorantes y antioxidantes naturales en la industria de alimentos: tecnologías de extracción y materias primas dedicadas. 455, 159–184. INIA.
- Planas-Riverola, A., Gupta, A., Betegón-Putze, I., Bosch, N., Ibañes, M., & Caño-Delgado, A. I. (2019). Brassinosteroid signaling in plant development and adaptation to stress. Development, 146(5), dev151894. https://doi.org/10.1242/dev.151894
- Primo-Capella, A., Forner-Giner, M. Á., Martínez-Cuenca, M.-R., & Terol, J. (2022). Comparative transcriptomic analyses of citrus cold-resistant vs. sensitive rootstocks might suggest a relevant role of ABA signaling in triggering cold scion adaption. BMC Plant Biology, 22(1), 209. https://doi.org.org/10.1186/s12870-022-03578-w
- Raza, A., Razzaq, A., Mehmood, S. S., Zou, X., Zhang, X., Lv, Y., & Xu, J. (2019). Impact of climate change on crops adaptation and strategies to tackle its outcome: A review. Plants, 8(2), 34. https://doi.org/10.3390/plants8020034
- Squeri, C., Miras-Moreno, B., Gatti, M., Garavani, A., Poni, S., Lucini, L., & Trevisan, M. (2021). Gas exchange, vine performance and modulation of secondary metabolism in Vitis vinifera L. cv Barbera following long-term nitrogen deficit. Planta, 253(3), 73. https://doi.org.org/10.1007/s00425-021-03590-8
- Su, M., Wang, S., Liu, W., Yang, M., Zhang, Z., Wang, N., & Chen, X. (2022). MdJa2 Participates in the Brassinosteroid Signaling Pathway to Regulate the Synthesis of Anthocyanin and Proanthocyanidin in Red-Fleshed Apple. Frontiers in Plant Science, 13, 1-13. https://doi.org/10.3389/fpls.2022.830349
- Sun, S., Lin, M., Qi, X., Chen, J., Gu, H., Zhong, Y., Sun, L., Muhammad, A., Bai, D., Hu, C., & Fang, J. (2021). Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances. BMC Plant Biology, 21(1), 365. https://doi.org.org/10.1186/s12870-021-03152-w
- Sun, Y., Fan, X. Y., Cao, D. M., Tang, W., He, K., Zhu, J. Y., ... & Wang, Z. Y. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental cell, 19(5), 765-777. https://doi.org/10.1016/j.devcel.2010.10.010
- Suprasanna, P. (2020). Plant abiotic stress tolerance: Insights into resilience build-up. Journal of Biosciences, 45(1), 1-8. https://doi.org/10.1007/s12038-020-00088-5
- Symons, G. M., Davies, C., Shavrukov, Y., Dry, I. B., Reid, J. B., & Thomas, M. R. (2006). Grapes on steroids. Brassinosteroids are involved in grape berry ripening. Plant physiology, 140(1), 150-158. https://doi.org/10.1104/pp.105.070706
- Vega, M., Meza, B., Solórzano, J., & Macías, E. (2022). La seguridad alimentaria como instrumento para reducir la desnutrición crónica infantil en Ecuador. Una revisión. Memorias Sucre Review, 2(1), 385–404. https://doi.org/10.37117/s.v21i1.450
- Vergara, A., Torrealba, M., Alcalde, J. A., & Pérez‐Donoso, A. G. (2020). Commercial brassinosteroid increases the concentration of anthocyanin in red tablegrape cultivars (Vitis vinifera L.). Australian Journal of Grape and Wine Research, 26(4), 427-433. https://doi.org/10.1111/ajgw.12457
- Wang, X., Gao, Y., Wang, Q., Chen, M., Ye, X., Li, D. & Gao, D. (2019a). 24-Epibrassinolide-alleviated drought stress damage influences antioxidant enzymes and autophagy changes in peach (Prunus persicae L.) leaves. Plant Physiology and Biochemistry, 135, 30-40. https://doi.org/10.1016/j.plaphy.2018.11.026
- Wang, Y. T., Chen, Z. Y., Jiang, Y., Duan, B. B., & Xi, Z. M. (2019b). Involvement of ABA and antioxidant system in brassinosteroid-induced water stress tolerance of grapevine (Vitis vinifera L.). Scientia Horticulturae, 256, 108596. https://doi.org/10.1016/j.scienta.2019.108596
- Wu, Z., Gu, S., Gu, H., Cheng, D., Li, L., Guo, X., ... & Chen, J. (2022). Physiological and transcriptomic analyses of brassinosteroid function in kiwifruit root. Environmental and Experimental Botany, 194, 104685. https://doi.org/10.1016/j.envexpbot.2021.104685
- Xia, H., Liu, X., Wang, Y., Lin, Z., Deng, H., Wang, J. & Liang, D. (2022). 24-Epibrassinolide and nitric oxide combined to improve the drought tolerance in kiwifruit seedlings by proline pathway and nitrogen metabolism. Scientia Horticulturae, 297, 110929. https://doi.org/10.1016/j.scienta.2022.110929
- Yan, T., Mei, C., Song, H., Shan, D., Sun, Y., Hu, Z., Wang, L., Zhang, T., Wang, J., & Kong, J. (2022). Potential roles of melatonin and ABA on apple dwarfing in semi-arid area of Xinjiang China. PeerJ, 10, e13008. https://doi.org/10.7717/peerj.13008
- Yuan, L., Yuan, Y., Du, J., Sun, J., & Guo, S. (2012). Effects of 24-epibrassinolide on nitrogen metabolism in cucumber seedlings under Ca (NO3)2 stress. Plant Physiology and Biochemistry, 61, 29-35. https://doi.org/10.1016/j.plaphy.2012.09.004
- Zeng, G., Gao, F., Li, C., Li, D., & Xi, Z. (2022). Characterization of 24-epibrassinolide-mediated modulation of the drought stress responses: Morphophysiology, antioxidant metabolism and hormones in grapevine (Vitis vinifera L.). Plant Physiology and Biochemistry, 184. 98-111. https://doi.org/10.1016/j.plaphy.2022.05.019
- Zhang, F., Ji, S., Wei, B., Cheng, S., Wang, Y., Hao, J., Wang, S., & Zhou, Q. (2020). Transcriptome analysis of postharvest blueberries (Vaccinium corymbosum ‘Duke’) in response to cold stress. BMC Plant Biology, 20(1), 80. https://doi.org/10.1186/s12870-020-2281-1
- Zhang, P., Zuo, Q., Jin, H., Pervaiz, T., Dong, T., Pei, D., Ren, Y., Jia, H., & Fang, J. (2022). Role of SnRK2s in grape berry development and stress response. Scientia Horticulturae, 302, 111175. https://doi.org/10.1016/j.scienta.2022.111175
- Zheng, J., An, Y., & Wang, L. (2018). 24-Epibrassinolide enhances 5-ALA-induced anthocyanin and flavonol accumulation in calli of ‘Fuji’ apple flesh. Plant Cell, Tissue and Organ Culture (PCTOC), 134(2), 319–330. https://doi.org/10.1007/s11240-018-1418-5
- Zhu, F., Yun, Z., Ma, Q., Gong, Q., Zeng, Y., Xu, J., Cheng, Y., Deng, X. (2015). Effects of exogenous 24-epibrassinolide treatment on postharvest quality and resistance of Satsuma mandarin (Citrus unshiu), Postharvest Biology and Technology, 100, (8-15). https://doi.org/10.1016/j.postharvbio.2014.09.014.