Incremento de la prolina por la aplicación del bioestimulante CBX-103 mejora el crecimiento de Arabidopsis thaliana Col 0 bajo condiciones de estrés salino

Fresia  Mejía; Gustavo  Sandoval; Juan  Lucar

doi:10.17268/agroind.sci.2024.01.04

Authors

Fresia Mejía Biogen Agro SAC. Departamento de Investigación y Desarrollo. Lima, Perú https://orcid.org/0000-0003-0090-7609
Gustavo Sandoval Universidad Nacional Mayor de San Marcos. Facultad de Ciencias Biológicas. Grupo de Investigación en Bioinformática y Biología Estructural. Lima, Perú https://orcid.org/0000-0002-8392-9880
Juan Lucar Biogen Agro SAC. Departamento de Investigación y Desarrollo. Lima, Perú https://orcid.org/0009-0009-1064-5359

DOI:

https://doi.org/10.17268/agroind.sci.2024.01.04

Keywords:

Arabidopsis thaliana Col 0, bioestimulant CBX-103, carboxylic acids, proline, salt stress

Abstract

Agriculture faces new, increasingly complicated challenges in the face of a constantly changing environment that causes different types of stress in crops, one of them being salinity. Numerous investigations have been carried out to understand the effect of salt stress on the physiology of plants, as well as different ways of dealing with it and creating tolerance and/or resistance so that the productivity of crops is not affected. Among these alternatives we find biostimulants. The biostimulant CBX-103 is composed of carboxylic acids, succinic acids, oligogalacturonides, among others, which are obtained through a controlled enzymatic fermentation of the plant extract of Saccharum officinarum L. In the present study it is demonstrated that foliar applications of the biostimulant CBX- 103 in Arabidopsis thaliana Col 0 plants grown under salt stress increase leaf proline content, significantly reducing the harmful effects of stress, which is demonstrated at a biometric level and regulating growth states. A pathway in the energy regulation of plants is proposed as a mode of action due to the increase in the accumulation of proline obtained and the effect of its components.

References

Acosta, D. L., Menéndez, D. C., & Rodríguez, A. F. (2018). Los oligogalacturónidos en el crecimiento y desarrollo de las plantas. Cultivos Tropicales, 39(2), 127-134.

Almanza-Merchán, P. J., Tovar-León, Y. P., & Velandia-Díaz, J. D. (2016). Comportamiento de la biomasa y de las tasas de crecimiento de dos variedades de lulo (Solanum quitoense Lam.) en Pachavita, Boyacá. Ciencia y Agricultura, 13(1), 67-76.

Alharby, H .F., Al-Zahrani, H. S., Hakeem, K. R., Alsamadany, H., Desoky, E.-S. M.; Rady, M.M. (2021). Silymarin-Enriched Biostimulant Foliar Application Minimizes the Toxicity of Cadmium in Maize by Suppressing Oxidative Stress and Elevating Antioxidant Gene Expression. Biomolecules, 11, 465. https://doi.org/10.3390/biom11030465

Aswani, V., Rajsheel, P., Bapatla, R. B., Sunil, B., & Raghavendra, A. S. (2019). Oxidative stress induced in chloroplasts or mitochondria promotes proline accumulation in leaves of pea (Pisum sativum): another example of chloroplast-mitochondria interactions. Protoplasma, 256, 449-457. https://doi.org/10.1007/s00709-018-1306-1

Bates, L. S., Walden, R. P., & Tear, G. D. (1973). Rapid determination of free proline for water stress studies. Plant Soil, 39, 205–210. https://doi.org/10.1007/BF00018060

Bedoya-Perales N., Maus D., Neimaier A., Escobedo-Pacheco E., Pumi G. (2023). Assessment of the variation of heavy metals and pesticide residues in native and modern potato (Solanum tuberosum L.) cultivars grown at different altitudes in a typical mining region in Peru. Toxicology Reports, 11, 23-34. https://doi.org/10.1016/j.toxrep.2023.06.005

Bertrand, H., Nalin, R., Bally, R., & Cleyet-Marel, J. C. (2001). Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biology and fertility of soils, 33, 152-156. https://doi.org/10.1007/s003740000305

Boyes, D. C., Zayed, A. M., Ascenzi, R., McCaskill, A. J., Hoffman, N. E., Davis, K. R., & Görlach, J. (2001). Growth stage-based phenotypic analysis of Arabidopsis: A model for high throughput functional genomics in plants. Plant Cell, 13(7), 1499–1510. https://doi.org/10.1105/tpc.13.7.1499

Costales, D., Martínez, L., & Núñez, M. (2007). Efecto del tratamiento de semillas con una mezcla de oligogalacturónidos sobre el crecimiento de plántulas de tomate (Lycopersicon esculentum Mill.). Cultivos Tropicales, 28(1), 85-91.

Dagar, J. C., Yadav, R. K., & Sharma, P. C. (2019). Research Developments in Saline Agriculture. Salinity Tolerance Indicators. 10.1007/978-981-13-5832-6 (Chapter 5), 155–201. https://doi.org/10.1007/978-981-13-5832-6_5

Desoky, E. -S. M., Elrys, A. S., Mansour, E., Eid, R. S. M., Selem, E., Rady, M. M., Ali, E. F., Mersal, G. A. M., & Semida, W. M. (2021). Application of biostimulants promotes growth and productivity by fortifying the antioxidant machinery and suppressing oxidative stress in faba bean under various abiotic stresses. Scientia Horticulturae, 288, 110340. https://doi.org/10.1016/j.scienta.2021.110340

Dwiningsih, Y., Kumar, A., Thomas, J., Ruiz, C., Alkahtani, J., Baisakh, N., & Pereira, A. (2021). Quantitative trait loci and candidate gene identification for chlorophyll content in RIL rice population under drought conditions. Indonesian Journal of Natural Pigments, 3(2), 54-64. http://doi.org/10.33479/ijnp.2021.03.2.54

Figueroa, L., & Neaman, A. (2023). Salinos, pero ácidos: una extraña combinación en suelos del valle de Lluta en el norte de Chile. Idesia (Arica), 41(1), 133-137. https://dx.doi.org/10.4067/S0718-34292023000100133

Gardner, F. P., Pearce, R. B., & Mitchell, R. L. (2017). Physiology of crop plants. Scientific publishers.

Ghosh, U. K., Islam, M. N., Siddiqui, M. N., Cao, X., & Khan, M. A. R. (2022). Proline, a multifaceted signalling molecule in plant responses to abiotic stress: understanding the physiological mechanisms. Plant Biology, 24(2), 227-239. https://doi.org/10.1111/plb.13363

Gupta, A., Rai, S., Bano, A., Khanam, A., Sharma, S., Pathak, N. (2021). Comparative evaluation of different salt tolerant plant growth promoting bacterial isolates in mitigating the induced adverse effect of salinity in Pisum sativum. Biointerface Research in Applied Chemistry, 11(5), 13141–13154. https://doi.org/10.33263/BRIAC115.1314113154

Hadavi, E., & Ghazijahani, N. (2022). Simple Organic Acids as Plant Biostimulants. In Biostimulants: Exploring Sources and Applications. Singapore: Springer Nature Singapore, 71–105. https://doi.org/10.1007/978-981-16-7080-0_4

Hameed, A., Ahmed, M. Z., Hussain, T., Aziz, I., Ahmad, N., Gul, B., & Nielsen, B. L. (2021). Effects of salinity stress on chloroplast structure and function. Cells, 10(8), 2023. https://doi.org/10.3390/cells10082023

Hess, M., Barralis, G., Bleiholder, H., Buhr, L., Eggers, T. H., Hack, H., & Stauss, R. (1997). Use of the extended BBCH scale—general for the descriptions of the growth stages of mono, and dicotyledonous weed species. Weed research, 37(6), 433-441. https://doi.org/10.1046/j.1365-3180.1997.d01-70.x

Hunt, R. (1982). Plant growth curves. The functional approach to plant growth analysis. Edward Arnold Ltd.

Jiménez-Vázquez, K. R., García-Cárdenas, E., Barrera-Ortiz, S., Ortiz-Castro, R., Ruiz-Herrera, L. F., Ramos-Acosta, B. P., Coria-Arellano, J. L., Sáenz-Mata, J., & López-Bucio, J. (2020). The plant beneficial Rhizobacterium achromobacter sp. 5B1 influences root development through auxin signaling and redistribution. Plant Journal, 103(5). https://doi.org/10.1111/tpj.14853

Lynch J. (1995). Root architecture and plant productivity. Plant Physiol.,109(1), 7-13. https://doi.org/10.1104/pp.109.1.7

Mayén-Villa, R. I., Morales-Rosales, E. J., Morales-Morales, E. J., & López-Sandoval, J. A. (2023). Rendimiento de tomate (Solanum lycopersicum) en función de fosfito de potasio como fertilizante foliar. Ecosistemas y recursos agropecuarios, 10(2). https://doi.org/10.19136/era.a10n2.3543

Monshausen, G. B., & Gilroy, S. (2009). The exploring root–root growth responses to local environmental conditions. Curr Opin Plant Biol., 12, 766-772. https://doi.org/10.1016/j.pbi.2009.08.002

Morton, M. J. L., Awlia, M., Al-Tamimi, N., Saade, S., Pailles, Y., Negrão, S., & Tester, M. (2019). Salt stress under the scalpel – Dissecting the genetics of salt tolerance. Plant J., 97, 148–163. https://doi.org/10.1111/tpj.14189

Ordoñez, J. C., Van Bodegom, P. M., Witte, J. P. M., Wright, I. J., Reich, P. B., & Aerts, R. (2009). A global study of relationships between leaf traits, climate and soil measures of nutrient fertility. Global Ecology and Biogeography, 18(2), 137-149. https://doi.org/10.1111/j.1466-8238.2008.00441.x

Orsini, F., Pennisi, G., Mancarella, S., Al Nayef, M., Sanoubar, R., Nicola, S., & Gianquinto, G. (2018). Hydroponic lettuce yields are improved under salt stress by utilizing white plastic film and exogenous applications of proline. Sci. Hortic., 233, 283–293. https://doi.org/10.1111/j.1466-8238.2008.00441.x

Passioura, J. B. (2002). Environmental biology and crop improvement. Functional Plant Biology, 29(5), 537-546. https://doi.org/10.1071/FP02020

Pereira, E. G., Amaral, M. B., Bucher, C. A., Santos, L. A., Fernandes, M. S., & Rossetto, C. A. V. (2021). Proline osmopriming improves the root architecture, nitrogen content and growth of rice seedlings. Biocatalysis and Agricultural Biotechnology, 33,101998. https://doi.org/10.1016/j.bcab.2021.101998

Poorter, H. (1989). Plant growth analysis: towards a synthesis of the classical and the functional approach. Physiologia Plantarum, 75(3), 237-244. https://doi.org/10.1111/j.1399-3054.1989.tb06175.x

Poorter, H., & Garnier, E. (1996). Plant growth analysis: an evaluation of experimental design and computational methods. Journal of Experimental Botany, 47(9), 1343-1351. https://doi.org/10.1093/jxb/47.9.1343

Poorter, H., & Sack, L. (2012). Pitfalls and possibilities in the analysis of biomass allocation patterns in plants. Frontiers in Plant Science, 3(259), 1-10. https://doi.org/10.3389/fpls.2012.00259

Porra, R. J., Thompson, W. A., & Kriedemann, P. E. (1989). Determi-nation of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll II standards by atomic absorption spectroscopy. Biochim Biophys Acta, 975(3), 384–394. https://doi.org/10.1016/S0005-2728(89)80347-0

Radford, P. (1967). Growth analysis formulae. Their use and abuse. Crop Sci, 7(3), 171 - 175. https://doi.org/10.2135/cropsci1967.0011183X000700030001x

Reyes-Pérez, J. J., Ramos-Remache, R. A., Llerena-Ramos, L. T., Ramírez-Arrebato, M. Á., & Falcón-Rodríguez, A. B. (2021). Potentialities of oligogalacturonides and chitosaccharides on plant rooting. Terra Latinoamericana, 39.

Rolly, N. K., Imran, Q. M., Lee, I. J., & Yun, B. W. (2020). Salinity stress‐mediated suppression of expression of salt overly sensitive signaling pathway genes suggests negative regulation by AtbZIP62 transcription factor in Arabidopsis thaliana. International Journal of Molecular Sciences, 21(5), 1–17. https://doi.org/10.3390/ijms21051726

Sahi, C., Singh, A., & Kumar, K. (2006). Salt stress response in rice: genetics, molecular biology and comparative genomics. Funct. Integr. Genomics, 6, 263–284. https://doi.org/10.1007/s10142-006-0032-5

Scaglia, B., Pognani, M., & Adani, F. (2017). The anaerobic digestion process capability to produce biostimulant: the case study of the dissolved organic matter (DOM) vs. auxin-like property. Science of The Total Environment, 589, 36-45, https://doi.org/10.1016/j.scitotenv.2017.02.223

Shahid, S. A., Zaman, M., & Heng, L. (2018). Soil Salinity: Historical Perspectives and a World Overview of the Problem. In: Guideline for Salinity Assessment, Mitigation and Adaptation Using Nuclear and Related Techniques, Springer, Cham., 43–53. https://doi.org/10.1007/978-3-319-96190-3_2

Sekhar, P. N., Amrutha, R. N., Sangam, S., Verma, D. P. S., & Kishor, P. K. (2007). Biochemical characterization, homology modeling and docking studies of ornithine δ-aminotransferase—an important enzyme in proline biosynthesis of plants. Journal of Molecular Graphics and Modelling, 26(4), 709-719. https://doi.org/10.1016/j.jmgm.2007.04.006

Singh, R. P., Prakash, S., Bhatia, R., Negi, M., Singh, J., Bishnoi, M., & Kondepudi, K. K. (2020). Generation of structurally diverse pectin oligosaccharides having prebiotic attributes. Food Hydrocolloids, 108, 105988. https://doi.org/10.1016/j.foodhyd.2020.105988

Sivakumar, M. V. K., & Shaw, R. H. (1978). Methods of growth analysis in field-grown soya beans (Glicine max L.). Merril. Ann. Bot., 42(1), 213 - 222. https://doi.org/10.1093/oxfordjournals.aob.a085442

Souza, C. R., de Mello, A., Antunes, P., de Araújo Bitencourt, J., Sampaio, I., Carneiro, P. L. (2017). Species validation and cryptic diversity in the Geophagus brasiliensis Quoy & Gaimard, 1824 complex (Teleostei, Cichlidae) from Brazilian coastal basins as revealed by DNA analyses. Hydrobiologia, 809, 309-321. https://doi.org/10.1007/s10750-017-3482-y

Tuteja, N. (2007). Mechanisms of high salinity tolerance in plants. Methods Enzymol., 428, 419-438. https://doi.org/10.1016/S0076-6879(07)28024-3

Uddin, Md., & Juraimi, A. (2013). Salinity Tolerance Turfgrass: History and Prospects. The Scientific World Journal. 409413. https://doi.org/10.1155/2013/409413

Wani, A., Ahmad, A., Hayat, S., Tahir, I. (2016). Is foliar spray of proline sufficient for mitigation of salt stress in Brassica juncea cultivars?. Environ. Sci. Pollut. Res., 23, 13413–13423. https://doi.org/10.1007/s11356-016-6533-4

Yang, Y., & Guo, Y. (2018). Elucidating the molecular mechanisms mediating plant salt stress responses. New Phytol., 217, 523–539. https://doi.org/10.1111/nph.14920

Yildirim, E., Turan, M., & Donmez, M. F. (2008) Mitigation of salt stress in radish (Raphanus sativus L.) by plant growth: Promoting rhizobacteria. Romanian Biotechnological Letters, 86(3), 52-62.