Biochemical and enzymatic alterations of watermelon associated with irrigation management and inoculation with Rhizobacteria

Mycaella Gonçalves de Araújo; Alessandro Carlos Mesquita; Welson Lima Simões; Raquel Nunes de Carvalho; Ana Thaila Rodrigues Felix; Jucicléia Soares da Silva

doi:10.17268/sci.agropecu.2025.004

Authors

Mycaella Gonçalves de Araújo Universidade do Estado da Bahia, Departamento de Tecnologia e Ciências Sociais, Juazeiro, BA, Brazil. https://orcid.org/0000-0002-2144-2196
Alessandro Carlos Mesquita Universidade do Estado da Bahia, Departamento de Tecnologia e Ciências Sociais, Juazeiro, BA, Brazil. https://orcid.org/0000-0002-9754-1676
Welson Lima Simões Empresa Brasileira de Pesquisa Agropecuária, Embrapa Semiárido, Petrolina, PE, Brazil. https://orcid.org/0000-0003-1474-9410
Raquel Nunes de Carvalho Universidade do Estado da Bahia, Departamento de Tecnologia e Ciências Sociais, Juazeiro, BA, Brazil. https://orcid.org/0000-0002-8751-6215
Ana Thaila Rodrigues Felix Universidade do Estado da Bahia, Departamento de Tecnologia e Ciências Sociais, Juazeiro, BA, Brazil. https://orcid.org/0000-0003-1071-1490
Jucicléia Soares da Silva Empresa Brasileira de Pesquisa Agropecuária, Embrapa Semiárido, Petrolina, PE, Brazil. https://orcid.org/0000-0003-3409-0326

DOI:

https://doi.org/10.17268/sci.agropecu.2025.004

Keywords:

Plant growth promotion, reactive oxygen species, semi-arid region, oxidative stress, hydric stress

Abstract

Water stress has caused major losses in the agricultural productivity of crops, inducing the search for alternatives for sustainable cultivation. In this context, the objective of this study was to evaluate the tolerance of watermelon under water stress, inoculated with bacterial strains of the genus Bacillus spp., regarding the biochemical and enzymatic variables in the flowering stage. A randomized block design was adopted in a split-plot 4x4 factorial scheme, with plots consisting of four levels of soil water availability (40%, 60%, 80% and 100% of field capacity - FC) and subplots consisting of four inoculations (Negative Control (NC); XX6.9 bacteria; P6.2 bacteria; MIX – co-inoculation of XX6.9 and P6.2 bacteria), with five replicates. XX6.9 bacteria and NC were the treatments most affected by severe water stress, since at the soil water availability (SWA) level of 40% FC they showed high contents of the oxidative marker (MDA) and proline. Although the inoculation with XX6.9 bacteria promoted a higher content of osmoregulators such as proteins, total soluble sugars and reducing sugars, it was not enough to attenuate the effects of water deficit. On the other hand, treatments with P6.2 bacteria and MIX of bacteria showed reduced levels of MDA at the SWA level of 40% FC, accompanied by high enzymatic activity of POD and CAT, which may contribute to the tolerance of the watermelon crop to water stress.

References

Abbasi, S., Sadeghi, A., & Safaie, N. (2020). Streptomyces alleviate drought stress in tomato plants and modulate the expression of transcription factors ERF1 and WRKY70 genes. Scientia Horticulturae, 265(109206), 1-9. https://doi.org/10.1016/j.scienta.2020.109206

Alkahtani, M. D., Hafez, Y. M., Attia, K., Rashwan E, Husnain L. A., Algwaiz, H. I., & Abdelaal, K. A. (2021b). Evaluation of silicon and proline application on the oxidative machinery in drought-stressed sugar beet. Antioxidants, 10(398), 1-19. https://doi.org/10.3390/antiox10030398

Alkahtani, M., Hafez, Y., Attia, K., Al-Aateeq, T., Ali, M. A., Hasanuzzaman, M., & Abdelaal, K. (2021). Bacillus thuringiensis and silicon modulate antioxidant metabolism and improve the physiological traits to confer salt tolerance in lettuce. Plants, 10(1025), 1-16. https://doi.org/10.3390/plantas10051025

Anee, T.I., Nahar, K., Rahman, A., Mahmud, J. A., Bhuiyan, T. F., Alam, M. U., Fujita, M., & Hasanuzzaman, M. (2019). Oxidative damage and antioxidant defense in Sesamum indicum after different waterlogging durations. Plants, 8(7), 196-214. https://doi.org/10.3390/plantas8070196

Azeem, M., Haider, M. Z., Javed, S., Salim, M. H., & Alatawi, A. (2022). Drought stress amelioration in maize (Zea mays L.) by inoculation of Bacillus spp. strains under sterile soil conditions. Agriculture, 12(1), 50-71. https://doi.org/10.3390/agriculture12010050

Bates, L. S., Waldren, R. A., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and soil, 39, 205-207. https://doi.org/10.1007/BF00018060

Bezerra, J. D. C., França, S. A., Nascimento Júnior, J. R.S. do., Castro, F. M. de., Silva, N. V. da, & Barbosa, S. N. (2020). Biossíntese de lignina em plantas submetidas ao déficit hídrico. Pubvet, 14(9), 1-14. https://doi.org/10.31533/pubvet.v14n9a653.1-14

Bhadrecha, P., Singh, S., Dwibedi, V. (2023). ‘A plant’s major strength in rhizosphere’, the plant growth promoting rhizobacteria. 2023. Archives of Microbiology, 205(5), 165-190. https://doi.org/10.1007/s00203-023-03502-2

Bikdeloo, M., Colla, G., Rouphael, Y., Hassandokht, M. R., Soltani, F., Salehi, R., Kumar, P., & Cardarelli, M. (2021). Morphological and physio-biochemical responses of watermelon grafted onto rootstocks of wild watermelon [Citrullus colocynthis (L.) Schrad] and commercial interspecific cucurbita hybrid to drought stress. Horticulturae, 7(10), 359-371. https://doi.org/10.3390/horticulturae7100359

Bradford, M. M., (1976). A rapid and sensitive method for quantification of microgran quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem, 72, 248-254. https://doi.org/10.1006/abio.1976.9999

Cui, G., Xiao, X., Zhang, W., Lang, D., Li, Z., & Zhang, X. (2021). Exogenous silicon relieve drought stress and salt stress of Glycyrrhiza uralensis seedlings by regulating proline metabolism and nitrogen assimilation. The Journal of Horticultural Science and Biotechnology, 96(6), 728-737. https://doi.org/10.1080/14620316.2021.1921624

Cruz, C., Cardoso, P., Santos, J., Matos, D., & Figueira, E. (2022). Bioprospecting Soil Bacteria from Arid Zones with Plant to Increase Plant Tolerance to Drought, Growth and Biochemical Status of Maize Inoculated Growth-Promoting Bacteria Isolated from Sal Island, Cape Verde. Plants, 11(21), 2912-2931. https://doi.org/10.3390/plants11212912

Dias, K., C., F., P., Souza, I., J., S., Dinas, S. S. E., Oliveira, M. C. B., Ferreira, V. Q., Barros, Y. C., & Jesus Santos, A. F de. (2022). Proteção para a cultura de milho contra a seca mediada por bactérias da Caatinga. Agrometeoros, 30, 1-7. https://doi.org/10.31062/agrom.v30.e026986

Devarajan, A. K., Muthukrishanan, G., Truu, J., Truu, M., Ostonen, I., Kizhaeral, S. S., Panneerselvam, P., & Gopalasubramanian, S. K. (2021). The foliar application of rice phyllosphere bacteria induces drought-stress tolerance in Oryza sativa (L.). Plants, 10(2), 387-408. https://doi.org/10.3390/plants10020387

Dubey, A., Kumar, A., Malla, M. A., Chowdhary, K., Singh, G., Ravikanth, H. G., Harish Sharma, S., Saati-Santamaria, Z., Menéndez, E., & Dames, J. F. (2021). Approaches for the amelioration of adverse effects of drought stress on crop plants. Frontiers in Bioscience-Landmark, 26(10), 928-947. https://doi.org/10.52586/4998

EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária. Sistema brasileiro de classificação de solos. 3ª edição. Brasília, DF, 2013. 353 p.

Ferreira, D. F. (2011). Sisvar: A computer statistical analysis system. Ciência e Agrotecnologia, 35(6), 1039-1042. https://doi.org/10.1590/S1413-70542011000600001

Gamalero, E., & Glick, B. R. (2022). Recent advances in bacterial amelioration of plant drought and salt stress. Biology, 11(3), 437-463. https://doi.org/10.3390/biologia11030437

Heath, R. L., & Packer. (1968). Photoperoidation in isolated chloroplasts I. Kinetic and stoichiometry of fatt acid peroxidation. Arch. Biochem. Biophys, 125, 189-198. https://doi.org/10.1016/0003-9861(68)90654-1

Jayaraj, M. S., & Beevy, S. S. (2021). Impact of drought on the characteristics attributes in the varieties of Momordica Charantia L. International Journal of Botany Studies, 6(3), 125-131.

Kamer, M. E. A., Khalil, G. A., & Yousry, M. M. (2022). Yield and Quality Performance of Some New Sweet Melon Lines Under Water Stress Conditions. Journal of the Advances in Agricultural Researches, 27(1), 148-161. https://doi.org/10.21608/jalexu.2022.114554.1036

La, V. H., Lee, B. R., Zhang, Q., Park, S. H., Islam, M. T., & Kim, T. H. (2019). Salicylic acid improves drought-stress tolerance by regulating the redox status and proline metabolism in Brassica rapa. Horticulture, Environment, and Biotechnology, 60(1), 31-40. https://doi.org/10.1007/s13580-018-0099-7

Latef, A. A. H. A., Zaid, A., Abo-baker, A. B. A. E., Salem, W., & Abu Alhmad, M. F. (2020). Mitigation of copper stress in maize by inoculation with Paenibacillus polymyxa and Bacillus circulans. Plants, 9(11), 1513-1531. https://doi.org/10.3390/plantas9111513

Lu, K., Sun, J., Li, Q., Li, X., & Jin, S. (2021). Effect of cold stress on growth, physiological characteristics, and calvin-cycle-related gene expression of grafted watermelon seedlings of different gourd rootstocks. Horticulturae, 7(10), 391-404. https://doi.org/10.3390/horticulturae7100391

Lu, J., Nawaz, M. A., Wei N., Cheng, F., & Bie, Z. (2020). Suboptimal temperature acclimation enhances chilling tolerance by improving photosynthetic adaptability and osmoregulation ability in watermelon. Horticultural Plant Journal, 6(1), 49-60. https://doi.org/10.1016/j.hpj.2020.01.001

Martínez-Valderrama, J., Olcina, J., Delacámara, G., Guirado, E., & Maestre, F. T. (2023). Complex Policy mixes are needed to cope with Agricultural Water demands under Climate Change. Water demands under Climate Change. Water Resources Management, 37(6), 2805-2834. https://doi.org/10.1007/s11269-023-03481-5

Maslennikova, D., & Lastochkina, O. (2021). Contribution of ascorbate and glutathione in endobacteria Bacillus subtilis-mediated drought tolerance in two Triticum aestivum L. genotypes contrasting in drought sensitivity. Plants, 10(12), 2557-2569. https://doi.org/10.3390/plantas10122557

Mendoza-Labrador, J., Romero-Perdomo, F., Abril, J., Hernández, J. P., Uribe-Vélez, D., & Buitrago, R. B. (2021). Bacillus strains immobilized in alginate macrobeads enhance drought stress adaptation of guinea grass. Rhizosphere, 19(14), 1-9 https://doi.org/10.1016/j.rhisph.2021.100385

Miller, G. L. (1959). Use dinitrosalicylis acid reagent for determination of reducing sugars. Analytical Chemistry, 31(2), 426-428. https://doi.org/10.1021/ac60147a030

Mohan, A., Shanmugam, S., & Nithyalakshmi, V. (2024). Comparison of the nutritional, physico-chemical and anti-nutrient properties of freeze and hot air dried watermelon (Citrullus lanatus) Rind. Biosciences Biotechnology Research Asia, 13(2), 1113-1119. http://dx.doi.org/10.13005/bbra/2140

Moreno-Galván, A. E., Cortés-Patiño, S., Romero-Perdomo, F., Uribe-Vélez, D., Bashan, Y., & Bonilla R. R. (2020). Proline accumulation and glutathione reductase activity induced by drought-tolerant rhizobacteria as potential mechanisms to alleviate drought stress in Guinea grass. Applied Soil Ecology, 147, 1-9. https://doi.org/10.1016/j.apsoil.2019.103367

Olotu, Y., Okodugha, D. A., Olarinde, O., Momoh, V. E., & Ibrahim, R. (2024). Estimation of consumptive water use for Watermelon in Auchi, Nigeria. Studia Universitatis Babes-Bolyai Engineering, 69(1). https://doi.org/10.24193/subbeng.2024.1.20

Peixoto, H. P. P., Cambraia, J., Sant’ana, R., Mosquim, P. R., & Moreira, A. M. (1999). Aluminium effects on lipid peroxidation and the activities of enzymes of oxidative metabolism in sorghum. Revista Brasileira de Fisiologia Vegetal, 11(3), 137-143.

Pinski, A., Betekhtin, A., Hupert-Kocurek, K., Mur, L. A., & Hasterok, R. (2019). Defining the genetic basis of plant–endophytic bacteria interactions. International Journal of Molecular Sciences, 20(8), 1947-1979. https://doi.org/10.3390/ijms20081947

Prgomet, I., Pascual-Seva, N., Morais, M. C., Aires, A., Barreales, D., Ribeiro, A. C., Silva, A. P., Barrosa, A. I. R. N. A, & Gonçalves, B. (2020). Physiological and biochemical performance of almond trees under deficit irrigation. Scientia Horticulturae, 261, 1-11. https://doi.org/10.1016/j.scienta.2019.108990

Santos Junior, J. L. dos, Oliveira, M. F. da C., & Silva, E. C. da. (2020). Acúmulo de solutos orgânicos em mudas de Ceiba glaziovii (Kutze) Kum. em resposta à seca intermitente. Scientia Plena, 16(1). https://doi.org/10.14808/sci.plena.2020.011201

Sheteiwy, M. S., Abd Elgawad, H., Xiong, Y. C., Macovei, A., Brestic, M., Skalicky, M., Hiba, Y. A., & El‐Sawah, A. M. (2021). Inoculation with Bacillus amyloliquefaciens and mycorrhiza confers tolerance to drought stress and improve seed yield and quality of soybean plant. Physiologia Plantarum, 172(4), 2153-2169. https://doi.org/10.1111/pp.13454

Silva, D. M. R., Barros, A. C., Silva, R. B., Galdino, W. D. O., Souza, J. W. G. D., Marques, I. C. D. S., ... & Rodrigues, J. D. (2024). Impact of Photosynthetic Efficiency on Watermelon Cultivation in the Face of Drought. Agronomy, 14(5), 950. https://doi.org/10.3390/agronomy14050950

Silva, E. P da., Barros, Y. C., & Santos, A. F. de J. (2023). Mitigação do déficit hídrico em plantas de milho por Bacillus sp. isolados de plantas endêmicas da caatinga. Scientific Electronic Archives, 16(6), 1-7. https://doi.org/10.36560/16620231508

Sood, G., Kaushal, R., & Sharma, M. (2020). Alleviation of drought stress in maize (Zea mays L.) by using endogenous endophyte Bacillus subtilis in North West Himalayas. Acta Agriculturae Scandinavica, Section B—Soil & Plant Science, 70(5), 361-370. https://doi.org/10.1080/09064710.2020.1743749

Teisseire, V. H., & Guy, V. Y. (2000). Copper-induced changes in antioxidant enzymes activities in fronds of duckweed (Lemna minor). Plant Science, 153, 65–72. https://doi.org/10.1016/S0168-9452(99)00257-5

Thomloudi, E. E., Tsalgatidou, P. C., Douka, D., Spantidos, T. N., Dimou, M., Venieraki, A., & Katinakis, P. (2019). Multistrain versus single-strain plant growth promoting microbial inoculants-The compatibility issue. Hell. Plant Prot. J., 12(6), 61–77. https://doi.org/10.3390/biology12060779

Vieira, M. L., Cunha, A. J. da., & Souza, D. S. (2021). Organomineral associado a Bacillus aryabhattai como atenuador do déficit hídrico em mudas de café. Revista Vitae-Educação, Saúde e Meio Ambiente, 1(9): 319–328. https://doi.org/10.17648/2525-2771-v1n9-9

Vieira, D. A., Carvalho, M. M. P., Rodrigues, B. A., Marinho, L. B., & Mesquita, A. C. (2020). Metabolic behavior in the allocation of biomass of melon cultivars under water deficit conditions. Research, Society and Development, 9(8), 1-18. https://doi.org/10.33448/rsd-v9i8.5128

Yadav, V. K., Yadav, R. C., Choudhary, P., Sharma, S. K., & Bhagat, N. (2022). Mitigation of drought stress in wheat (Triticum aestivum L.) by inoculation of drought tolerant Bacillus paramycoides DT-85 and Bacillus paranthracis DT-97. Journal of Applied Biology and Biotechnology, 10(1), 59-69. https://doi.org/10.7324/JABB.2022.10s109

Yemm, E. W., & Willis, A. J. (1954). The estimation of carbohydrates in plants extracts by antrone. Biochemical Journal, 57(3), 508-514. https://doi.org/10.1042/bj0570508

Zahedyan, A., Jahromi, A. A., Zakerin, A., Abdossi, V., & Torkashvand, A. M. (2022). Nitroxin bio-fertilizer improves growth parameters, physiological and biochemical attributes of cantaloupe (Cucumis melo L.) under water stress conditions. Journal of the Saudi Society of Agricultural Sciences, 21(1), 8-20. https://doi.org/10.1016/j.jssas.2021.06.017