Sains Malaysiana 53(1)(2024): 23-37

http://doi.org/10.17576/jsm-2024-5301-03

Tripartite Introductions of PGPR, Humic Acid, and N-Fertilizer Improve the Growth and Yield of Sweet Potato under Glasshouse Conditions

(Pengenalan Tripihak PGPR, Asid Humik dan Baja N Meningkatkan Pertumbuhan dan Hasil Ubi Keledek di bawah Keadaan Rumah Kaca)

BURAQ MUSA SADEQ¹, ALI TAN KEE ZUAN^1,*, SUSILAWATI KASIM¹, JAWADYN TALIB ALKOORANEE², WONG MUI YUN³, NUR MAIZATUL IDAYU OTHMAN⁴, AMAILY AKTER¹, SAYMA SERINE CHOMPA¹, ABBA NABAYI⁵ & MD EKHLASUR RAHMAN^1,6

¹Department of Land Management, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia

²Department of Plant Protection, Faculty of Agriculture, University of Wasit, Wasit, Iraq

³Department of Plant Protection, Faculty of Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia

⁴Faculty of Plantation and Agrotechnology, Universiti Teknologi MARA, Melaka, Kampus Jasin 77300 Merlimau, Melaka, Malaysia

⁵Department of Soil Science, Faculty of Agriculture, Federal University Dutse, Nigeria. PMB 7156, Ibrahim Aliyu bye-pass Jigawa state, 720101, Nigeria

⁶Divisional Laboratory, Soil Resource Development Institute, Krishi Khamar Sharak, Farmgate, Dhaka-1215, Bangladesh

Received: 17 April 2023/Accepted: 4 December 2023

Abstract

This study was undertaken to investigate the effects of plant growth-promoting rhizobacteria (PGPR) with humic acid (HA) as amendments on the morphological and physiological growth characteristics and yield of Sepang Oren sweet potato (Ipomoea batatas[L.] Lam). The experiment was conducted under glasshouse conditions at the Faculty of Agriculture, Universiti Putra Malaysia, for 110 days. Two factors were used in this experiment: The first factor was PGPR-HA inoculations (UPMB10, UPMRB9, and mixed strains) and non-inoculation-HA, and the second factor was the Nitrogen fertilizer levels (50, 75, and 100%). The treatments were replicated three times and arranged factorially in a randomized complete block design. The results showed that inoculations with PGPRs-HA (UPMRB9 and UPMB10 strains) positively affect the plant growth significantly (SPAD measurements, number of leaves, vine length, root length, leaf area index, root dry weight, shoot dry weight, and root: shoot ratio) of sweet potato upon addition of 50% and 75% of N-fertilizer, respectively. The nutrient content of soil and plant leaf significantly increased by 12-15% and 14-18%, respectively, compared to the uninoculated, when applied with the same inoculation. After 30 days, the population of soil bacteria increased, reaching a value of 8.65 log₁₀ CFU/g soil. The use of PGPR-HA inoculations with N-fertilization resulted in a considerable rise in the majority of plant and soil parameters compared to the treatments without PGPR inoculation. Therefore, PGPR supplemented with humic acid (HA) may be considered a viable and sustainable strategy for enhancing sweet potatoes' morphological and physiological attributes. This technique can result in increased crop productivity and serve as a substitute for nitrogen-based fertilizers.

Keywords: Bacterial population; humic acid (HA); PGPR; soil nutrients; sweet potato yield

Abstrak

Penyelidikan ini dijalankan untuk mengkaji kesan rizobakteria penggalak pertumbuhan tumbuhan (PGPR) dengan asid humik (HA) sebagai pindaan terhadap ciri pertumbuhan morfologi dan fisiologi serta hasil ubi keledek Sepang Oren (Ipomoea batatas [L.] Lam). Uji kaji dijalankan di bawah keadaan rumah kaca di Fakulti Pertanian, Universiti Putra Malaysia, selama 110 hari. Dua faktor telah digunakan dalam uji kaji ini: Faktor pertama ialah inokulasi PGPR-HA (UPMB10, UPMRB9 dan strain campuran) dan bukan inokulasi-HA serta faktor kedua ialah kepekatan baja Nitrogen (50, 75 dan 100%). Setiap rawatan mengandungi tiga replikasi dan disusun secara faktorial dalam reka bentuk blok lengkap rawak. Hasil menunjukkan bahawa inokulasi dengan PGPRs-HA (strain UPMRB9 dan UPMB10) memberi kesan positif kepada pertumbuhan tumbuhan dengan ketara (ukuran SPAD, bilangan daun, panjang pokok, panjang akar, indeks luas daun, berat kering akar, berat kering pucuk dan nisbah akar: pucuk) ubi keledek selepas penambahan 50% dan 75% baja N. Kandungan nutrien tanah dan daun tumbuhan masing-masing meningkat dengan ketara sebanyak 12-15% dan 14-18% berbanding dengan tumbuhan yang tidak diinokulasi. Selepas 30 hari, populasi bakteria tanah meningkat, mencapai nilai 8.65 log₁₀ CFU/g tanah. Penggunaan inokulasi PGPR-HA dengan pembajaan N menghasilkan peningkatan yang ketara dalam majoriti parameter tumbuhan dan tanah berbanding dengan rawatan tanpa inokulasi PGPR. Oleh itu, PGPR Bersama-sama asid humik (HA) boleh dianggap sebagai strategi yang mampan untuk meningkatkan sifat morfologi dan fisiologi ubi keledek. Teknik ini boleh menghasilkan peningkatan produktiviti tanaman dan berfungsi sebagai pengganti baja berasaskan nitrogen.

Kata kunci: Asid humik (HA); hasil ubi keledek; nutrien tanah; PGPR; populasi bakteria

REFERENCES

Abdelrahman, H.M., Zaghloul, R.A., Hassan, E.A., El-Zehery, H.R.A. & Salem, A.A. 2021. New strains of plant growth-promoting rhizobacteria in combination with humic acid to enhance squash growth under saline stress. Egyptian Journal of Soil Science 61(1): 129-146.

Agbede, T.M. & Oyewumi, A. 2022. Benefits of biochar, poultry manure and biochar–poultry manure for improvement of soil properties and sweet potato productivity in degraded tropical agricultural soils. Resources, Environment and Sustainability 7: 100051. https://doi.org/10.1016/j.resenv.2022.100051

Ahmad, S., Daur, I., Al-Solaimani, S.G., Mahmood, S., Bakhashwain, A.A., Madkour, M.H. & Yasir, M. 2016. Effect of rhizobacteria inoculation and humic acid application on canola (Brassica napus L.) crop. Pakistan Journal of Botany 48: 2109-2120.

Al-Taey, D.K., Al-Shareefi, M.J., Mijwel, A.K., Al-Tawaha, A.R. & Al-Tawaha, A.R. 2019. The beneficial effects of biofertilizers combinations and humic acid on growth, yield parameters and nitrogen content of broccoli grown under drip irrigation system. Bulgarian Journal of Agricultural Science 25(5): 959-966.

Ashwini, N., Kumar, P., Joshi, A.K., Sharma, N.C., Sharma, N. & Sharma, N. 2022. Synergistic action of humic acid substances and bio-inoculants in guava (Psidium guajavaL.): Impact on growth traits, fruiting, nutrient profiling and rhizosphere stochiometry in meadow rainy season plant-soil interface. Journal of Plant Nutrition 46(4): 574-588.

Baard, V., Bakare, O.O., Daniel, A.I., Nkomo, M., Gokul, A., Keyster, M. & Klein, A. 2023. Biocontrol potential of Bacillus subtilis and Bacillus tequilensis against four fusarium species. Pathogens 12(2): 254.

Bashan, Y., de-Bashan, L.E., Prabhu, S.R. & Hernandez, J.P. 2014. Advances in plant growth-promoting bacterial inoculant technology: Formulations and practical perspectives (1998-2013). Plant and Soil 378: 1-33.

Bahadur, I., Maurya, B.R., Meena, V.S., Saha, M., Kumar, A. & Aeron, A. 2017. Mineral release dynamics of tricalcium phosphate and waste muscovite by mineral-solubilizing rhizobacteria isolated from indo-gangetic plain of India. Geomicrobiology Journal 34(5): 454-466.

Benz, M., Schink, B. & Brune, A. 1998. Humic acid reduction by Propionibacterium freudenreichii and other fermenting bacteria. Applied and Environmental Microbiology 64: 4507-4512.

Bowman, D.C., Paul, J.L. & Carlson, R.M. 1988. A method to exclude nitrate from Kjeldahl digestion of plant tissues. Communications in Soil Science and Plant Analysis 19: 205-213.

Chen, X., Kou, M., Tang, Z., Zhang, A. & Li, H. 2017. The use of humic acid urea fertilizer for increasing yield and utilization of nitrogen in sweet potato. Plant, Soil and Environment 63(5): 201-206.

Çığ, F., Sönmez, F., Nadeem, M.A. & Sabagh, A.E. 2021. Effect of biochar and PGPR on the growth and nutrients content of einkorn wheat (Triticum monococcumL.) and post-harvest soil properties. Agronomy 11: 2418.

Egamberdiyeva, D. & Höflich, G. 2004. Effect of plant growth-promoting bacteria on growth and nutrient uptake of cotton and pea in a semi-arid region of Uzbekistan. Journal of Arid Environments 56(2): 293-301.

Ekin, Z. 2020. Co-application of humic acid and bacillus strains enhances seed and oil yields by mediating nutrient acquisition of safflower (Carthamus tinctoriusL.) plants in a semi-arid region. Applied Ecology and Environmental Research 18: 1883-1900.

Ekin, Z. 2019. Integrated use of humic acid and plant growth promoting rhizobacteria to ensure higher potato productivity in sustainable agriculture. Sustainability 11(12): 3417.

El-Sawah, A.M., El-Keblawy, A., Ali, D.F.I., Ibrahim, H.M., El-Sheikh, M.A., Sharma, A. & Sheteiwy, M.S. 2021. Arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria enhance soil key enzymes, plant growth, seed yield, and qualitative attributes of guar. Agriculture 11: 194.

Etesami, H., Alikhani, H.A. & Mirseyed Hosseini, H. 2015. Indole-3-acetic acid and 1-aminocyclopropane-1-carboxylate deaminase: Bacterial traits required in rhizosphere, rhizoplane and/or endophytic competence by beneficial bacteria. Bacterial Metabolites in Sustainable Agroecosystem. Sustainable Development and Biodiversity, vol 12, edited by Maheshwari, D. Springer, Cham. pp. 183-258.

Folina, A., Tataridas, A., Mavroeidis, A., Kousta, A., Katsenios, N. & Efthimiadou, A. 2021. Evaluation of various nitrogen indices in N-Fertilizers with inhibitors in field crops: A review. Agronomy 11: 418.

Goswami, D., Thakker, J.N. & Dhandhukia, P.C. 2016. Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review. Cogent Food & Agriculture 2(1): 1127500.

Gupta, S., Stirk, W.A., Plačková, L., Kulkarni, M.G., Doležal, K. & Van Staden, J. 2021. Interactive effects of plant growth-promoting rhizobacteria and a seaweed extract on the growth and physiology of Allium cepa L. (onion). Journal of Plant Physiology 262: 153437.

Huang, X.F., Chaparro, J.M., Reardon, K.F., Zhang, R., Shen, Q. & Vivanco, J.M. 2014. Rhizosphere interactions: Root exudates, microbes, and microbial communities. Botany 92(4): 267-275.

Itelima, J.U., Bang, W.J., Onyimba, I.A., Sila, M.D. & Egbere, O.J. 2018. Bio-fertilizers as key player in enhancing soil fertility and crop productivity: A review. Direct Research Journal of Agriculture and Food Science 6(3): 73-83.

Kapadia, C., Sayyed, R.Z., El Enshasy, H.A., Vaidya, H., Sharma, D., Patel, N. & Zuan, A.T.K. 2021. Halotolerant microbial consortia for sustainable mitigation of salinity stress, growth promotion, and mineral uptake in tomato plants and soil nutrient enrichment. Sustainability 13: 8369.

Karim, N.A., Devarajan, T. & Ahmad, A. 2022. Principal component analysis for phenotypic characterization of sweet potato (Ipomoea batatas(L.) Lam.) genotypes in Malaysia. Trends in Sciences 19: 4612.

Kashiani, P. 2012. Genetic potential of selected sweet corn inbred lines and analysis of their combining ability assisted by microsatellite DNA markers. Doctoral dissertation. Universiti Putra Malaysia (Unpublished).

Kamali, S.R., Tsai, C.H. & Chen, C.N. 2021. Comparison of three digestion methods for determination of selenium in green tea samples using fluorescence spectrometry. IOP Conference Series: Earth and Environmental Science 712(1): 012016. doi:10.1088/1755-1315/712/1/012016

Kaur, T., Devi, R., Kumar, S., Sheikh, I., Kour, D. & Yadav, A.N. 2022. Microbial consortium with nitrogen fixing and mineral solubilizing attributes for growth of barley (Hordeum vulgareL.). Heliyon 8(4): e09326.

Khan, Z., Rahman, M.H.U., Haider, G., Amir, R., Ikram, R.M., Ahmad, S., Schofield, H.K., Riaz, B., Iqbal, R., Fahad, S., Datta, R., Baazeem, A., El Sabagh, A. & Danish, S. 2021. Chemical and biological enhancement effects of biochar on wheat growth and yield under arid field conditions. Sustainability 13(11): 5890.

Laftah, S.K. & Alabdulla, S.A. 2022. Response of some growth traits of safflower (Carthamus tinctoriusL.) to spray with humic acid under levels of phosphorus fertilizer. IOP Conference Series: Earth and Environmental Science 1060(1): 012115.

Mabrouk, Y., Hemissi, I., Salem, I.B., Mejri, S., Saidi, M. & Belhadj, O. 2018. Potential of rhizobia in improving nitrogen fixation and yields of legumes. Symbiosis 107: 73495.

Mahapatra, S., Yadav, R. & Ramakrishna, W. 2022. Bacillus subtilis impact on plant growth, soil health and environment: Dr. Jekyll and Mr. Hyde. Journal of Applied Microbiology 132(5): 3543-3562.

Manna, M.C., Rahman, M.M., Naidu, R., Bari, A.F., Singh, A.B., Thakur, J.K. & Subbarao, A. 2021. Organic farming: A prospect for food, environment and livelihood security in Indian agriculture. Advances in Agronomy 170: 101-153.

Meena, K., Ram, R.B., Meena, M.L., Meena, J.K. & Meena, D.C. 2017. Effect of organic manures and bio-fertilizers on growth, yield and quality of broccoli (Brassica oleraceavar.) cv. KTS-1. Chemical Science Review and Letters 6: 2153-2158.

Meng, F., Huang, Q., Yuan, G., Cai, Y. & Han, F.X. 2021. The beneficial applications of humic substances in agriculture and soil environments. In New Trends in Removal of Heavy Metals from Industrial Wastewater, edited by Shah, M.P., Couto, S.R. & Kumar, V. Elsevier. pp. 131-160.

Moreira, B.C., Prates Júnior, P., Dell, B. & Kasuya, M.C.M. 2022. Roots and beneficial interactions with soil microbes. In Subsoil Constraints for Crop Production, edited by Oliveira, T.S.D. & Bell, R.W. Springer, Cham. pp. 263-287.

Mosharrof, M., Uddin, M., Sulaiman, M.F., Mia, S., Shamsuzzaman, S.M. & Haque, A.N.A. 2021. Combined application of biochar and lime increases maize yield and accelerates carbon loss from an acidic soil. Agronomy 11(7): 1313.

Muhammad, R., Nor, N.M., Ikram, E.H.K. & Sharif, M.S.M. 2022. Sustainability of underutilized local crop through product development of Malaysia purple sweet potato cracker. Malaysian Journal of Medicine & Health Science 18: 305-314.

Neela, S. & Fanta, S.W. 2019. Review on nutritional composition of orange‐fleshed sweet potato and its role in management of vitamin A deficiency. Food Science & Nutrition 7: 1920-1945.

Prasad, R., Kumar, M. & Varma, A. 2015. Role of PGPR in soil fertility and plant health. In Plant-Growth-Promoting Rhizobacteria (PGPR) and Medicinal Plants, edited by Egamberdieva, D., Shrivastava, S. & Varma, A. Soil Biology, vol. 42. Springer, Cham. pp. 247-260.

Pandita, D. 2022. Plant growth promoting bacteria (PGPB): Applications and challenges in bioremediation of metal and metalloid contaminated soils. In Metals Metalloids Soil Plant Water Systems, edited by Aftab, T. & Hakeem, K. Massachusetts: Academic Press. pp. 485-500.

Sadeq, B.M., Zuan, K., Tan, A., Kasim, S., Yun, W.M., Othman, N.M.I., Alkooranee, J.T., Chompa, S.S., Akter, A. & Rahman, M.E. 2023. Humic acid-amended formulation improves shelf-life of plant growth-promoting rhizobacteria (PGPR) under laboratory conditions. Pertanika Journal of Science & Technology 31(3): 1137-1155.

Sharma, I.P., Chandra, S., Kumar, N. & Chandra, D. 2017. PGPR: Heart of soil and their role in soil fertility. In Agriculturally Important Microbes for Sustainable Agriculture, edited by Meena, V., Mishra, P., Bisht, J. & Pattanayak, A. Singapore: Springer. pp. 51-67.

Savarese, C., Cozzolino, V., Verrillo, M., Vinci, G., De Martino, A., Scopa, A. & Piccolo, A. 2022. Combination of humic biostimulants with a microbial inoculum improves lettuce productivity, nutrient uptake, and primary and secondary metabolism. Plant and Soil 481: 285-314.

Shankar, A.B. & Kaushik, P. 2022. Visiting sweet potato from a breeding perspective: An update. PrePrints 2020: 2022040149.

Tang, C., Cheng, K., Liu, B., Antonietti, M. & Yang, F. 2022. Artificial humic acid facilitates biological carbon sequestration under freezing-thawing conditions. Science of The Total Environment 849: 157841.

Thomas, G.W. 1983. Chapter 9. Exchangeable cations. In Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties, edited by Page, A.L. Madison: American Society of Agronomy, Soil Science Society of America. pp. 159-165.

Wang, D., Chen, X., Tang, Z., Liu, M., Jin, R., Zhang, A. & Zhao, P. 2022. Application of humic acid compound fertilizer for increasing sweet potato yield and improving the soil fertility. Journal of Plant Nutrition 45(13): 1933-1941.

Wu, Y., Li, S. & Chen, G. 2020. Impact of humic acids on phosphorus retention and transport. Journal of Soil Science and Plant Nutrition 20: 2431-2439.

Yang, F., Tang, C. & Antonietti, M. 2021. Natural and artificial humic substances to manage minerals, ions, water, and soil microorganisms. Chemical Society Reviews 50(10): 6221-6239.

Yasmin, F., Othman, R. & Maziz, M.N.H. 2020. Yield and nutrient content of sweet potato in response of plant growth-promoting rhizobacteria (PGPR) inoculation and N fertilization. Jordan Journal of Biological Science Jordan 13: 117-122.

Yuan, Z., Cao, Q., Zhang, K., Ata-Ul-Karim, S.T., Tian, Y., Zhu, Y. & Liu, X. 2016. Optimal leaf positions for SPAD meter measurement in rice. Frontiers in Plant Science 7: 719.

Zeng, Q., Ding, X., Wang, J., Han, X., Iqbal, H. & Bilal, M. 2022. Insight into soil nitrogen and phosphorus availability and agricultural sustainability by plant growth-promoting rhizobacteria. Environmental Science and Pollution Research 29: 45089-45106.

Zhao, C., Liu, G., Chen, Y., Jiang, Y., Shi, Y., Zhao, L., Liao, P., Wang, W., Xu, K., Dai, Q. & Huo, Z. 2022. Excessive nitrogen application leads to lower rice yield and grain quality by inhibiting the grain filling of inferior grains. Agriculture 12(7): 962.

Zhu, F. & Sun, J. 2019. Physicochemical and sensory properties of steamed bread fortified with purple sweet potato flour. Food Bioscience 30: 100411.

Zilaie, M.N., Arani, A.M., Etesami, H., Dinarvand, M. & Dolati, A. 2022. Halotolerant plant growth-promoting rhizobacteria-mediated alleviation of salinity and dust stress and improvement of forage yield in the desert halophyte Seidlitzia rosmarinus. Environmental and Experimental Botany 201: 104952.

*Corresponding author; email: tkz@upm.edu.my