Abstract
Rhizoctonia solani causes root rot in soybean, a worldwide severe concern for soybean cultivation. The fungus grows and clogs the xylem tissue of the host plant by producing numerous sclerotia, which results in disease symptoms, such as yellowing of leaves, wilt, and plant death. Overuse of chemical fungicides increases the threat of developing resistance to pathogens, reduces soil productivity, and negatively impacts the health of the soil, the environment, and humans. An integrated pest management strategy improves crop yield, profit, and safety. The present study focused on a fungicide (carbendazim) compatibility test with a biocontrol agent (Pseudomonas fluorescence). It evaluated the effect of this combined approach on photosynthetic reactions and growth in soybean in the presence of the fungal pathogen R. solani. The study showed that P. fluorescence significantly inhibited the mycelial growth of R. solani (43%) and tolerated 0.05–0.15% concentration of carbendazim. This confirms the suitability compatibility of P. fluorescence with chemical fungicides for IPM. These novel blending significantly reduced the disease incidence by about 75%, and a 72% decrease in disease severity was observed compared to pathogen control. Moreover, this combined approach has also improved plant growth, yield parameters, and photosynthetic efficiency in the presence of R. solani treated with an integrated system showed better overall growth despite being infected by the pathogen.
Similar content being viewed by others
Data Availability
All the data studied are included in the manuscript itself.
References
Lamichhane JR, Durr C, Schwanck AA, Robin MH, Sarthou JP, Cellier V, Messean A, Aubertot JN (2017) Integrated management of damping-off diseases, a review. Agron Sustain Dev 37(10):1–25. https://doi.org/10.1007/s13593-017-0417-y
Reznikov S, Vellicce GR, González V (2016) Evaluation of chemical and biological seed treatments to control charcoal rot of soybean. J Gen Plant Pathol 82:273–280. https://doi.org/10.1007/s10327-016-0669-4
Amrate PK, Pancheshwar DK, Shrivastava MK (2020) Screening of genotypes to identify the resistance source against major diseases of soybean under high disease pressure conditions. Int J Curr Microbiol Appl Sci 9(5):1739–1745
Yasmin H, Mumtaz S, Jabeen Z, Naz R, Nosheen A, Hassan MN (2020) Multi-trait Pseudomonas spp. isolated from monocropped wheat (Triticum aestivum L.) suppress fusarium root and crown rot. Phytopathology 110:582–592. https://doi.org/10.1094/PHYTO-10-19-0383-R
Rai S, Omar AF, Rehan M, Al-Turki A, Sagar A, Ilyas N, Sayyed RZ, Mirza H (2022) Crop microbiome: their role and advances in molecular and omic techniques for the sustenance of agriculture. Planta 257:27. https://doi.org/10.1007/s00425-022-04052-5
Suriani NL, Suprapta D, Novizar N, Parwanayoni NI, Darmadi A, Dewi D, Sudatri KS, Ahmad F, Sayyed RZ, Syed A, Elgorban A, Bahkali A, Enshasy H, Dalin DJ (2020) A mixture of piper leaves extracts and rhizobacteria for sustainable plant growth promotion and biocontrol of blast pathogen of organic Bali rice. Sustainability 12(20):8490. https://doi.org/10.3390/su12208490
Piel C, Pouchieu C, Carles C, Béziat B, Boulanger M, Bureau M, Busson A, Grüber A, Lecluse Y, Migault L (2019) Agricultural exposures to carbamate herbicides, fungicides, and central nervous system tumour incidence in the cohort AGRICAN. Environ Int 130:104876. https://doi.org/10.1016/j.envint.2019.05.070
Qessaoui R, Bouharroud R, Furze JN, El Aalaoui M, Akroud H, Amarraque A, Vaerenberg VJ, Tahzima R, Mayad EH, Chebli B (2019) Applications of new rhizobacteria Pseudomonas isolates in agroecology via fundamental processes complementing plant growth. Sci Rep 9:12832. https://doi.org/10.1038/s41598-019-49216-8
Redouan Q, Rachid B, Abdera HA, Hind L, Abdelhadi A, Naima AA, Abdelghani T, El Hassan M, Bouchra C (2019) Effect of Pseudomonas as a preventive and curative control of tomato leaf miner Tuta absoluta (Lepidoptera: Gelechiidae). J Appl Sci 19:473–479. https://doi.org/10.3923/jas.2019.473.479
Reshma P, Naik MK, Aiyaz M, Niranjana SR, Chennappa G, Shaikh SS, Sayyed RZ (2018) Induced systemic resistance by 2,4-diacetylphloroglucinol positive fluorescent Pseudomonas strains against rice sheath blight. Indian J Expl Biol 56(3):207–212
Vinay JU, Naik MK, Rangeshwaran R, Chennappa G, Shaikh SS, Sayyed RZ (2016) Detection of antimicrobial traits in fluorescent pseudomonas and molecular characterization of an antibiotic pyoluteorin. 3 Biotech 6(2):227. https://doi.org/10.1007/s13205-016-0538-z
Sharifi R, Ryu CM (2018) Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Ann Bot 27(122):349–355. https://doi.org/10.1093/aob/mcy108
Choudhary DK (2011) Plant growth-promotion (PGP) activities and molecular characterization of rhizobacterial strains isolated from soybean (Glycine max L. Merril) plants against charcoal rot pathogen Macrophomina phaseolina. Biotechnol Lett 33(11):2287–2295. https://doi.org/10.1007/s10529-011-0699-0
Meena M, Swapnil P (2019) Regulation of WRKY genes in plant defines with beneficial fungus Trichoderma: current perspectives and future prospects. Arch Phytopathol Plant Protect 52:1–17. https://doi.org/10.1080/03235408.2019.1606490
Food and Agriculture Organization for the United Nations (2020) NSP—Integrated Pest Management. http://www.fao.org/agriculture/crops/thematic-sitemap/theme/pests/ipm/en/
Prabhukarthikeyan SR, Raguchander T (2016) Antifungal metabolites of Pseudomonas fluorescens against Pythium aphanidermatum. J Pure Appl Microbiol 10(1):579–584
Suresh P, Varathraju G, Shanmugaiah V, Almaary KS, Elbadawi YB, Mubarak A (2021) Partial purification and characterization of 2,4-diacetyl phloroglucinol producing Pseudomonas fluorescens VSMKU3054 against bacterial wilt disease of tomato. Saudi J Biol Sci 28(4):2155–2167. https://doi.org/10.1016/j.sjbs.2021.02.073
Yildiz F, Yildiz M, Delen N, Conskuntuna A, Kinay P, Turuksay H (2006) The effects of biological and chemical treatment on gray mold disease in tomatoes grown under greenhouse conditions. Turk J Agric For 31:319–325
Vasebi Y, Saifi N, Alizadeh A (2013) Biological control of soybean charcoal root rot disease using bacterial and fungal antagonists in vitro and greenhouse condition. J Crop Prot 2(2):139–150
Groth JV, Ozmon EA, Busch RH (1999) Repeatability and relationship of incidence and severity measures of the scab of wheat caused by Fusarium graminearum in inoculated nurseries. Plant Dis. https://doi.org/10.1094/PDIS.1999.83.11.1033
Pérez-Patricio M, Camas-Anzueto JL, Sanchez-Alegría A, Aguilar-González A, Gutiérrez-Miceli F, Escobar-Gómez E (2018) Optical method for estimating the chlorophyll contents in plant leaves. Sensors 18:650. https://doi.org/10.3390/s18020650
Force L, Critchley C, Van Remsen JJS (2003) New fluorescence parameters for monitoring photosynthesis in plants. The effect of illumination on the fluorescence parameters of the JIP-test. Photosyn Res 78:17–33. https://doi.org/10.1023/A:1026012116709
Shaikh SS, Reddy MS, Sayyed RZ (2016) Plant growth promoting rhizobacteria: an eco-friendly approach for sustainable agroecosystem. In: Hakee K, Akhtar M, Abdullah S (eds) Plant, soil and microbes. Cham, Springer, pp 182–203. https://doi.org/10.1007/978-3-319-27455-3_10
Khan RM, Akram A (2000) Effects of certain antagonistic fungi and rhizobacteria on wilt disease complex of tomato caused by Fusarium oxysporum. Nematol Mediterr 28:139–144
Zope VP, Enshasy HAE, Sayyed RZ (2019) Plant growth promoting rhizobacteria: an overview in agricultural perspectives. In: Sayyed R (ed) Plant growth promoting rhizobacteria for sustainable stress management. Microorganisms for sustainability, vol 13. Springer, Singapore, pp 345–362. https://doi.org/10.1007/978-981-13-6986-5_13
Mohamed OM, Hussein AAR, Badawi MH, Mabel HE (2020) Antifungal activity of Pseudomonas fluorescence metabolites against some phytopathogenic fungi. Middle East J Appl Sci 10(02):158–168. https://doi.org/10.36632/mejas/2020.10.2.18
Panpatte DG, Jhala YK, Shelat HN, Vyas RV (2016) Pseudomonas fluorescence: a promising biocontrol agent and PGPR for sustainable agriculture. In: Singh D, Singh H, Praha R (eds) Microbial inoculants in sustainable agricultural productivity. Springer India, New Delhi, pp 257–270. https://doi.org/10.1007/978-81-322-2647-5_15
Sayyed RZ, Chincholkar SB (2009) Siderophore-producing A. faecalis exhibits more biocontrol potential vis-à-vis chemical fungicides. Curr Microbiol 58(1):47–51. https://doi.org/10.1007/s00284-008-9264-z
Castaldi S, Petrillo C, Donadio G, Piaz FD, Cimmino A, Masi M, Evidente A, Isticato R (2021) Plant growth promotion function of Bacillus sp. strains isolated from salt-pan rhizosphere and their biocontrol potential against Macrophomina phaseolina. Int J Mol Sci 22(7):3324. https://doi.org/10.3390/ijms22073324
Reddy BP, Reddy MS, Kumar KVK (2009) Characterization of antifungal metabolites of Pseudomonas fluorescens and their effect on mycelial growth of Magnaporthe grisea and Rhizoctonia solani. Int J PharmTech Res 1(4):1490–1493
Dubey SC, Singh V, Priyanka K, Upadhyay BK, Singh B (2015) Combined application of fungal and bacterial bio-agents, together with fungicide and Mesorhizobium for integrated management of Fusarium wilt of chickpea. Biocontrol 60:413–424. https://doi.org/10.1007/s10526-015-9653-8
O’Brien PA (2017) Biological control of plant diseases. Australas Plant Pathol 46(4):293–304. https://doi.org/10.1007/s13313-017-0481-4
Jambhulkar PP, Sharma P, Manokaran R, Lakshmana DK, Rokadia P, Jambhulkar N (2018) Assessing synergism of combined applications of Trichoderma harzianum and Pseudomonas fluorescence to control blast and bacterial leaf blight of rice. Eur J Plant Pathol 152:747–757. https://doi.org/10.1007/s10658-018-1519-3
Omar TM, O’Neill RS (2006) Biological control of fusarium crown and root rot of tomato with antagonistic bacteria and integrated control when combined with the fungicide carbendazim. Plant Pathol 55:92–99. https://doi.org/10.1111/j.1365-3059.2005.01315.x
Karuna C, Kurhade RM, Gade Y, Belkar K, Chaitanya BH (2016) Detecting tolerance in Pseudomonas fluorescens to the pesticide. Agric Sci Digest 36(3):247–249
Mishra G, Kumar N, Giri K, Pandey S, Kumar R (2014) Effect of fungicides and bioagents on number of microorganisms in soil and yield of soybean (Glycine max). Nusant Biosci 6(1):2087–2394. https://doi.org/10.13057/nusbiosci/n060108
Mufti R, Bano A (2019) PGPR-induced defense responses in the soybean plant against charcoal rot disease. Eur J Plant Pathol 155:983–1000. https://doi.org/10.1007/s10658-019-01828-6
Ullah H, Yasmin H, Mumtaz S, Jabeen Z, Naz R, Nosheen A, Hassan MN (2019) Multi-trait Pseudomonas spp. isolated from monocropped wheat (Triticum aestivum L). suppress fusarium root and crown rot. Phytopathology 110:582–592. https://doi.org/10.1094/PHYTO-10-19-0383-R
Kaur C, Maini P, Shukla NP (2007) Effect of captan and carbendazim fungicides on nodulation and biological nitrogen fixation in soybean. Asian J Exp Sci 21(2):385–388
Naz H, Sayyed RZ, Khan RU, Wani OA, Maqsood A, Maqsood S, Fahad A, Lim HR, Show PL (2023) Mesorhizobium improves chickpea growth under chromium stress and alleviates chromium contamination of soil. J Environ Manag 338(2023):117779. https://doi.org/10.1016/j.jenvman.2023.117779
Moretti LG, Crusciol CAC, Kuramae EE, Bossolani JW, Moreira A, Costa NR, Alves CJ, Pascoaloto IM, Rondina ABL, Hungria M (2020) Effects of growth-promoting bacteria on soybean root activity, plant development, and yield. Agron J 112:418–428. https://doi.org/10.1002/agj2.20010
Wasule DL, Wadyalkar SR, Buldeo AN (2007) Effect of phosphate solubilizing bacteria on the role of Rhizobium on nodulation by soybean. In: First international meeting on microbial phosphate solubilisation. Developments in plant and soil sciences, vol 102. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5765-6
Jabborova D, Wirth S, Kannepalli A, Narimanov A, Desouky S, Davranov K, Sayyed RZ, Enshasy HAE, Malek RA, Syed A, Bahkali AH (2020) Co-inoculation of rhizobacteria and biochar application improves growth and nutrient in soybean and enriches soil nutrients and enzymes. Agronomy 10:1142. https://doi.org/10.3390/agronomy1008114
Kanti VM, Ranganatha HM, Patil SS, Swathi P, Rajeev S, Srivalli P (2013) Development of heterotic pairs or groups of cotton genotypes based on predicted double cross performance. Int J Agric Crop Sci 6(5):231–235
Gaurav A, Pallavi PK (2018) Effect of Pseudomonas aeruginosa on the growth of chickpea (Pisum sativum L.) plant under saline condition. Int J Curr Microbiol Appl Sci 7(10):1549–1554. https://doi.org/10.20546/ijcmas.2018.710.173
Hamani AKM, Wang G, Soothar MK, Shen X, Gao Y, Qiu R, Mehmood F (2020) Responses of leaf gas exchange attributes, photosynthetic pigments, and antioxidant enzymes in NaCl-stressed cotton (Gossypium hirsutum L.) seedlings to exogenous glycine betaine and salicylic acid. BMC Plant Biol 20(1):1–14. https://doi.org/10.1186/s12870-020-02624-9
Karthikeya V, Sankaralingam A, Sevugapperumal N (2006) Management of groundnut root rot with biocontrol agents and organic amendments. Arch Phytopathol Plant Prot 39(3):215–223. https://doi.org/10.1080/03235400500094225
Mohammadi P, Tozlu E, Kotan R, Kotan MS (2017) Potential of some bacteria for biological control of postharvest citrus green mold caused by Penicillum digitatum. Plant Prot Sci 53:1–14. https://doi.org/10.17221/55/2016-PPS
Srivastava P, Sahgal M, Sharma K, Enshasy HE, Gafur A, Alfarraj S, Ansari MJ, Sayyed RZ (2022) Optimization and identification of siderophores produced by Pseudomonas monteilli strain MN759447 and its antagonism towards fungus associated with mortality in Dalbergia sissoo plantation forests. Front Plant Sci 13:984522. https://doi.org/10.3389/fpls.2022.984522/full
Kannepalli A, Davranov K, Narimanov A, Enakiev Y, Syed A, Elgorban AM, Bahkali AH, Wirth S, Sayyed RZ, Gafur A (2021) Co-inoculation of rhizobacteria promotes growth, yield, and nutrient contents in soybean and improves soil enzymes and nutrients under drought conditions. Sci Rep 11:22081. https://doi.org/10.1038/s41598-021-01337-9
Jabborova D, Annapurna K, Azimov A, Tyagi S, Pengani KR, Sharma S, Vikram K, Poczai P, Nasif O, Ansari MJ, Sayyed RZ (2021) Co-inoculation of biochar and arbuscular mycorrhizae for growth promotion and nutrient fortification in soybean under drought conditions. Front Plant Sci 13:947547. https://doi.org/10.3389/fpls.2022.947547
Funding
This project was funded by Researchers Supporting Project Number (RSP2023R367), King Saud University, Riyadh, Saudi Arabia.
Author information
Authors and Affiliations
Contributions
KP and AP conceptualized the problem and planned the experiments, KP and RST carried out work, and KP, RST, AJ, RZS, and AP wrote the manuscript. AS, JPB, and RZS performed the formal analysis and edited the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical Approval
The research involves no human participant or animal.
Consent to Participate
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Paliwal, K., Jajoo, A., Tomar, R.S. et al. Enhancing Biotic Stress Tolerance in Soybean Affected by Rhizoctonia solani Root Rot Through an Integrated Approach of Biocontrol Agent and Fungicide. Curr Microbiol 80, 304 (2023). https://doi.org/10.1007/s00284-023-03404-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00284-023-03404-y