Synergistic effects of endophytic bacteria and silicon on controlling common bacterial blight disease in beans

Abstract

Enhancing the effectiveness of environmentally friendly and sustainable practices in plant disease management is crucial for promoting their wider adoption and use. In this context, the combined use of bacterial biocontrol agents and silicon applications holds significant potential. This study aimed to evaluate the effects of individual and combined applications of endophytic bacteria (EB) and silicon on controlling common leaf blight disease caused by Xanthomonas axonopodis pv. phaseoli (Xap) in beans. Additionally, the effects of these treatments on plant biomass and chlorophyll content were investigated. Bean plants (Phaseolus vulgaris cv. Gina) were grown in a peat/perlite medium under soilless conditions in a climate chamber. Silicon dioxide (SiO₂) (30 mM) and endophytic bacteria were applied to the root collar using the drenching method. The pathogen Xap was inoculated by spraying the leaves, and disease severity was assessed using a 1–5 scale. Plant growth parameters were also recorded. Among the tested EB isolates, Pseudomonas caspiana V30G2 was the most effective in suppressing disease severity. Disease severity was reduced by 31% with V30G2 and by 21% with SiO₂ when applied individually. Notably, the combined application of both agents exhibited a synergistic effect, reducing disease severity by 55%. Although some improvements were observed in specific parameters, such as leaf number, neither the individual nor the combined treatments significantly influenced overall plant biomass or chlorophyll content. Nevertheless, the results suggest that the combined application of silicon and endophytic bacteria, when appropriately selected, has significant potential for environmentally friendly and sustainable disease management, enhancing the disease suppression efficacy of each treatment.

Keywords

• biocontrol
• Xanthomonas axonopodis pv. phaseoli
• Pseudomonas caspiana
• silicon dioxide

Fasulye bakteriyel adi yanıklık hastalığının kontrolünde endofitik bakteri ve silisyumun sinerjistik etkileri

Abstract

Bitki hastalıklarının yönetiminde çevre dostu ve sürdürülebilir uygulamaların etkinliğini artırmak, onların daha geniş çapta benimsenmesi ve kullanımını teşvik etmek için çok önemlidir. Bu bağlamda, bakteriyel biyokontrol ajanları ile silisyumun (Si) birlikte kullanılması önemli bir potansiyel taşımaktadır. Bu çalışma, fasulyelerde Xanthomonas axonopodis pv. phaseoli (Xap)’nin neden oluğu adi yaprak yanıklığı hastalığının kontrolünde Endofitik Bakteriler (EB) ve silisyumun teksel ve birlikte uygulamalarının etkilerini belirlemeyi amaçlamıştır. Ek olarak, bu uygulamaların bitki biyokütlesi ve klorofil içeriği üzerindeki etkileri araştırılmıştır. Fasulye (Phaseolus vulgaris cv. Gina) fideleri, iklim odasında topraksız tarım sisteminde torf ve perlitten oluşan yetiştirme ortamında geliştirilmiştir. Silisyum dioksit (SiO₂) (30 mM) ve EB, içirme yöntemi kullanılarak kök boğazına uygulanmıştır. Patojen Xap, yapraklara püskürtülerek uygulanmış ve hastalık şiddeti 1-5 skalası kullanılarak değerlendirilmiştir. Test edilen EB arasında, Pseudomonas caspiana V30G2 hastalık şiddetini baskılamada en etkili izolat olmuştur. Teksel uygulamalarda hastalığın şiddeti V30G2 ile %31, SiO₂ ile %21 düzeyinde azaltılmıştır. Ancak, her iki etkenin birlikte uygulanması sinerjistik bir etki göstererek hastalık şiddetini %55 oranında azaltmıştır. Yaprak sayısı gibi belirli parametrelerde bazı pozitif etkiler gözlemlenmiş fakat ne tek başına ne de birlikte yapılan uygulamalar genel bitki biyokütlesini veya klorofil içeriğini önemli ölçüde etkilememiştir. Sonuç olarak, uygun şekilde seçilmiş silikon ve endofitik bakterilerin birlikte uygulanmasının çevre dostu ve sürdürülebilir hastalık yönetimi için önemli bir potansiyele sahip olduğunu ve her bir uygulamanın hastalık baskılama etkinliğini artırdığını göstermektedir.

Keywords

• biyokontrol
• Xanthomonas axonopodis pv. phaseoli
• Pseudomonas caspiana
• silisyum dioksit

References

1. Akköprü A., 2020. Potential using of transgenerational resistance against common bacterial blight in Phaseolus vulgaris. Crop Protection, 127, 104967. https://doi.org/10.1016/j.cropro.2019.104967
2. Akköprü A., Akat Ş., Özaktan H., Gül A., Akbaba M., 2021. The long-term colonization dynamics of endophytic bacteria in cucumber plants, and their effects on yield, fruit quality and angular leaf spot disease. Scientia Horticulturae, 282, 110005. doi:10.1016/j.scienta.2021.110005
3. Alattas H., Glick B.R., Murphy D.V., Scott C., 2024. Harnessing Pseudomonas spp. for sustainable plant crop protection. Frontiers in Microbiology, 15:1485197. https://doi.org/10.3389/fmicb.2024.1485197
4. Andrade C.C.L., Resende R.S., Rodrigues F.A., Ferraz H.G.M., Moreira W. R., Oliveira J.R., Marian R.L.R., 2013. Silicon reduces bacterial speck development on tomato. Tropical Plant Pathology, 38 (5), 436–442. https://doi.org/10.1590/S1982-56762013005000021
5. Babier Y., Akköprü A., 2020. Çeşitli kültür bitkilerinden izole edilen endofitik bakterilerin karakterizasyonu ve bitki patojeni bakterilere karşı antagonistik etkilerinin belirlenmesi. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi, 30 (3), 521–534. https://doi.org/10.29133/yyutbd.727138
6. Belete T., Bastas K.K., Francesconi S., Balestra G.M., 2021. Biological effectiveness of Bacillus subtilis on common bean bacterial blight. Journal of Plant Pathology, 103 (1), 249–258. https://doi.org/10.1007/s42161-020-00727-8
7. Bolwerk A., Lagopodi A.L., Wijfjes A.H., Lamers G.E., Chin-A-Woeng T.F., Lugtenberg B.J., Bloemberg G.V., 2003. Interactions in the tomato rhizosphere of two Pseudomonas biocontrol strains with the phytopathogenic fungus Fusarium oxysporum f.sp. radicis-lycopersici. Molecular Plant-Microbe Interactions, 16 (11), 983–993. https://doi.org/10.1094/MPMI.2003.16.11.983
8. Bozkurt I.A., 2009. Fasulye bakteriyel yanıklık hastalığına (Xanthomonas axonopodis pv. phaseoli) karşı antagonistik bakterilerle mücadele olanakları. Ege Üniversitesi Fen Bilimleri Enstitüsü, Basılmamış Doktora Tezi, 171 s., İzmir.

9. Cai K., Gao D., Luo S., Zeng R., Yang J., Zhu X., 2008. Physiological and cytological mechanisms of silicon-induced resistance in rice against blast disease. Physiologia Plantarum, 134 (2), 324–333. https://doi.org/10.1111/j.1399-3054.2008.01140.x
10. Chérif M., Asselin A., Bélanger R.R., 1994. Defense responses induced by soluble silicon in cucumber roots infected by Pythium spp. Phytopathology, 84, 236–242. https://doi.org/10.1094/Phyto-84-236
11. Corrêa B.O., Soares V.N., Sangiogo M., de Oliveira J.R., Moura A.B., 2017. Interaction between bacterial biocontrol-agents and strains of Xanthomonas axonopodis pv. phaseoli effects on biocontrol efficacy of common blight in beans. African Journal of Microbiology Research, 11 (32), 1294–1302. https://doi.org/10.5897/AJMR2017.8565
12. Çelik R., 2021. Endofit bakteri ve silisyum dioksitin fasulyede adi yaprak yanıklığı (Xanthomonas axonopodis pv. phaseoli) üzerine etkileri. Van Yüzüncü Yıl Üniversitesi, Fen Bilimleri Enstitüsü, Basılmamış Yüksek Lisans Tezi, 92 s., Van.
13. Çelik R., Akköprü A., 2025. Evaluating the control potential of silicon dioxide against Xanthomonas axonopodis pv. phaseoli in beans. Turkish Journal of Agriculture - Food Science and Technology. In print.
14. Duman K., Soylu S., 2019. Characterization of plant growth-promoting traits and antagonistic potentials of endophytic bacteria from bean plants against Pseudomonas syringae pv. phaseolicola. Bitki Koruma Bülteni, 59 (3), 59–69. https://doi.org/10.16955/bitkorb.597214
15. Ertekin D.Ç., Çalış Ö., Yanar Y., 2016. Orta Karadeniz Bölgesi’nde Pseudomonas savastanoi pv. phaseolicola ve Xanthomonas axonopodis pv. phaseoli’nin izolasyonu ve tanılanması. Mediterranean Agricultural Sciences, 34 (1), 25–32. https://doi.org/10.29136/mediterranean.776787
16. Etesami H., 2024. Enhancing crop disease management through integrating biocontrol bacteria and silicon fertilizers: challenges and opportunities. Journal of Environmental Management, 371, 123102. doi: 10.1016/j.jenvman.2024.123102
17. Etesami H., Jeong B.R., 2022. Biodissolution of silica by rhizospheric silicate-solubilizing bacteria-chapter 19. In: silicon and nano-silicon in environmental stress management and crop quality improvement. Etesami H., Al Saeedi A.H., El-Ramady H., Fujita M., Pessarakli M., Hossain M.A. (Eds.). Academic Press, London, 265–276 p.
18. Etesami H., Jeong B.R., Glick B.R., 2021. Contribution of arbuscular mycorrhizal fungi, phosphate-solubilizing bacteria, and silicon to P uptake by plant. Frontiers in Plant Science, 12:699618. https://doi.org/10.3389/fpls.2021.699618
19. FAO, 2023. Food and Agriculture Organization of the United Nations. http://www.fao.org/faostat/en/#data/QC (accessed date: 01.04.2025).
20. Fauteux F., Remus-Borel W., Menzies J.G., Bélanger R.R., 2005. Silicon and plant disease resistance against pathogenic fungi. FEMS Microbiology Letters, 249 (1), 1–6. https://doi.org/10.1016/j.femsle.2005.06.022
21. Fortunato A.A., Rodrigues F.A., Datnoff L.E., 2015. Silicon control of soil-borne and seed-borne diseases. In: Silicon and Plant Diseases. Rodrigues F.A., Datnoff L.E. (Eds.). Springer, Cham, 39–59. https://doi.org/10.1007/978-3-319-22930-0_3
22. Gilbertson R.L., Maxwell D.P., 1992. Common blight of bean. In: Diseases of international importance. Vol 2. Chaube, H.S., Kumar, J.,, Mukhopadyay, A.N., Singh, U.S. (Eds.). Prentice Hall, Inglewood Cliffs, New Jersey. 18–39.
23. Grobelak A., Napora A., Kacprzak M., 2015. Using plant growth-promoting rhizobacteria (PGPR) to improve plant growth. Ecological Engineering, 84, 22–28. https://doi.org/10.1016/j.ecoleng.2015.07.019
24. Guerriero G., Hausman J-F., Legay S., 2016. Silicon and the plant extracellular matrix. Frontiers in Plant Science, 7: 463. doi:10.3389/fpls.2016.00463
25. Guével M.H., Menzies J.G., Bélanger R.R., 2007. Effect of root and foliar applications of soluble silicon on powdery mildew control and growth of wheat plants. European Journal of Plant Pathology, 119, 429–436. https://doi.org/10.1007/s10658-007-9181-1
26. Hallmann J., Quadt-Hallmann A., Mahaffee W.F., Kloepper J.W., 1997. Bacterial endophytes in agricultural crops. Journal of Microbiology, 43 (10), 895–914. https://doi.org/10.1139/m97-131
27. Hardoim P.R., Van Overbeek L.S., Van Elsas D.J., 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiology, 16 (10), 463–471. doi: 10.1016/j.tim.2008.07.008
28. Hoagland D.R., Arnon D.I., 1950. The water-culture method for growing plants without soil. California College Agricultural Experiment Station Circular, 347, Berkeley.
29. İmriz G., Özdemir F., Topal İ., Ercan B., Taş M.N., Yakışır E., Okur O., 2014. Bitkisel üretimde bitki gelişimini teşvik eden rizobakteri (PGPR)'ler ve etki mekanizmaları. Elektronik Mikrobiyoloji Dergisi, 12 (2), 1–19.
30. Kamilova F., Validov S., Azarova T., Mulders I., Lugtenberg B., 2005. Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environmental Microbiology, 7 (11), 1809–1817. https://doi.org/10.1111/j.1462-2920.2005.00889.x
31. Karavina C., Mandumbu R., Parwada C., Tibugari H., 2011. A review of the occurrence, biology and management of common bacterial blight. Journal of Agricultural Technology, 7(6), 1459–1474.
32. Khan M.R., Siddiqui Z.A., 2020. Use of silicon dioxide nanoparticles for the management of Meloidogyne incognita, Pectobacterium betavasculorum and Rhizoctonia solani disease complex of beetroot (Beta vulgaris L.). Scientia Horticulturae, 265, 109211. https://doi.org/10.1016/j.scienta.2020.109211
33. Kim S.G., Kim K.W., Park E.W., Choi D., 2002. Silicon-induced cell wall fortification of rice leaves: a possible cellular mechanism of enhanced host resistance to blast. Phytopathology, 92 (10), 1095–1103. doi: 10.1094/PHYTO.2002.92.10.1095
34. Kubi H.A.A., Khan M.A., Adhikari A., Imran M., Kang S.-M., Hamayun M., Lee I.-J., 2021. Silicon and plant growth-promoting rhizobacteria Pseudomonas psychrotolerans CS51 mitigates salt stress in Zea mays L. Agriculture, 11 (3), 272. https://doi.org/10.3390/agriculture11030272
35. Luyckx M., Hausman J-F., Lutts S., Guerriero G., 2017. Silicon and plants: current knowledge and technological perspectives. Frontiers in Plant Science, 8, 411. https://doi.org/10.3389/fpls.2017.00411
36. Ma J.F., 2004. Role of silicon in enhancing the resistance of plants to biotic and abiotic stresses. Soil Science and Plant Nutrition, 50, 11-18. https://doi.org/10.1080/00380768.2004.10408447
37. Mahmood S., Daur I., Al-Solaimani S.G., Ahmad S., Madkour M.H., Yasir M., Hirt H., Ali S., Ali Z., 2016. Plant growth promoting rhizobacteria and silicon synergistically enhance salinity tolerance of mung bean. Frontiers in Plant Science, 7, 876. https://doi.org/10.3389/fpls.2016.00876
38. Mercado-Blanco J., Lugtenberg B.J., 2014. Biotechnological applications of bacterial endophytes. Current Biotechnology, 3 (1), 60–75.
39. Olur Ü., 2019. Tuzlu ortamda gelişen bitkilerden izole edilen endofit bakterilerin hıyar bitkisinde köşeli yaprak leke hastalığı (Pseudomonas syringae pv. lachrymans), tuz stresi ve bitki gelişimine etkileri. Van Yüzüncü Yıl Üniversitesi, Fen Bilimleri Enstitüsü, Yüksek lisans tezi, 87 s., Van.
40. Opio A.F., Allen D.J., Teri J.M., 1996. Pathogenic variation in Xanthomonas campestris pv. phaseoli, the causal agent of common bacterial blight in Phaseolus beans. Plant Pathology, 45 (6), 1126–1133.
41. Osdaghi E., 2014. Occurrence of common bacterial blight on mung bean (Vigna radiata) in Iran caused by Xanthomonas axonopodis pv. phaseoli. New Disease Reports, 30 (1), 9.
42. https://doi.org/10.5197/j.2044-0588.2014.030.009
43. Park S.J., Rupert T., Anderson T.R., 1999. White mold: germplasm screening under various field conditions in Ontario. Annual Report of the Bean Improvement Cooperative, 42, 51–52.
44. Polanco L.R., Rodrigues F.A., Nascimento K.J.T., Shulman P., Silva L.C., Neves F.W., Vale F.X.R., 2012. Biochemical aspects of bean resistance to anthracnose mediated by silicon. Annals of Applied Biology, 161 (2), 140–150. https://doi.org/10.1111/j.1744-7348.2012.00558.x
45. Rajput V.D., Minkina T., Feizi M., Kumari A., Khan M., Mandzhieva S., Sushkova S., El-Ramady H., Verma K.K., Singh A., van Hullebusch E.D., Singh R.K., Jatav H.S., Choudhary R., 2021. Effects of silicon and silicon-based nanoparticles on rhizosphere microbiome, plant stress and growth. Biology, 10 (8), 791. https://doi.org/10.3390/biology10080791
46. Raturi G., Sharma Y., Rana V., Thakral V., Myaka B., Salvi P., Singh M., Dhar H., Deshmukh R., 2021. Exploration of silicate solubilizing bacteria for sustainable agriculture and silicon biogeochemical cycle. Plant Physiology and Biochemistry, 166, 827–838. doi: 10.1016/j.plaphy.2021.06.039
47. Rezakhani L., Motesharezadeh B., Tehrani M.M., Etesami H., Hosseini H.M., 2022. The effect of silicon fertilization and phosphate-solubilizing bacteria on chemical forms of silicon and phosphorus uptake by wheat plant in a calcareous soil. Plant and Soil, 477, 259–280. https://doi.org/10.1007/s11104-021-05274-4
48. Rodrigues F., Dallagnol L.J., Duarte H.S.S., Datnoff L.E., 2015. Silicon control of foliar diseases in monocots and dicots. In: Silicon and plant diseases. Rodrigues, F., Datnoff, L. (Eds.). Springer, Cham. https://doi.org/10.1007/978-3-319-22930-0_4
49. Romano I., Ventorino V., Pepe O., 2020. Effectiveness of plant beneficial microbes: overview of the methodological approaches for the assessment of root colonization and persistence. Frontiers in Plant Science, 11, 6. https://doi.org/10.3389/fpls.2020.00006
50. Rudolph K., 1993. Infection of the plant by Xanthomonas. In: Xanthomonas. Swings, J.G., Civerolo, E.L. (Eds.). Chapman and Hall, London, 193–264.
51. Saettler A.W., 1989. The need for detection assay, detection of bacteria in seed and other planting material. In: Detection of bacteria in seed and other planting material. Saettler, A.W., Schaad, N.W., Roth, D.A. (Eds.). APS Press, 122 p.
52. Sahebi M., Hanafi M.M., Siti Nor Akmar A., Rafii M.Y., Azizi P., Tengoua F.F., Nurul Mayzaitul Azwa J., Shabanimofrad M., 2015. Importance of silicon and mechanisms of biosilica formation in plants. Biomed Research International, 2015, 396010. https://doi.org/10.1155/2015/396010
53. Sallam N.M.A., Aldayel M.F., 2025. Synergistic effects of Rahnella aquatilis and Trichoderma orientale in biocontrol of common bacterial blight in bean. Egyptian Journal of Biological Pest Control, 35, 9. https://doi.org/10.1186/s41938-025-00847-2
54. Santoyo G., Moreno-Hagelsieb G., del Carmen Orozco-Mosqueda M., Glick B.R., 2016. Plant growth-promoting bacterial endophytes. Microbiological Research, 183, 92–99. https://doi.org/10.1016/j.micres.2015.11.008
55. Savant N.K., Snyder G.H., Datnoff L.E., 1997. Silicon management and sustainable rice production. In: Advances in agronomy. Sparks, D.L. (Ed.). Academic Press, San Diego, CA, USA, 58, 151–199. https://doi.org/10.1016/S0065-2113(08)60255-2
56. Schwartz H.F., Gent D.H., Franc G.D., Harveson R.M., 2007. Dry bean, disease, common bacterial blight. High Plains IPM Guide, a cooperative effort of the University of Wyoming, University of Nebraska, Colorado State University, and Montana State University.
57. Sharma S.B., Sayyed R.Z., Trivedi M.H., Gobi T.A., 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus, 2, 587. doi: 10.1186/2193-1801-2-587
58. Shetty R., Frette X., Jensen B., Shetty N.P., Jensen J.D., Jørgensen H.J.L., NewmanM.A., Christensen L.P., 2011. Silicon-induced changes in antifungal phenolic acids, flavonoids, and key phenylpropanoid pathway genes during the interaction between miniature roses and the biotrophic pathogen Podosphaera pannosa. Plant Physiology, 157 (4), 2194–2295. https://doi.org/10.1104/pp.111.185215
59. Siddiqui Z.A., Hashmi A., Khan M.R., Parveen A., 2020. Management of bacteria Pectobacterium carotovorum, Xanthomonas campestris pv. carotae, and fungi Rhizoctonia solani, Fusarium solani and Alternaria dauci with silicon dioxide nanoparticles on carrot. International Journal of Vegetable Science, 26 (6), 547–557. https://doi.org/10.1080/19315260.2019.1675843
60. Sistani K.R., Savant N.K., Reddy K.C., 1997. Effect of rice hull ash silicon on rice seedling growth. Journal of Plant Nutrition, 20 (1), 195–201. https://doi.org/10.1080/01904169709365242
61. Spadaro D., Gullino M.L., 2005. Improving the efficacy of biocontrol agents against soilborne pathogens. Crop Protection, 24 (7), 601–613. https://doi.org/10.1016/j.cropro.2004.11.003
62. Townsend G.R., Heuberger J.W., 1943. Methods for estimating losses caused by diseases in fungicide experiments. The Plant Disease Reporter, 27, 340-343.
63. Verma K.K., Song X.P., Li D.M., Singh M., Wu J.M., Singh R.K., Sharma A., Zhang B.Q., Li Y.R., 2022. Silicon and soil microorganisms improve rhizospheric soil health with bacterial community, plant growth, performance, and yield. Plant Signaling & Behavior, 17 (1), 2104004. doi: 10.1080/15592324.2022.2104004
64. Vidaver A., 1993. Xanthomonas campestris pv. phaseoli: cause of common bacterial blight of bean. In: Xanthomonas. Swings, J.G., Civerolo, E.L. (Eds.). London, UK: Chapman & Hall, 40-44.