Abstract
Meloidogyne incognita is among the most detrimental parasitic nematodes with a wide host range causing huge economic losses annually. Biological control of M. incognita has emerged as a promising alternative in sustainable agriculture. In our previous study, Bacillus velezensis TA-1 effectively controlled M. incognita in vitro and in the field trials through direct nematocidal activities. However, it remains poorly understood for the underlying mechanisms including whether TA-1 could induce host resistance against M. incognita. In the present study, the effects of TA-1 induced resistance against M. incognita in tomato were determined. Results showed that TA-1 colonized tomato roots, with 1.23 × 108 colony forming units (CFU)/g root tissues attached within 36 h, significantly reduced the number of galls in the local and systemic root systems in the split-root experiments by 44.0% and 28.1%, respectively. The bacteria also increased the basic defense responses of tomato plants, such as lignin accumulation and hydrogen peroxide (H2O2) content, which was associated with the enhanced activities of enzymes related to plant defense [e.g. phenylalanine ammonia-lyase (PAL), peroxidase (POD) and polyphenol oxidase (PPO)]. Moreover, TA-1 enhanced the expressions of tomato defense response genes in the salicylic acid (PR1a and PR-P6) and jasmonic acid (PI II and MC) pathways and induced resistance against M. incognita. These results suggested that TA-1 could effectively control M. incognita through induction of tomato resistance, therefore it could be used as a promising biocontrol agent to be incorporated in the integrated management programs in tomato production.
Similar content being viewed by others
References
Antil S, Kumar R, Pathak DV, Kumar A, Panwar A, Kumari A et al (2022) Potential of Bacillus altitudinis KMS-6 as a biocontrol agent of Meloidogyne javanica. J Pest Sci 95:1443–1452. https://doi.org/10.1007/s10340-021-01469-x
Avdiushko SA, Ye XS, Kuc J (1993) Detection of several enzymatic activities in leaf prints cucumber plant. Physiol Mol Plant P 42:441–454. https://doi.org/10.1006/pmpp.1993.1033
Ayaz M, Ali Q, Farzand A, Khan AR, Ling H, Gao X (2021) Nematicidal volatiles from Bacillus atrophaeus GBSC56 promote growth and stimulate induced systemic resistance in tomato against Meloidogyne incognita. Int J Mol Sci 22:5049. https://doi.org/10.3390/ijms22095049
Back MA, Haydock PPJ, Jenkinson P (2002) Disease complexes involving plant parasitic nematodes and soilborne pathogens. Plant Pathol 51:683–697. https://doi.org/10.1046/j.1365-3059.2002.00785.x
Chen J, Li Q, Song B (2020) Chemical nematicides: recent research progress and outlook. J Agr Food Chem 68:12175–12188. https://doi.org/10.1021/acs.jafc.0c02871
Chen CQ, Belanger RR, Benhamou N, Paulita TC (2000) Defense enzymes induced in cucumber roots by treatment with plant growth-promoting rhizobacteria (PGPR) and Pythium aphanidermatum. Physiol Mol Plant P 56:13–23. https://doi.org/10.1006/pmpp.1999.0243
Cheng X, Ji X, Li J, Qi W, Qiao K (2019) Characterization of antagonistic Bacillus methylotrophicus isolated from rhizosphere and its biocontrol effects on maize stalk rot. Phytopathology 109:571–581. https://doi.org/10.1094/PHYTO-07-18-0220-R
Cottyn B, Baeyen S, Pauwelyn E, Verbaendert I, Vos PD, Bleyaert P et al (2011) Development of a real-time PCR assay for Pseudomonas cichorii, the causal agent of midrib rot in greenhouse grown lettuce, and its detection in irrigating water. Plant Pathol 60:453–461. https://doi.org/10.1111/j.1365-3059.2010.02388.x
Desmedt W, Mangelinckx S, Kyndt T, Vanholme B (2020) A phytochemical perspective on plant defense against nematodes. Front Plant Sci 11:602079. https://doi.org/10.3389/fpls.2020.602079
Dutta S, Podile AR (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36(3):232–244. https://doi.org/10.3109/10408411003766806
Ebone LA, Kovaleski M, Deuner CC (2019) Nematicides: history, mode, and mechanism action. Plant Sci Today 6(2):91–97. https://doi.org/10.14719/pst.2019.6.2.468.
Engelbrecht G, Horak I, Rensburg PJJV, Claasens N (2018) Bacillus-based bionematicides: development, modes of action and commercialisation. Biocontrol Sci Technol 2:629–653. https://doi.org/10.1080/09583157.2018.1469000
Fan Z, Du Y, **ong Y, Liu Y, Li B, Wu T et al (2022) Biological control of M. javanica in tomato and induction of host resistance using Bacillus cereus in vitro, green house and field. Biol Control 175:105036. https://doi.org/10.1016/j.biocontrol.2022.105036
FAOSTAT, Food and Agriculture Organization of the United Nations (2023).Data of crop production. http://www.fao.org/faostat/en/#data/QC
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239–247. https://doi.org/10.1038/35041687
Fujimoto T, Mizukubo T, Abe H, Seo S (2015) Sclareol induces plant resistance to root-knot nematode partially through ethylene-dependent enhancement of lignin accumulation. Mol Plant Microbe Interact 28(4):398–407. https://doi.org/10.1094/MPMI-10-14-0320-R
Horak I, Engelbrecht G, van Rensburg PJJ, Claassens S (2019) Microbial metabolomics: essential definitions and the importance of cultivation conditions for utilizing Bacillus species as bionematicides. J Appl Microbiol 127:2. https://doi.org/10.1111/jam.14218
Hu H, Chen Y, Wang Y, Tang Y, Chen S, Yan S (2017) Endophytic Bacillus cereus effectively controls Meloidogyne incognita on tomato plants through rapid rhizosphere occupation and repellent action. Plant Dis 101(3):448–455. https://doi.org/10.1094/PDIS-06-16-0871-RE
Hu H, Gao Y, Li X, Chen S, Yan S, Tian X (2020) Identification and nematicidal characterization of proteases secreted by endophytic bacteria Bacillus cereus BCM2. Phytopathology 110(2):336–344. https://doi.org/10.1094/PHYTO-05-19-0164-R
Hu Y, You J, Wang Y, Long Y, Wang S, Pan F et al (2022) Biocontrol efficacy of Bacillus velezensis strain YS-AT-DS1 against the root-knot nematode Meloidogyne incognita in tomato plants. Front Microbiol 13:1035748. https://doi.org/10.3389/fmicb.2022.1035748
Huang H, Ullah F, Zhou DX, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci 10:800. https://doi.org/10.3389/fpls.2019.00800
Hussey R (1973) A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis Rep 57:1025–1028
Ji X, Li J, Meng Z, Li N, Dong B, Zhang S, Qiao K (2020) Fluopimomide effectively controls Meloidogyne incognita and shows a growth promotion effect in cucumber. J Pest Sci 93:1421–1430. https://doi.org/10.1007/s10340-020-01247-1
Jones J, Haegeman A, Danchin E, Gaur H, Helder J, Jones M et al (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961. https://doi.org/10.1111/mpp.12057
Kamalanathan V, Sevugapperumal N, Nallusamy S (2023) Antagonistic bacteria Bacillus velezensis VB7 possess nematicidal action and induce an immune response to suppress the infection of root-knot nematode (RKN) in tomato. Genes 14(7):1335. https://doi.org/10.3390/genes14071335
Kloepper J, Ryu C, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266. https://doi.org/10.1094/PHYTO.2004.94.11.1259
Li X, Hu H, Li J, Wang C, Chen S, Yan S (2019) Effects of the endophytic bacteria Bacillus cereus BCM2 on tomato root exudates and Meloidogyne incognita infection. Plant Dis 103(7):1551–1558. https://doi.org/10.1094/PDIS-11-18-2016-RE
Li J, Meng Z, Li N, Ji X, Dong B, Zhang S et al (2020) Evaluating a new non-fumigant nematicide fluopimomide for management of southern root-knot nematodes in tomato. Crop Prot 129:105040. https://doi.org/10.1016/j.cropro.2019.105040
Liu H, Fu G, Li Y, Zhang S, Ji X, Qiao K (2023) Biocontrol efficacy of Bacillus methylotrophicus TA-1 against Meloidogyne incognita in tomato. Plant Dis 107:2709–2715. https://doi.org/10.1094/PDIS-12-22-2801-RE
Livak KJ, Schmittgen TD (2002) Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V et al (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601. https://doi.org/10.1093/jxb/erq089
Martínez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CM, Van Wees SC (2017) Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213:1363–1377. https://doi.org/10.1111/nph.14251
Mellersh DG, Foulds IV, Higgins VJ, Heath MC (2002) H2O2 plays different roles in determining penetration failure in three diverse plant–fungal interactions. Plant J 29:257–268. https://doi.org/10.1046/j.0960-7412.2001.01215.x
Morrison IM (1972) A semi-micro methods for the determination if lignin and its use in predicting the digestibility of forage crops. J Sci Food Agric 23:455–463. https://doi.org/10.1002/jsfa.2740310704
Ongena M, Jacques P (2008) Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends Microbiol 16:115–125. https://doi.org/10.1016/j.tim.2007.12.009
Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492. https://doi.org/10.1016/0003-2697(84)90039-3
Peng G, Zhao X, Li Y, Wang R, Huang Y, Qi G (2019) Engineering Bacillus velezensis with high production of acetoin primes strong induced systemic resistance in Arabidopsis thaliana. Microbiol Res 227:126297. https://doi.org/10.1016/j.micres.2019.126297
Phani V, Gowda MT, Dutta TK (2023) Grafting vegetable crops to manage plant-parasitic nematodes: a review. J Pest Sci. https://doi.org/10.1007/s10340-023-01658-w
Pires D, Vicente C, Menéndez E, Faria J, Rusinque L, Camacho M et al (2022) The fight against plant-parasitic nematodes: current status of bacterial and fungal biocontrol agents. Pathogens 11:1178. https://doi.org/10.3390/pathogens11101178
Rao M, Kamalnath M, Umamaheswari R, Ra**ikanth R, Prabu P, Priti K et al (2017) Bacillus subtilis IIHR BS-2 enriched vermicompost controls root knot nematode and soft rot disease complex in carrot. Sci Hortic 218:56–62. https://doi.org/10.1016/j.scienta.2017.01.051
Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Goreti M et al (2011) A herbivore that manipulates plant defence. Ecol Lett 14:229–236. https://doi.org/10.1111/j.1461-0248.2010.01575.x
Siddiqui ZA, Mahmood I (1999) Role of bacteria in the management of plant-parasitic nematodes: a review. Bioresour Technol 69:167–179. https://doi.org/10.1016/S0960-8524(98)00122-9
Silva JC, Nunes TC, Guimarães RA, Pylro VS, Costa LS, Zaia R et al (2022) Organic practices intensify the microbiome assembly and suppress root-knot nematodes. J Pest Sci 95(2):709–721. https://doi.org/10.1007/s10340-021-01417-9
Simonetti E, Veronico P, Melillo MT, Delibes A, Andrés MF, López-Brana I (2009) Analysis of class III peroxidase genes expressed in roots of resistant and susceptible wheat lines infected by Heterodera avenae. Mol Plant Microbe Interact 22:1081–1092. https://doi.org/10.1094/MPMI-22-9-1081
Stenberg JA, Sundh I, Becher PG, Björkman C, Dubey M, Egan PA et al (2021) When is it biological control? A framework of definitions, mechanisms, and classifications. J Pest Sci 94(3):665–676. https://doi.org/10.1007/s10340-021-01354-7
Tian X, Zhao X, Zhao S, Zhao J, Mao Z (2022) The biocontrol functions of Bacillus velezenis strain Meloidogyne incognita. Front Microbiol 13:843041. https://doi.org/10.3389/fmicb.2022.843041
Uppalapati SR, Ayoubi P, Weng H, Palmer DA, Mitchell RE, Jones W et al (2005) The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 42:201–217. https://doi.org/10.1111/j.1365-313X.2005.02366.x
Walters D, Walsh D, Newton A, Lyon G (2005) Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 95:1368–1373. https://doi.org/10.1094/PHYTO-95-1368
Wright HD (1934) The preparation of nutrient agar with special reference to pneumococci, streptococci and other gram-positive organisms. J Pathol Bacteriol 39:359–373. https://doi.org/10.1002/path.1700390210
Yan Y, Mao Q, Wang Y, Zhao J, Fu Y, Yang Z et al (2021) Trichoderma harzianum induces resistance to root-knot nematodes by increasing secondary metabolite synthesis and defense-related enzyme activity in Solanum lycopersicum L. Biol Control 158:104609. https://doi.org/10.1016/j.biocontrol.2021.104609
Yang J, Park S, Lee H, Nam K, Lee K, Lee J et al (2023) Differential responses of antioxidant enzymes and lignin metabolism in susceptible and resistant sweetpotato cultivars during root-knot nematode infection. Antioxidants 12(6):1164. https://doi.org/10.3390/antiox12061164
Zhuang X, Zhao J, Bai M, ** X, Li Y, Yang Y et al (2021) Pochonia chlamydosporia isolate PC-170-induced expression of marker genes for defense pathways in tomatoes challenged by different pathogens. Microorganisms 9(9):1882. https://doi.org/10.3390/microorganisms9091882
Acknowledgements
This work was supported by Shandong Innovation Capability Enhancement Project for Technological Small and Medium sized Enterprises (2023TSGC0613), Shandong Provincial Natural Science Foundation (ZR2021MC065), Special Fund Project for Guiding Local Scientific and Technological Development by the Central Government (YDZX2022121), and National Natural Science Foundation of China (31601661).
Funding
This research is funded by Natural Science Foundation of Shandong Province, ZR2021MC065, ZR2021MC065, ZR2021MC065, ZR2021MC065, ZR2021MC065.
Author information
Authors and Affiliations
Contributions
KQ and ZW conceived and designed research. XJ, BL, SZ, MF conducted experiments and analyzed data. All authors contributed with the discussion of the results. KQ and YL supervised the research. KQ and SZ wrote and revised the paper. All authors read and approved this manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Aurelio Ciancio.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Ji, X., Liu, B., Fan, M. et al. Biocontrol of Meloidogyne incognita by Bacillus velezensis TA-1 through induction of host resistance in tomato. J Pest Sci (2024). https://doi.org/10.1007/s10340-024-01742-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10340-024-01742-9