ORIGINAL RESEARCH
Unfavorable Soil Environment for Root-Knot Nematode Infestation: Insights from Metabolomics and Microbial Diversity Analysis in Tomato Rhizosphere Soil
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Aimin Zhang 1,3,4
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Dandan Cao 1,3,4
 
 
 
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1
College of Life Science, Hebei University, Baoding, 071002, China
 
2
Seed Workstation of the Agriculture and Rural Department of Ningxia Hui Autonomous Region, Yinchuan, 750000, China
 
3
Hebei Innovation Center for Bioengineering and Biotechnology, Hebei University, Baoding, 071002, China
 
4
Engineering Research Center of Ecological Safety and Conservation in Beijing-Tianjin-Hebei (Xiong’an New Area) of MOE, Baoding, 071002, China
 
These authors had equal contribution to this work
 
 
Submission date: 2024-04-08
 
 
Final revision date: 2024-08-02
 
 
Acceptance date: 2024-09-21
 
 
Online publication date: 2024-11-06
 
 
Publication date: 2025-11-04
 
 
Corresponding author
Gangyong Zhao   

College of Life Science, Hebei University, Baoding, 071002, China
 
 
Dandan Cao   

College of Life Science, Hebei University, Baoding, 071002, China
 
 
Pol. J. Environ. Stud. 2025;34(6):7689-7701
 
KEYWORDS
TOPICS
ABSTRACT
Plant root-knot disease caused by nematodes is a serious threat to agricultural production worldwide, second only to fungal diseases. Meloidogyne incognita is the most prevalent nematode species among RKN infested vegetables and cash crops. To explore the most potential biocontrol agents for Meloidogyne incognita, this study employed metabolomics and high-throughput sequencing approaches to assess alterations in metabolite profiles and microbial community structures of the rhizosphere soil around tomato (Solanum lycopersicum) roots before and after Meloidogyne incognita infestation. Subsequently, a comprehensive analysis of the metabolome and microbial diversity was conducted to identify differentially accumulated metabolites, microbes, and their correlation with each other. As a result, a total of 51 metabolites and 28 microbial genera exhibited significant differences in abundance between the treatments. Specifically, 27 metabolites were increased in concentration while 24 decreased, and the abundance of 25 bacterial genera and three fungal species was significantly altered. Further analysis revealed that five metabolites, including 5-fluorouridine monophosphate and fusarochromanone, as well as nine microbial genera, such as Bacillus, Streptomyces, and Paenibacillus, exhibited potential correlation with the biocontrol agents. In conclusion, the infestation of tomatoes by M. incognita results in substantial alterations to the metabolite profiles and microbial community structures within the rhizosphere soil. Five of the metabolites and nine microbial genera were identified as potential candidates for biocontrol of M. incognita.
CONFLICT OF INTEREST
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
REFERENCES (31)
1.
SIKANDAR A., JIA L., WU H., YANG S. Meloidogyne enterolobii risk to agriculture, its present status and future prospective for management. Frontiers in Plant Science, 13, 1093657, 2023. https://doi.org/10.3389/fpls.2... PMid:36762171 PMCid:PMC9902769.
 
2.
EL-ASHRY R.M., AIOUB A.A., AWAD S.E. Suppression of Meloiodogyne incognita (Tylenchida: Heteroderidae) and Tylenchulus semipenterans (Tylenchida: Tylenchulidae) using Tilapia fish powder and plant growth promoting rhizobacteria in vivo and in vitro. European Journal of Plant Pathology, 165, 665, 2023. https://doi.org/10.1007/s10658....
 
3.
CUCIO C., ENGELEN A.H., COSTA R., MUYZER G. Rhizosphere Microbiomes of European Seagrasses are selected by the plant, but are not Species Specific. Frontiers in Microbiology, 7, 440, 2016. https://doi.org/10.3389/fmicb.... PMid:27065991 PMCid:PMC4815253.
 
4.
PHILIPPOT L., RAAIJMAKERS J.M., LEMANCEAU P., VAN DER PUTTEN W.H. Going back to the roots: the microbial ecology of the rhizosphere. Nature Reviews Microbiology, 11 (11), 789, 2013. https://doi.org/10.1038/nrmicr... PMid:24056930.
 
5.
HOLMER R., RUTTEN L., KOHLEN W., VAN VELZEN R., GEURTS R. Commonalities in symbiotic plant-microbe signalling. Advances in Botanical Research, 82, 187, 2017. https://doi.org/10.1016/bs.abr... PMCid:PMC5801047.
 
6.
HU L., ROBERT C.A.M., CADOT S., ZHANG X., YE M., LI B. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nature Communications, 9, 2738, 2018. https://doi.org/10.1038/s41467... PMid:30013066 PMCid:PMC6048113.
 
7.
VOGES M., BAI Y., SCHULZE-LEFERT P., SATTELY E.S. Plant-derived coumarins shape the composition of an Arabidopsis synthetic root microbiome. PNAS, 116 (25), 12558, 2019. https://doi.org/10.1073/pnas.1... PMid:31152139 PMCid:PMC6589675.
 
8.
FINKEL O.M., SALAS-GONZÁLEZ I., CASTRILLO G., CONWAY J.M., LAW T.F., TEIXEIRA P.J.P.L. A single bacterial genus maintains root growth in a complex microbiome. Nature, 587 (5832), 103, 2020. https://doi.org/10.1038/s41586... PMid:32999461 PMCid:PMC10329457.
 
9.
PANG Z., CHEN J., WANG T., GAO C., LI Z., GUO L., XU J., CHENG Y. Linking Plant Secondary Metabolites and Plant Microbiomes: A Review. Frontiers in Plant Science, 12, 621276, 2021. https://doi.org/10.3389/fpls.2... PMid:33737943 PMCid:PMC7961088.
 
10.
ALI A.A., EL-ASHRY R.M., AIOUB A.A. Animal manure rhizobacteria cofertilization suppresses phytonematodes and enhances plant production: Evidence from field and greenhouse. Journal of Plant Diseases and Protection, 129 (1), 171, 2021. https://doi.org/10.1007/s41348....
 
11.
FENG Y., RUI L., WANG X., WU X. Adaptation of pine wood nematode, Bursaphelenchus xylophilus, early in its interaction with two Pinus species that differ in resistance. Journal of Forestry Research, 33 (4), 1391, 2022. https://doi.org/10.1007/s11676....
 
12.
ZHAO X., LIN C., TAN J., YANG P., WANG R., QI G. Changes of rhizosphere microbiome and metabolites in Meloidogyne incognita infested soil. Plant and Soil, 483 (1-2), 331, 2023. https://doi.org/10.1007/s11104....
 
13.
TONG W., LI J., CONG W., ZHANG C., XU Z., CHEN X., YANG M., LIU J., YU L., DENG X. Bacterial Community Structure and Function Shift in Rhizosphere Soil of Tobacco Plants Infected by Meloidogyne incognita. Plant Pathology Journal, 38 (6), 583, 2022. https://doi.org/10.5423/PPJ.OA... PMid:36503187 PMCid:PMC9742794.
 
14.
STEEL R., TORRIE J. Principles and procedures of statistics: A biometrical approach MCGraw-Hill Book Company Toronto. Redvet, 13 (6), 481, 2012.
 
15.
KIRIENKO D.R., REVTOVICH A.V., KIRIENKO N.V. A High-Content, Phenotypic Screen Identifies Fluorouridine as an Inhibitor of Pyoverdine Biosynthesis and Pseudomonas aeruginosa Virulence. Msphere, 1, 2017. https://doi.org/10.1128/mSpher... PMid:27579370 PMCid:PMC4999921.
 
16.
HUANG C.Y., CHEN Y.C., WU-HSIEH B.A., FANG J.M., CHANG Z.F. The Ca-loop in thymidylate kinase is critical for growth and contributes to pyrimidine drug sensitivity of Candida albicans. JBC, 294 (27), 10686, 2019. https://doi.org/10.1074/jbc.RA... PMid:31152062 PMCid:PMC6615673.
 
17.
DREAU D., FOSTER M., HOGG M., CULBERSON C., NUNES P., WUTHIER R.E. Inhibitory effects of fusarochromanone on melanoma growth. Anti-Cancer Drugs, 18, 897, 2007. https://doi.org/10.1097/CAD.0b... PMid:17667595.
 
18.
ABDEL-RAHMAN A.A., KESBA H.H., AL-SAYED A.A. Activity and reproductive capability of Meloidogyne incognita and sunflower growth response as influenced by root exudates of some medicinal plants. Biocatalysis and Agricultural Biotechnology, 22, 2020. https://doi.org/10.1016/j.bcab....
 
19.
PIETERSE C.M.J., ZAMIOUDIS C., BERENDSEN R.L., WELLER D.M., VAN WEES S.C.M., BAKKER P.A.H.M. Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology, 52, 347, 2014. https://doi.org/10.1146/annure... PMid:24906124 PMCid:PMC11214898.
 
20.
REINHOLD-HUREK B., BUNGER W., BURBANO C.S., SABALE M., HUREK T. Roots shaping their microbiome: global hotspots for microbial activity. Annual Review of Phytopathology, 53, 403, 2015. https://doi.org/10.1146/annure... PMid:26243728.
 
21.
GOUDA S., KERRY R.G., DAS G., PARAMITHIOTIS S., SHIN H.S., PATRA JK. Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiological Research, 206, 131, 2017. https://doi.org/10.1016/j.micr... PMid:29146250.
 
22.
LUO T., HOU S.S., YANG L., QI G.F., ZHAO X.Y. Nematodes avoid and are killed by Bacillus mycoides-produced styrene. Journal of Invertebrate Pathology, 159, 129, 2018. https://doi.org/10.1016/j.jip.... PMid:30268676.
 
23.
LAMY E., PATUREL C., WINKLER T. Synthesis and reactivity of 4 phenylsul fonamide avermectin B1 and 4 Phenylsul finimineavermectin B1 monosaccharide derivative. Tetrahedron Letters, 47, 5657, 2006. https://doi.org/10.1016/j.tetl....
 
24.
QURESHI S.A., RUQQIA SULTANA V., ARA J., EHTESHAMUL-HAQUE S. Nematicidal potential of culture filtrates of soil fungi associated with rhizosphere and rhizoplane of cultivated and wild plants. Pakistan Journal of Botany, 44 (3), 1041, 2012.
 
25.
PERSHINA E.V., IVANOVA E.A., NAGIEVA A.G., ZHIENGALIEV A.T., CHIRAK E.L., ANDRONOV E.E., SERGALIEV N.K. A Comparative Analysis of Microbiomes in Natural and Anthropogenically Disturbed Soils of Northwestern Kazakhstan. Eurasian Soil Science, 49 (6), 673, 2016. https://doi.org/10.1134/S10642....
 
26.
FUDOU R., JOJIMA Y., IIZUKA T., YAMANAKA S. Haliangium ochraceum gen. nov., sp. nov. and Haliangium tepidum sp. nov.: novel moderately halophilic myxobacteria isolated from coastal saline environments. JGAM, 48 (2), 109, 2020. https://doi.org/10.2323/jgam.4... PMid:12469307 PMCid:PMC10971235.
 
27.
JANG J.H., KIM M.K., SATHIYARAJ S., LEE J., JUYOUNG K., MAENG S., LEE K.E., LEE E.Y., KANG M.S., SATHIYARAJ G. A report of eight unrecorded radiation resistant bacterial species in Korea isolated in 2018. Journal of Species Research, 7 (3), 210, 2018.
 
28.
ZHENG Z.G., ZHENG J.S., LIU H.L., PENG D.H., SUN M. Complete genome sequence of Fictibacillus phosphorivorans G25-29, a strain toxic to nematodes. Journal of Biotechnology, 239, 20, 2016. https://doi.org/10.1016/j.jbio... PMid:27677407.
 
29.
LIU M., XING S.S., YUAN W.D., WEI H., SUN Q.G., LIN X.Z., HUANG H.Q., BAO S.X. Pseudonocardia nematodicida sp nov., isolated from mangrove sediment in Hainan, China. Antonie Van Leeuwenhoek, 108 (3), 571, 2015. https://doi.org/10.1007/s10482... PMid:26115882.
 
30.
DE MENEZES C.B.A., TONIN M.F., SILVA L.J., DE SOUZA W.R., PARMA M., DE MELO L.S., ZUCCHI T.D., DESTEFANO S.A.L., FANTINATTI-GARBOGGINI F. Marmoricola aquaticus sp nov., an actinomycete isolated from a marine sponge. IJSEM, 65, 2286, 2015. https://doi.org/10.1099/ijs.0.... PMid:26231541.
 
31.
LEE S.D., LEE D.W., KO Y.H. Marmoricola korecus sp nov. IJSEM, 61, 1628, 2011. https://doi.org/10.1099/ijs.0.... PMid:20693360.
 
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