Abstract
Plasmodiophora brassicae Woronin is responsible for an infectious disease called clubroot, which poses a significant threat to cruciferous vegetables. This study aimed to determine the efficacy of biological agents including Trichoderma harzianum and Sophora flavescens in reducing clubroot severity in Pak choi. For this purpose, an in vitro pot experiment was conducted. For the application of T. harzianum (MD), 10 g powder was mixed in each pot with the substrate, while 5 mL (from the diluted solution 5 mL/L) of S. flavescens (RD), and 20 mL (from the diluted solution 500 µL/L) of fluazinam (ZD) was applied around the root of every plant along with clubroot pathogen P. brassicae. The results revealed that the clubroot disease index (DI) efficiently reduced by the application of T. harzianum and S. flavescens up to 36.02%, 45.43%, as compared to positive control fluazinam 49.05%, respectively. Moreover, under clubroot stress T. harzianum increased total chlorophyll contents, total carotenoid contents, shoot diameter, leaf number, fresh weight of shoot by 15.33%, 21.21%, 21.83%, 25%, 14.24%, and enzymatic activities of peroxidase (POD), catalase (CAT), superoxide dismutase (SOD) increased by 14.85%, 21.76% and 19.22%, respectively, as compared to fluazinam. Additionally, the 16S rRNA gene sequence of endophytic bacterial communities under clubroot stress revealed that plants treated with P. brassicae only (D) increased the relative abundance of phylum Proteobacteria by 82% as compared to fluazinam (67%). Beta diversity distance matrix analysis based on the principal coordinate algorithm (PCoA) and Non-metric multidimensional scaling method showed a significant distance between T. harzianum and other applied treatments. Overall, T. harzianum and S. flavescens affected and structured the bacterial community in Pak choi and efficiently reduced the clubroot disease. This study will facilitate researchers to biologically control cruciferous clubroot and their ecological functions with endophytic bacteria in brassica species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data can be provided by the corresponding author on demand.
References
Adetunji CO, Anani OA (2020) Bio-fertilizer from Trichoderma: Boom for agriculture production and management of soil and root borne plant pathogens. Innovations in Food Technology Current Perspectives and Future Goals. Springer, Singapore, pp 242–256
Andrzejak R, Janowska B (2022) Trichoderma spp. improves flowering, quality, and nutritional status of ornamental plants. Int J Mol Sci 23(24):15662. https://doi.org/10.3390/ijms232415662
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1007/978-981-15-6121-4
Arie T, Kobayashi Y, Kono Y, Gen O, Yamaguchi I (1999) Control of clubroot of crucifers by Phoma glomerata and its product epoxydon. Pestic Sci 55(5):602–604. https://doi.org/10.1002/(SICI)1096-9063
Arif S, Liaquat F, Yang S, Shah IH, Zhao L, Xiong X, Garcia D, Zhang Y (2021) Exogenous inoculation of endophytic bacterium Bacillus cereus suppresses clubroot (Plasmodiophora brassicae) occurrence in pak choi (Brassica campestris sp. chinensis L.). Planta 253:1–15. https://doi.org/10.1007/s00425-020-03546-4
Arif S, Munis MFH, Liaquat F, Gulzar S, Haroon U, Zhao L, Zhang Y (2023) Trichoderma viride establishes biodefense against clubroot (Plasmodiophora brassicae) and fosters plant growth via colonizing root hairs in pak choi (Brassica campestris spp. chinesnsis). Biol Control 183:105265. https://doi.org/10.1016/j.biocontrol.2023.105265
Auer S, Ludwig-Müller J (2014) Effects of the endophyte Acremonium alternatum on oilseed rape (Brassica napus) development and clubroot progression. Albanian Journal of Agricultural Sciences:15. https://ajas.inovacion.al/
Balamuralikrishnan M, Doraisamy S, Ganapathy T, Viswanathan R (2005) Effects of biotic and abiotic agents on Sugarcane mosaic virus titre, oxidative enzymes and phenolics in Sorghum bicolor. Acta Phytopathologica Et Entomologica Hungarica 40(1–2):9–22. https://doi.org/10.1556/aphyt.40.2005.1-2.2
Bao A-K, Wang S-M, Wu G-Q, Xi J-J, Zhang J-L, Wang C-M (2009) Overexpression of the Arabidopsis H+-PPase enhanced resistance to salt and drought stress in transgenic alfalfa (Medicago sativa L.). Plant Sci 176(2):232–240. https://doi.org/10.1016/j.plantsci.2008.10.009
Bhardwaj S, Gupta M, Gupta SK (2023) Probing efficacy of biological control agents, plant extracts and resistance inducing chemicals against damping-off of tomato. Ind Phytopathol. https://doi.org/10.1007/s42360-023-00644-7
Bokulich NA, Kaehler BD, Rideout JR, Dillon M, Bolyen E, Knight R, Huttley GA, Gregory Caporaso J (2018) Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin. Microbiome 6(1):1–17. https://doi.org/10.7287/peerj.preprints.3208v2
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37(8):852–857. https://doi.org/10.1038/s41587-019-0209-9
Bulgarelli D, Rott M, Schlaeppi K, Loren V, van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488(7409):91–95. https://doi.org/10.1038/nature11336
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17(3):392–403. https://doi.org/10.1016/j.chom.2015.01.011
Bulgari D, Bozkurt AI, Casati P, Caglayan K, Quaglino F, Bianco PA (2012) Endophytic bacterial community living in roots of healthy and ‘Candidatus Phytoplasma mali’-infected apple (Malus domestica, Borkh.) trees. Antonie Van Leeuwenhoek 102:677–687. https://doi.org/10.1007/s10482-012-9766-3
Bulgari D, Casati P, Quaglino F, Bianco PA (2014) Endophytic bacterial community of grapevine leaves influenced by sampling date and phytoplasma infection process. BMC Microbiol 14(1):1–11. https://doi.org/10.1186/1471-2180-14-198
Chai A, Xie X, Shi Y, Li B (2014) Research status of clubroot (Plasmodiophora brassicae) on cruciferous crops in China. Can J Plant Path 36(sup1):142–153. https://doi.org/10.1080/07060661.2013.868829
Cheah L, Veerakone S, Kent G (2000) Biological control of clubroot on cauliflower with Trichoderma and Streptomyces spp. NZPP 53:18–21. https://doi.org/10.30843/nzpp.2000.53.3642
Chen LH, Huang XQ, Zhang FG, Zhao DK, Yang XM, Shen QR (2012) Application of Trichoderma harzianum SQR-T037 bio-organic fertiliser significantly controls Fusarium wilt and affects the microbial communities of continuously cropped soil of cucumber. J Sci Food Agric 92(12):2465–2470. https://doi.org/10.1002/jsfa.5653
Choudhury H, Pandey M, Hua CK, Mun CS, Jing JK, Kong L, Ern LY, Ashraf NA, Kit SW, Yee TS (2018) An update on natural compounds in the remedy of diabetes mellitus: a systematic review. J Tradit Complement Med 8(3):361–376. https://doi.org/10.1016/j.jtcme.2017.08.012
Diederichsen E, Beckmann J, Schondelmeier J, Dreyer F (2006) Genetics of clubroot resistance in Brassica napus “Mendel.” Acta Hortic 706:307–311. https://doi.org/10.17660/ActaHortic.2006.706.35
Diederichsen E, Frauen M, Ludwig-Müller J (2014) Clubroot disease management challenges from a German perspective. Can J Plant Path 36(sup1):85–98. https://doi.org/10.1080/07060661.2013.861871
Dixon GR (2017) Managing clubroot disease (caused by Plasmodiophora brassicae Wor.) by exploiting the interactions between calcium cyanamide fertilizer and soil microorganisms. J Agric Sci 155(4):527–543. https://doi.org/10.1017/S0021859616000800
Dombrowski N, Schlaeppi K, Agler MT, Hacquard S, Kemen E, Garrido-Oter R, Wunder J, Coupland G, Schulze-Lefert P (2017) Root microbiota dynamics of perennial Arabis alpina are dependent on soil residence time but independent of flowering time. ISME J 11(1):43–55. https://doi.org/10.1038/ismej.2016.109
Donald C, Porter I (2009) Integrated control of clubroot. J Plant Growth Regul 28(3):289–303. https://doi.org/10.1007/s00344-009-9094-7
Donald E, Porter I, Lancaster R (2001) Band incorporation of fluazinam (Shirlan) into soil to control clubroot of vegetable brassica crops. Aust J Exp Agric 41(8):1223–1226. https://doi.org/10.1071/EA00135
Douglas GM, Maffei VJ, Zaneveld J, Yurgel SN, Brown JR, Taylor CM, Huttenhower C, Langille MG (2019) PICRUSt2: an improved and extensible approach for metagenome inference. BioRxiv. https://doi.org/10.1101/672295
El-Shatoury SA, El-Kraly OA, Trujillo ME, El-Kazzaz WM, El-Din E-SG, Dewedar A (2013) Generic and functional diversity in endophytic actinomycetes from wild compositae plant species at South Sinai-Egypt. Res Microbiol 164(7):761–769. https://doi.org/10.1016/j.resmic.2013.03.004
Gulzar S, Manzoor MA, Liaquat F, Shah IH, Rehman A, Hameed MK, Arif S, Zhou X, Zhang Y (2023a) Effects of melatonin and Trichoderma harzianum on pak choi yield, chlorophyll contents and antioxidant defense system under clubroot disease. S Afr J Bot 158:292–300. https://doi.org/10.1016/j.sajb.2023.05.021
Gulzar S, Manzoor MA, Liaquat F, Zahid MS, Arif S, Zhou X, Zhang Y (2023b) Endophytic bacterial diversity by 16S rRNA gene sequencing of Pak choi roots under fluazinam, Trichoderma harzianum, and Sophora flavescens inoculation. Funct Integr Genom 23(2):194. https://doi.org/10.1007/s10142-023-01119-8
Haber CL, Allen LN, Zhao S, Hanson RS (1983) Methylotrophic bacteria: biochemical diversity and genetics. Science 221(4616):1147–1153. https://doi.org/10.1126/science.221.4616.1147
Hahm S-S, Kim J-T, Han K-S, Kim B-R, Kim H-K, Nam Y-K, Yu S-H (2012) Biocontrol efficacy of endophytic bacteria Flavobacterium hercynim EPB-C313 for control of Chinese cabbage clubroot. Res Plant Dis 18(3):210–216. https://doi.org/10.5423/RPD.2012.18.3.210
Hao Z, Wang L, He Y, Liang J, Tao R (2011) Expression of defense genes and activities of antioxidant enzymes in rice resistance to rice stripe virus and small brown planthopper. Plant Physiol Biochem 49(7):744–751. https://doi.org/10.1016/j.plaphy.2011.01.014
Haque MA, Yun HD, Cho KM (2016) Diversity of indigenous endophytic bacteria associated with the roots of Chinese cabbage (Brassica campestris L.) cultivars and their antagonism towards pathogens. J Microbiol 54:353–363. https://doi.org/10.1007/s12275-016-5641-7
He X, Fang J, Huang L, Wang J, Huang X (2015) Sophora flavescens Ait.: traditional usage, phytochemistry and pharmacology of an important traditional Chinese medicine. J Ethnopharmacol 172:10–29. https://doi.org/10.1016/j.jep.2015.06.010
Huang H, Ullah F, Zhou D-X, 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
Huang X, Yang XX, Zhang ZM, Zhou X, Xiang YJ, Zhang L, Liu Y (2022) First Report of Plasmodiophora brassicae causing clubroot on Thlaspi arvense L. Sichuan Province of China. Plant Dis 106(12):3209. https://doi.org/10.1094/PDIS-12-21-2763-PDN
Iwaniuk P, Borusiewicz A, Lozowicka B (2022) Fluazinam and its mixtures induce diversified changes of crucial biochemical and antioxidant profile in leafy vegetable. Sci Hortic 298:110988. https://doi.org/10.1016/j.scienta.2022.110988
Jaschke D, Dugassa-Gobena D, Karlovsky P, Vidal S, Ludwig-Müller J (2010) Suppression of clubroot (Plasmodiophora brassicae) development in Arabidopsis thaliana by the endophytic fungus Acremonium alternatum. Plant Pathol 59(1):100–111. https://doi.org/10.1111/j.1365-3059.2009.02199.x
Javed MA, Schwelm A, Zamani-Noor N, Salih R, Silvestre Vañó M, Wu J, González García M, Heick TM, Luo C, Prakash P (2022) The clubroot pathogen Plasmodiophora brassicae: a profile update. Mol Plant Pathol. https://doi.org/10.1111/mpp.13283
Katoh K, Misawa K, Ki K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059–3066. https://doi.org/10.1093/nar/gkf436
Khalid M, Hui N, Hayat K, Huang D (2020) Suppression of clubroot (Plasmodiophora brassicae) development in Brassica campestris sp. chinensis L. via exogenous inoculation of Piriformospora indica. J Radiat Res Appl Sci 13(1):180–190. https://doi.org/10.1080/16878507.2020.1719337
Khalil MI, Youssef SA, Tartoura KA, Eldesoky AA (2021) Comparative evaluation of physiological and biochemical alteration in tomato plants infected by Alternaria alternata in response to Trichoderma viride and Chaetomium globosum application. Physiol Mol Plant Pathol 115:101671. https://doi.org/10.1016/j.pmpp.2021.101671
Klewer A, Luerßen H, Graf H, Siemens J (2001) Restriction fragment length polymorphism markers to characterize Plasmodiophora brassicae single-spore isolates with different virulence patterns. J Phytopathol 149(3–4):121–127.
Koh H (2018) An adaptive microbiome α-diversity-based association analysis method. Sci Rep 8(1):1–12. https://doi.org/10.1038/s41598-018-36355-7
Koleva II, Van Beek TA, Linssen JP, Groot Ad, Evstatieva LN (2002) Screening of plant extracts for antioxidant activity: a comparative study on three testing methods. Phytochem Anal 13(1):8–17. https://doi.org/10.1002/pca.611
Kuźniak E, Skłodowska M (2004) The effect of Botrytis cinerea infection on the antioxidant profile of mitochondria from tomato leaves. J Exp Bot 55(397):605–612. https://doi.org/10.1093/jxb/erh076
Kużniak E, Skłodowska M (2005) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222(1):192–200. https://doi.org/10.1007/s00425-005-1514-8
Lacava P, Araújo WL, Marcon J, Maccheroni W Jr, Azevedo JLd (2004) Interaction between endophytic bacteria from citrus plants and the phytopathogenic bacteria Xylella fastidiosa, causal agent of citrus-variegated chlorosis. Lett Appl Microbiol 39(1):55–59. https://doi.org/10.1111/j.1472-765X.2004.01543.x
Ling N, Song Y, Raza W, Huang Q, Guo S, Shen Q (2015) The response of root-associated bacterial community to the grafting of watermelon. Plant and Soil 391(1–2):253–264. https://doi.org/10.1007/s11104-015-2399-3
Liu C, Yang Z, He P, Munir S, Wu Y, Ho H, He Y (2018) Deciphering the bacterial and fungal communities in clubroot-affected cabbage rhizosphere treated with Bacillus subtilis XF-1. Agr Ecosyst Environ 256:12–22. https://doi.org/10.1016/j.agee.2018.01.001
Liu C, Yang Z, He P, Munir S, He P, Wu Y, Ho H, He Y (2019) Fluazinam positively affected the microbial communities in clubroot cabbage rhizosphere. Sci Hortic 256:108519. https://doi.org/10.1016/j.scienta.2019.05.046
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Rio TGD, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237
Luo Y, Dong D, Gou Z, Wang X, Jiang H, Yan Y, Wu C, Zhou C (2018) Isolation and characterization of Zhihengliuella aestuarii B18 suppressing clubroot on Brassica juncea var. tumida Tsen. Eur J Plant Pathol 150(1):213–222. https://doi.org/10.1007/s10658-017-1269-7
Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60:157–166. https://doi.org/10.1007/s00248-010-9658-x
McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610–618. https://doi.org/10.1038/ismej.2011.139
Méndez-Bravo A, Herrera-Cornelio LC, García-Toscano DF, Kiel-Martínez AL, Guevara-Avendaño E, Ramírez-Vázquez M, Pérez-Bautista Y, Méndez-Bravo A, Reverchon F (2023) Beneficial effects of selected rhizospheric and endophytic bacteria, inoculated individually or in combination, on non-native host plant development. Rhizosphere 26:100693. https://doi.org/10.1016/j.rhisph.2023.100693
Mohsenzadeh M (2007) Evaluation of antibacterial activity of selected Iranian essential oils against Staphylococcus aureus and Escherichia coli in nutrient broth medium. Pak J Biol Sci 10(20):3693–3697. https://doi.org/10.3923/pjbs.2007.3693.3697
Murthy PS, Borse BB, Khanum H, Srinivas P (2009) Inhibitory effects of Ajowan (Trachyspermum ammi) ethanolic extract on A. ochraceus growth and ochratoxin production. Turk J Biol 33(3):211–217. https://doi.org/10.3906/biy-0805-13
Narisawa K, Ohki K, Hashiba T (2000) Suppression of clubroot and Verticillium yellows in Chinese cabbage in the field by the root endophytic fungus Heteroconium Chaetospira. Plant Pathol 49(1):141–146. https://doi.org/10.1046/j.1365-3059.2000.00425.x
Naseem H, Ahsan M, Shahid MA, Khan N (2018) Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance. J Basic Microbiol 58(12):1009–1022. https://doi.org/10.1002/jobm.201800309
Peng G, Lahlali R, Hwang S-F, Pageau D, Hynes RK, McDonald MR, Gossen BD, Strelkov SE (2014) Crop rotation, cultivar resistance, and fungicides/biofungicides for managing clubroot (Plasmodiophora brassicae) on canola. Can J Plant Path 36(sup1):99–112. https://doi.org/10.1080/07060661.2013.860398
Pham VT, Rediers H, Ghequire MG, Nguyen HH, De Mot R, Vanderleyden J, Spaepen S (2017) The plant growth-promoting effect of the nitrogen-fixing endophyte Pseudomonas stutzeri A15. Arch Microbiol 199:513–517. https://doi.org/10.1007/s00203-016-1332-3
Preston GM (2004) Plant perceptions of plant growth-promoting Pseudomonas. Philos Trans R Soc Lond B Biol Sci 359(1446):907–918. https://doi.org/10.1098/rstb.2003.1384
Rakholiya K, Chanda S (2012) In vitro interaction of certain antimicrobial agents in combination with plant extracts against some pathogenic bacterial strains. Asian Pac J Trop Biomed 2(3):S1466–S1470. https://doi.org/10.1016/S2221-1691(12)60439-0
Saraiva ALdR, Bhering AdS, do Carmo MG, Andreote FD, Dias AC, Coelho IdS, (2020) Bacterial composition in brassica-cultivated soils with low and high severity of clubroot. J Phytopathol 168(11–12):613–619. https://doi.org/10.1111/jph.12941
Schepers H, Kessel G, Lucca F, Förch M, Van Den Bosch G, Topper C, Evenhuis A (2018) Reduced efficacy of fluazinam against Phytophthora infestans in the Netherlands. Eur J Plant Pathol 151:947–960. https://doi.org/10.1007/s10658-018-1430-y
Schwelm A, Fogelqvist J, Knaust A, Jülke S, Lilja T, Bonilla-Rosso G, Karlsson M, Shevchenko A, Dhandapani V, Choi SR (2015) The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci Rep 5(1):11153. https://doi.org/10.1038/srep11153
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60–R60. https://doi.org/10.1186/gb-2011-12-6-r60
Siemens J, Graf H, Bulman S, In O, Ludwig-Müller J (2009) Monitoring expression of selected Plasmodiophora brassicae genes during clubroot development in Arabidopsis thaliana. Plant Pathol 58(1):130–136. https://doi.org/10.1111/j.1365-3059.2008.01943.x
Smith D, Garrison M, Hollowell J, Isleib T, Shew B (2008) Evaluation of application timing and efficacy of the fungicides fluazinam and boscalid for control of Sclerotinia blight of peanut. Crop Prot 27(3–5):823–833. https://doi.org/10.1016/j.cropro.2007.11.010
Somerfield PJ, Clarke KR, Gorley RN (2021) Analysis of similarities (ANOSIM) for 2-way layouts using a generalised ANOSIM statistic, with comparative notes on permutational multivariate analysis of variance (PERMANOVA). Austral Ecol 46(6):911–926. https://doi.org/10.1111/aec.13059
Song L-Y, Ma Y-T, Fang W-J, He Y, Wu J-L, Zuo S-R, Deng Z-Z, Wang S-F, Liu S-K (2019) Inhibitory effects of oxymatrine on hepatic stellate cells activation through TGF-β/miR-195/Smad signaling pathway. BMC Complement Altern Med 19(1):1–9. https://doi.org/10.1186/s12906-019-2560-2
Tian B-Y, Cao Y, Zhang K-Q (2015) Metagenomic insights into communities, functions of endophytes and their associates with infection by root-knot nematode, Meloidogyne incognita, in tomato roots. Sci Rep 5(1):17087. https://doi.org/10.1038/srep17087
Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant Chinese Cabbage. Mycologia 99(2):175–184. https://doi.org/10.1080/15572536.2007.11832577
Vukelić ID, Prokić LT, Racić GM, Pešić MB, Bojović MM, Sierka EM, Kalaji HM, Panković DM (2021) Effects of Trichoderma harzianum on photosynthetic characteristics and fruit quality of tomato plants. Int J Mol Sci 22(13):6961. https://doi.org/10.3390/ijms22136961
Wang X, Song M, Wang Y, Gao C, Zhang Q, Chu X, Fang H, Yu Y (2012) Response of soil bacterial community to repeated applications of carbendazim. Ecotoxicol Environ Saf 75:33–39. https://doi.org/10.1016/j.ecoenv.2011.08.014
Wellburn A, Lichtenthaler H (1984) Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Advances in photosynthesis research. Springer, Berlin, pp 9–12
Woo SL, Hermosa R, Lorito M, Monte E (2023) Trichoderma: a multipurpose, plant-beneficial microorganism for eco-sustainable agriculture. Nat Rev Microbiol 21(5):312–326. https://doi.org/10.1038/s41579-022-00819-5
Xiong X, Yao M, Fu L, Ma Z-q, Zhang X (2016) The botanical pesticide derived from Sophora flavescens for controlling insect pests can also improve growth and development of tomato plants. Ind Crops Prod 92:13–18. https://doi.org/10.1016/j.indcrop.2016.07.043
Zhang M, Smith JAC, Harberd NP, Jiang C (2016) The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol 91(6):651–659. https://doi.org/10.1007/s11103-016-0488-1
Zhang J, Liu Y-X, Zhang N, Hu B, Jin T, Xu H, Qin Y, Yan P, Zhang X, Guo X (2019) NRT1. 1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol 37(6):676–684. https://doi.org/10.1038/s41587-019-0104-4
Zhang Y, Li W, Lu P, Xu T, Pan K (2022) Three preceding crops increased the yield of and inhibited clubroot disease in continuously monocropped Chinese cabbage by regulating the soil properties and rhizosphere microbial community. Microorganisms 10(4):799. https://doi.org/10.3390/microorganisms10040799
Zhang C, Du C, Li Y, Wang H, Zhang C, Chen P (2023) Advances in biological control and resistance genes of brassicaceae clubroot disease-the study case of China. Int J Mol Sci 24(1):785. https://doi.org/10.3390/ijms24010785
Zhao K, Penttinen P, Guan T, Xiao J, Chen Q, Xu J, Lindstrom K, Zhang L, Zhang X, Strobel GA (2011) The diversity and anti-microbial activity of endophytic actinomycetes isolated from medicinal plants in Panxi plateau, China. Curr Microbiol 62:182–190. https://doi.org/10.1007/s00284-010-9685-3
Zhao Y, Gao Z, Tian B, Bi K, Chen T, Liu H, Xie J, Cheng J, Fu Y, Jiang D (2017) Endosphere microbiome comparison between symptomatic and asymptomatic roots of Brassica napus infected with Plasmodiophora brassicae. PLoS One 12(10):e0185907. https://doi.org/10.1371/journal.pone.0185907
Zhou L, Zhang L, He Y, Liu F, Li M, Wang Z, Ji G (2014) Isolation and characterization of bacterial isolates for biological control of clubroot on Chinese cabbage. Eur J Plant Pathol 140(1):159–168. https://doi.org/10.1007/s10658-014-0451-4
Zhou X, Jia H, Ge X, Wu F (2018) Effects of vanillin on the community structures and abundances of Fusarium and Trichoderma spp. in cucumber seedling rhizosphere. J Plant Interact 13(1):45–50. https://doi.org/10.1080/17429145.2017.1414322
Acknowledgements
Thankyou Prof. Chen Jie for generously providing the materials.
Funding
Shanghai Agriculture Applied Technology Development Program under grant number 20180203 supported the present study.
Author information
Authors and Affiliations
Contributions
YZ designed the experiments and managed the research work. SG performed the experimental work, conducted data analysis, and wrote the manuscript. FL and MKH provided supervision for the manuscript write-up and assisted with the submission process. MSZ and AR helped in data analysis. MAM and IHS collected samples and helped in experimental part of research. After proofreading, the manuscript was approved by all authors.
Corresponding author
Ethics declarations
Conflict of interest
No conflict of interest has been declared by all the authors mentioned in the manuscript.
Additional information
Handling Euthor: Boon Chin Tan.
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
Gulzar, S., Liaquat, F., Hameed, M.K. et al. Clubroot (Plasmodiophora brassicae) Suppression Under Biocontrol Agents in Pak choi with Variations in Physiological, Biochemical, and Bacterial Diversity. J Plant Growth Regul 43, 1331–1349 (2024). https://doi.org/10.1007/s00344-023-11186-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-023-11186-7