Skip to main content
SpringerLink
Log in

Mechanism of benzoxazinoids affecting the growth and development of Fusarium oxysporum f. sp. fabae

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Continuous cropping of faba bean (Vicia faba L.) has led to a high incidence of wilt disease. The implementation of an intercropping system involving wheat and faba bean can effectively control the propagation of faba bean wilt disease. To investigate the mechanisms of wheat in mitigating faba bean wilt disease in a wheat-faba bean intercropping system. A comprehensive investigation was conducted to assess the temporal variations in Fusarium oxysporum f. sp. fabae (FOF) on the chemotaxis of benzoxazinoids (BXs) and wheat root through indoor culture tests. The effects of BXs on FOF mycelial growth, spore germination, spore production, and electrical conductivity were examined. The influence of BXs on the ultrastructure of FOF was investigated through transmission electron microscopy. Eukaryotic mRNA sequencing was utilized to analyze the differentially expressed genes in FOF upon treatment with BXs. FOF exhibited a significant positive chemotactic effect on BXs in wheat roots and root secretions. BXs possessed the potential to exert significant allelopathic effects on the mycelial growth, spore germination, and sporulation of FOF. In addition, BXs demonstrated a remarkable ability to disrupt the structural integrity and stability of the membrane and cell wall of the FOF mycelia. BXs possessed the capability of posing threats to the integrity and stability of the cell membrane and cell wall. This ultimately resulted in physiological dysfunction, effectively inhibiting the regular growth and developmental processes of the FOF.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Acharya J, Kaspar TC, Robertson AE (2021) Effect of 6-Methoxy-2-Benzoxazolinone (MBOA) on Pythium species and Corn Seedling Growth and Disease. Plant Dis 105(4):0191–2917

    Article  Google Scholar 

  • Ahmad S, Veyrat N, Gordon-Weeks R, Zhang Y, Martin J, Smart L, Ton J (2011) Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol 157(1):317–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allen RN, Newhook FJ (1973) Chemotaxis of zoospores of Phytophthora cinnamomi to ethanol in capillaries of soil pore dimensions. Trans Br Mycological Soc 61(2):287–IN12

    Article  CAS  Google Scholar 

  • Alonso-Monge R, Román E, Arana DM, Pla J, Nombela C (2009) Fungi sensing environmental stress. Clin Microbiol Infect 15:17–19

    Article  CAS  PubMed  Google Scholar 

  • Bibo-Verdugo B, Jiang Z, Caffrey CR, O’Donoghue AJ (2017) Targeting proteasomes in infectious organisms to combat disease. FEBS J 284(10):1503–1517

    Article  CAS  PubMed  Google Scholar 

  • Bo T, Han PP, Su QZ, Fu P, Guo FZ, Zheng ZX et al (2016) Antimicrobial epsilon-poly-l-lysine induced changes in cell membrane compositions and properties of saccharomyces cerevisiae. Food Control(61-).

  • Boudreau MA, Shew BB, Andrako LD (2016) Impact of intercropping on epidemics of groundnut leaf spots: defining constraints and opportunities through a 7-year field study. Plant Pathol 65(4):601–611

    Article  CAS  Google Scholar 

  • Cameron JN, Carlile MJ (1978) Fatty acids, aldehydes and alcohols as attractants for zoospores of Phytophthora palmivora. Nature 271(5644):448–449

    Article  CAS  Google Scholar 

  • Capaldi AP, Kaplan T, Liu Y, Habib N, Regev A, Friedman N, O’Shea EK (2008) Structure and function of a transcriptional network activated by the MAPK Hog1. Nat Genet 40(11):1300–1306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carlile MJ (1983) Motility, taxis, and tropism in Phytophthora. Phytophthora, It’s Biology Taxonomy, Ecology and Pathology, 95–107

  • Catt SC, Braich S, Kaur S, Paull JG (2017) QTL detection for flowering time in faba bean and the responses to ambient temperature and photoperiod. Euphytica 213:1–13

    Article  Google Scholar 

  • Chen S, Zhou Y, Chen Y et al (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor

  • Ding X, Yang M, Huang H, Chuan Y, He X, Li C, Zhu S (2015) Priming maize resistance by its neighbors: activating 1, 4-benzoxazine-3-ones synthesis and defense gene expression to alleviate leaf disease. Front Plant Sci 6:830

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellis SW, Grindle M, Lewis DH (1991) Effect of osmotic stress on yield and polyol content of dicarboximide-sensitive and-resistant strains of Neurospora Crassa. Mycol Res 95(4):457–464

    Article  CAS  Google Scholar 

  • Fu X, Wu X, Zhou X, Liu S, Shen Y, Wu F (2015) Companion cropping with potato onion enhances the disease resistance of tomato against Verticillium Dahliae. Front Plant Sci 6:726

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao X, Wu M, Xu R, Wang X, Pan R, Kim HJ, Liao H (2014) Root interactions in a maize/soybean intercropping system control soybean soil-borne disease, red crown rot. PLoS ONE, 9(5), e95031

  • Guo Y, Lv J, Zhao Q, Dong Y, Dong K (2020) Cinnamic acid increased the incidence of Fusarium wilt by increasing the pathogenicity of Fusarium oxysporum and reducing the physiological and biochemical resistance of faba bean, which was alleviated by intercropping with wheat. Front Plant Sci 11:608389

    Article  PubMed  PubMed Central  Google Scholar 

  • Hailu G (2015) A review on the comparative advantage of intercropping systems. J Biology Agric Healthc 5(7):28–38

    Google Scholar 

  • Ho HH, Hickman CJ (1967) Factors governing zoospore responses of Phytophthora Megasperma var. Sojae to plant roots. Can J Bot 45(11):1983–1994

    Article  Google Scholar 

  • Hohmann S (2009) Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae. FEBS Lett 583(24):4025–4029

    Article  CAS  PubMed  Google Scholar 

  • Homulle Z, George TS, Karley AJ (2021) Root traits with team benefits: understanding belowground interactions in intercropping systems. Plant Soil, 1–26

  • Huang LF, Song LX, Xia XJ, Mao WH, Shi K, Zhou YH, Yu JQ (2013) Plant-soil feedbacks and soil sickness: from mechanisms to application in agriculture. J Chem Ecol 39:232–242

    Article  CAS  PubMed  Google Scholar 

  • Karina Lucas Silva-Brandão, Natália Faraj Murad, Aline Peruchi, et al et al (2021) Transcriptome differential co-expression reveals distinct molecular response of fall-armyworm strains to DIMBOA [J]. Pest Management Science. 77 (1): 518–526

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements[J]. Nat Methods 12(4):357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Köhler JR, Hube B, Puccia R, Casadevall A, Perfect JR (2017) Fungi that infect humans. Microbiol Spectr 5(3):5–3

    Article  Google Scholar 

  • Kumar M, Chand R, Dubey RS, Shah K (2015) Effect of tricyclazole on morphology, virulence and enzymatic alterations in pathogenic fungi bipolaris sorokiniana for management of spot blotch disease in barley. World J Microbiol Biotechnol 31(1):23–35

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YN, Ye QQ, Hou WF, Zhang GQ (2018) Development of antibacterial ε-polylysine/chitosan hybrid films and the effect on citrus. Int J Biol Macromol 118:2051–2056

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Feng J, Zheng L, Huang J, Yang Y, Li X (2020a) Intercropping with marigold promotes soil health and microbial structure to assist in mitigating tobacco bacterial wilt. J Plant Pathol 102:731–742

    Article  Google Scholar 

  • Li Z, Wang T, He C, Cheng K, Zeng R, Song Y (2020b) Control of Panama disease of banana by intercropping with Chinese chive (Allium tuberosum Rottler): cultivar differences. BMC Plant Biol 20:1–13

  • Liu X, Li J, Zhou L, Liu X, Zhang W (2004) Inhibition effect of Dingbu on Fusarium graminearum and corn spot pathogen. J Microbiol 01:109–114

    CAS  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of Fold change and dispersion for RNA-seq data with DESeq2[J]. Genome Biol 15(12):550

    Article  PubMed  PubMed Central  Google Scholar 

  • Lv J, Dong Y, Dong K, Zhao Q, Yang Z, Chen L (2020) Intercropping with wheat suppressed Fusarium wilt in faba bean and modulated the composition of root exudates. Plant Soil 448:153–164

    Article  CAS  Google Scholar 

  • Lyu D, Smith DL (2022) The root signals in rhizospheric inter-organismal communications. Front Plant Sci, 13

  • Mei X, Yang M, Ding X, Chuan Y, &Zhu S (2015) The mechanism of action of Benzothiazole secreted by maize root on Phytophthora capsici (eds.) Proceedings of the 2015 Academic Annual Meeting of the Chinese Society of Plant Pathology (pp.468). China Agricultural Publishing House

  • Moreno AD, González-Fernández C, Tomás-Pejó E (2022) Insights into cell robustness against lignocellulosic inhibitors and insoluble solids in bioethanol production processes. Sci Rep 12(1):1–13

    Article  Google Scholar 

  • Niemeyer HM (2009) Hydroxamic acids derived from 2-hydroxy-2 H-1, 4-benzoxazin-3 (4 H)-one: key defense chemicals of cereals. J Agric Food Chem 57(5):1677–1696

    Article  CAS  PubMed  Google Scholar 

  • Nourbakhsh F, Koocheki A, Mahallati MN (2019) Investigation of biodiversity and some of the ecosystem services in the intercropping of corn, soybean and marshmallow. Int J Plant Prod 13:35–46

    Article  Google Scholar 

  • Pertea M, Pertea GM, Antonescu CM et al (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads[J]. Nat Biotechnol 33(3):290–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rep M, Krantz M, Thevelein JM, Hohmann S (2000) The Transcriptional response of Saccharomyces cerevisiae to osmotic shock: Hot1p AND Msn2p/Msn4p ARE REQUIRED FOR THE INDUCTION OF SUBSETS OF HIGH OSMOLARITY GLYCEROL PATHWAY-DEPENDENT GENES* 210. J Biol Chem 275(12):8290–8300

    Article  CAS  PubMed  Google Scholar 

  • Scavo A, Mauromicale G (2021) Crop allelopathy for sustainable weed management in agroecosystems: knowing the present with a view to the future. Agronomy 11(11):2104

    Article  CAS  Google Scholar 

  • Schulz M, Marocco A, Tabaglio V (2012) BOA detoxification of four summer weeds during germination and seedling growth. J Chem Ecol 38:933–946

    Article  CAS  PubMed  Google Scholar 

  • Schulz M, Marocco A, Tabaglio V, Macias FA, Molinillo JM (2013) Benzoxazinoids in rye allelopathy-from discovery to application in sustainable weed control and organic farming. J Chem Ecol 39:154–174

    Article  CAS  PubMed  Google Scholar 

  • Shen S, Park JW, Lu Z et al (2014) rMATS: robust and flexible detection of differential alternative splicing from replicate RNA-Seq data[J]. Proceedings of the National Academy of Sciences, 111(51): E5593-E5601

  • Statements & Declarations

  • Stoddard FL, Nicholas AH, Rubiales D, Thomas J, Villegas-Fernández AM (2010) Integrated pest management in faba bean. Field Crops Res 115(3):308–318

    Article  Google Scholar 

  • Tian XL, Wang CB, Bao XG, Wang P, Li XF, Yang SC, Li L (2019) Crop diversity facilitates soil aggregation in relation to soil microbial community composition driven by intercropping. Plant Soil 436:173–192

    Article  CAS  Google Scholar 

  • Virtanen AI, Hietala PK (1955) 2 (3)-Benzoxazolinone, an anti-fusarium factor in rye seedlings. Acta Chem Scand 9(9):1543–1544

    Article  CAS  Google Scholar 

  • Wahlross O, Virtanen AI (1959) The precursors of 6-methoxybenzoxazolinone in maize and wheat plants, their isolation and some of their properties (No. REP-9686. CIMMYT.)

  • Wang L, Feng Z, Wang X et al (2009) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data[J]. Bioinformatics 26(1):136–138

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Mei X, Liu Y, Du F, Yang M, Zu Y (2021) Research progress on defense related substances such as benzoxazines in plants. J Plant Physiol 04767–779. https://doi.org/10.13592/j.cnki.ppj.2020.0413

  • Werner D (2000) Organic signals between plants and microorganisms. The rhizosphere. CRC, pp 213–238

  • Wouters FC, Blanchette B, Gershenzon J, Vassão DG (2016) Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem Rev 15:1127–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu DY, Jiang BW, Ye CY, Michael PT, Fan LJ (2022) Horizontal transfer and evolution of the biosynthetic gene cluster for benzoxazinoids in plants [J]. Plant Commun 3(3):100320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S et al (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang M, Zhang Y, Qi L, Mei X, Liao J, Ding X, Zhu S (2014) Plant-plant-microbe mechanisms involved in soil-borne disease suppression on a maize and pepper intercropping system. PLoS ONE, 9(12), e115052

  • Ye T, Ma Z, Zhang X, Wang W, Han X, Wang Z (2011) Study on osmotic pressure sensitivity and conductivity changes of Tebuconazole resistant fusarium graminearum. North China Agricultural J S2:184–189

    Google Scholar 

  • Zhang X, Cao J, Zhai C, Chen J (2002) Cloning and expression of proB, a osmotic pressure Regulator gene of Bacillus subtilis. J Microbiol 02:163–168. https://doi.org/10.13343/j.cnki.wsxb.202.02.005

    Article  Google Scholar 

  • Zhang L, Fang Y, Ji S, Jiao Y, Liao J, Li J, Yang M (2015) Analysis of the inhibitory activity and antimicrobial substances of corn root exudates against tobacco black shank pathogen Chinese. J Biol pest Control 01115–122. https://doi.org/10.16409/j.cnki.2095-039x.2015.01.016

  • Zhang H, Yang Y, Mei X, Li Y, Wu J, Li Y, Liu Y (2020) Phenolic acids released in maize rhizosphere during maize-soybean intercropping inhibit Phytophthora blight of soybean. Front Plant Sci 11:886

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Mundt CC (2000) Genetic diversity and disease control in rice. Nature 406(6797):718–722

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank all the reviewers who participated in the review, as well as MJEditor (www.mjeditor.com) for providing English editing services during the preparation of this manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (32260802).

Author information

Author notes

  1. Zixuan Cen and Bijie Hu contributed equally to this work.

Authors and Affiliations

  1. College of Resources and Environment, Yunnan Agricultural University, Kunming, China

    Zixuan Cen, Bijie Hu, Siyin Yang, Guanglei Ma, Yiran Zheng & Yan Dong

Authors
  1. Zixuan Cen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bijie Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siyin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guanglei Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yiran Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yan Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZC conceived the original screening and research plans, finished writing this thesis. YD supervised the experiments agreed to serve as the author responsible for contact and ensures communication. BH provided technical assistance to ZC. MG and SY designed the experiments. ZC and YZ analyzed the data. All authors contributed to the article and approved the submitted version.

Corresponding author

Correspondence to Yan Dong.

Ethics declarations

Competing interests

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cen, Z., Hu, B., Yang, S. et al. Mechanism of benzoxazinoids affecting the growth and development of Fusarium oxysporum f. sp. fabae. Plant Mol Biol 114, 42 (2024). https://doi.org/10.1007/s11103-024-01439-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11103-024-01439-8

Keywords

Search

Navigation