Skip to main content

Advertisement

SpringerLink
Log in

Control of Panama Disease of Banana by Rotating and Intercropping with Chinese Chive (Allium Tuberosum Rottler): Role of Plant Volatiles

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Intercropping and rotating banana (Musa spp.) with Chinese chive (Allium tuberosum Rottler) has been used as an effective method to control Panama disease (Fusarium wilt) of banana in South China. However, the underlying mechanism is unknown. In this study, we used aqueous leachates and volatiles from Chinese chive to evaluate their antimicrobial activity on Fusarium oxysporum f. sp. cubense race 4 (FOC), the causal agent of Panama disease in banana, and identified the antifungal compounds. Both leaf and root leachates of Chinese chive displayed strong inhibition against FOC, but the concentrated leachates showed lower inhibition than the original leachates. In a sealed system volatiles emitted from the leaves and roots of Chinese chive inhibited mycelial growth of FOC. Volatile compounds emitted from the intact growing roots mimicking natural environment inhibited spore germination of FOC. We identified five volatiles including 2-methyl-2-pentenal and four organosulfur compounds (dimethyl trisulfide, dimethyl disulfide, dipropyl disulfide, and dipropyl trisulfide) from the leaves and roots of Chinese chive. All these compounds exhibited inhibitory effects on FOC, but 2-methyl-2-pentenal and dimethyl trisulfide showed stronger inhibition than the other three compounds. 2-Methyl-2-pentenal at 50–100 μl/l completely inhibited the mycelial growth of FOC. Our results demonstrate that antifungal volatiles released from Chinese chive help control Panama disease in banana. We conclude that intercropping and rotating banana with Chinese chive can control Panama disease and increase cropland biodiversity.

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

Similar content being viewed by others

References

  • Akila, R., Rajendran, L., Harish, S., Saveetha, K., Raguchander, T., and Samiyappan, R. 2011. Combined application of botanical formulations and biocontrol agents for the management of Fusarium oxysporum f. sp. cubense (Foc) causing Fusarium wilt in banana. Biol. Control. 57:175–183.

    Article  Google Scholar 

  • Aochi, Y. O. and Farmer, W. J. 2005. Impact of soil microstructure on the molecular transport dynamics of 1, 2-dichlorethane. Geoderma 127:137–153.

    Article  CAS  Google Scholar 

  • Auger, J., Arnault, I., Diwo-Allain, S., Ravier, M., Molia, F., and Pettiti, M. 2004. Insecticidal and fungicidal potential of Allium substances as biofumigants. Agroindustria 3:5–8.

    Google Scholar 

  • Baumann, D. T., Bastiaans, L., Goudriaan, J., van Laar, H. H., and Kropff, M. J. 2002. Analysing crop yield and plant quality in an intercropping system using an eco-physiological model for interplant competition. Agric. Syst. 73:173–203.

    Article  Google Scholar 

  • Block, E. 1992. The organosulfur chemistry of the genus Allium—implications for the organic chemistry of sulfur. Angew. Chem. Int. Ed. Engl. 31:1135–1178.

    Article  Google Scholar 

  • Cai, X. J., Uden, P. C., Block, E., Zhang, X., Quimby, B. D., and Sullivan, J. J. 1994. Allium chemistry: identification of natural abundance organoselenium volatiles from garlic, elephant garlic, onion, and Chinese chive using headspace gas chromatography with atomic emission detection. J. Agric. Food Chem. 42:2081–2084.

    Article  CAS  Google Scholar 

  • Cai, H., You, M., and Lin, C. 2010. Effects of intercropping systems on community composition and diversity of predatory arthropods in vegetable fields. Acta Ecol. Sin. 30:190–195.

    Article  Google Scholar 

  • Griffiths, G., Trueman, L., Crowther, T., Thomas, B., and Smith, B. 2002. Onions—a global benefit to health. Phytother. Res. 16:603–615.

    Article  PubMed  CAS  Google Scholar 

  • Grimm, D. 2008. Plant genomics. A bunch of trouble. Science 322:1046–1047.

    Article  PubMed  CAS  Google Scholar 

  • Herbert, J. A. and Marx, D. 1990. Short-term control of Panama disease in South Africa. Phytophylactica. 22:339–340.

  • Huang, Y. H., Wei, Y. R., Li, C. Y., Zuo, C. W., and Yi, G. J. 2011. Suppressive effect of Chinese leek on Fusarium oxysporum f. sp. cubense Race 4 and Fusarium wilt disease. J. Fruit Sci. 28:857–862.

    Google Scholar 

  • Huang, Y. H., Wang, R. C., Li, C. H., Zuo, C. W., Wei, Y. R., Zhang, L., and Yi, G. J. 2012. Control of Fusarium wilt in banana with Chinese leek. Eur. J. Plant Pathol. 134:87–95.

    Article  PubMed  Google Scholar 

  • Hwang, S. C. and Ko, W. H. 2004. Cavendish banana cultivars resistant to Fusarium wilt acquired through somaclonal variation in Taiwan. Plant Dis. 88:580–588.

    Article  Google Scholar 

  • Iwalokun, B. A., Ogunledun, A., Ogbolu, D. O., Bamiro, S. B., and Jimi-Omojola, J. 2004. In vitro antimicrobial properties of aqueous garlic extract against multidrug-resistant bacteria and Candida species from Nigeria. J. Med. Food 7(3):327–333.

    PubMed  CAS  Google Scholar 

  • Kim, J. W., Kim, Y. S., and Kyung, K. H. 2004. Inhibitory activity of essential oils of garlic and onion against bacteria and yeasts. J. Food Prot. 67:499–504.

    PubMed  CAS  Google Scholar 

  • Li, M. H., Yang, B., Leng, Y., Chao, C. P., Liu, J. M., He, Z. F., Jiang, Z. D., and Zhong, S. 2011. Molecular characterization of Fusarium oxysporum f. sp. cubense race 1 and 4 isolates from Taiwan and Southern China. Can. J. Plant Pathol. 33(2):168–178.

    Article  CAS  Google Scholar 

  • Lian, J., Wang, Z. F., Cao, L. X., Tan, H. M., Inderbitzin, P., Jiang, Z. D., and Zhou, S. N. 2009. Artificial inoculation of banana tissue culture plantlets with indigenous endophytes originally derived from native banana plants. Biol. Control. 51:427–434.

    Article  Google Scholar 

  • Mau, J. L., Chen, C. P., and Hsieh, P. C. 2001. Antimicrobial effect of extracts from Chinese chive, cinnamon, and corni fructus. J. Agric. Food Chem. 49:183–188.

    Article  PubMed  CAS  Google Scholar 

  • Mazelis, M. 1993. Catabolism of sulfur containing amino acids, pp. 95–108, in L. J. De Kok, I. Stulen, H. Rennenberg, C. Brunold, and W. Rauser (eds.), Sulfur nutrition and assimilation in higher plants. SPB Academic Press, The Hague.

    Google Scholar 

  • Mithofer, A., Wanner, G., and Boland, W. 2005. Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol. 137:1160–1168.

    Article  PubMed  Google Scholar 

  • Müller-Schärer, H. 1996. Interplanting ryegrass in winter leek: Effect on weed control, crop yield and allocation of N-fertiliser. Crop. Prot. 15:641–648.

    Article  Google Scholar 

  • Legutowska, H., Kucharczyk, H., and Surowiec, J. 2000. Control of thrips infestation on leek by intercropping with clover, carrot or bean. Acta Hortic. 571–574.

  • Thangavelu, R., and Mustaffa, M. M. 2012. Current advances in the Fusarium wilt disease management in banana with emphasis on biological control. in C. J. Cumagun (ed.), Plant Pathology. InTech, pp 273–298. ISBN: 978-953-51-0489-6. Available from: http://www.intechopen.com/books/plant-pathology/current-advancesinthe-fusarium-wilt-disease-management-in-banana-with-emphasis-on-biological-contr.

  • Nel, B., Steinberg, C., Labuschagne, N., and Viljoen, A. 2007. Evaluation of fungicides and sterilants for potential application in the management of Fusarium wilt of banana. Crop. Prot. 26:697–705.

    Article  CAS  Google Scholar 

  • Paul, J. Y., Becker, D. K., Dickman, M. B., Harding, R. M., Khanna, H. K., and Dale, J. L. 2011. Apoptosis-related genes confer resistance to Fusarium wilt in transgenic ‘Lady Finger’ bananas. Plant Biotechnol. J. 9:1141–1148.

    Article  PubMed  CAS  Google Scholar 

  • Pino, J. A., Fuentes, V., and Correa, M. T. 2001. Volatile constituents of Chinese chive (Allium tuberosum Rottl. ex Sprengel) and rakkyo (Allium chinense G. Don). J. Agric. Food Chem. 49:1328–1330.

    Article  PubMed  CAS  Google Scholar 

  • Ploetz, R. C. 2006. Fusarium wilt of banana is caused by several pathogens referred to as Fusarium oxysporum f. sp. cubense. Phytopathology 96:653–656.

    Article  PubMed  Google Scholar 

  • Ploetz, R. C. and Pegg, K. G. 2000. Fungal diseases of the root, corm and pseudostem. Fusarium wilt, pp. 143–159, pp. 143–159, in D. R. Jones (ed.), Diseases of Banana, Abacá and Enset. CABI Publishing, Wallingford.

    Google Scholar 

  • Potts, M. J. and Gunadi, N. 1991. The influence of intercropping with Allium on some insect populations in potato (Solatium tuberosum). Ann. Appl. Biol. 119:207–213.

    Article  Google Scholar 

  • Rattanachaikunsopon, P. and Phumkhachorn, P. 2009. Potential of Chinese chive oil as a natural antimicrobial for controlling Flavobacterium columnare infection in Nile tilapia Oreochromis niloticus. Fish. Sci. 75:1431–1437.

    Article  CAS  Google Scholar 

  • Rivlin, R. S. 2001. Historical perspective on the use of garlic. J. Nutr. 131:951–954.

    Google Scholar 

  • Rose, P., Whiteman, M., Moore, P. K., and Zhu, Y. Z. 2005. Bioactive S-alk (en) yl cysteine sulfoxide metabolites in the genus Allium: The chemistry of potential therapeutic agents. Nat. Prod. Rep. 22:351–368.

    Article  PubMed  CAS  Google Scholar 

  • Saravanan, T., Muthusamy, M., and Marimuthu, T. 2003. Development of integrated approach to manage the fusarial wilt of banana. Crop. Prot. 22:1117–1123.

    Article  Google Scholar 

  • Schliemann, W., Kolbe, B., Schmidt, J., Nimtz, M., and Wray, V. 2008. Accumulation of apocarotenoids in mycorrhizal roots of leek (Allium porrum). Phytochemistry 69:1680–1688.

    Article  PubMed  CAS  Google Scholar 

  • Seo, K. I., Moon, Y. H., Choi, S. U., and Park, K. H. 2001. Antibacterial activity of S-methyl methane thiosulfinate and S-methyl 2-propene-1- thiosulfinate from Chinese chive [Allium tuberosum] toward Escherichia coli O157: H7. Biosci. Biotechnol. Biochem. 65:966–968.

    Article  PubMed  CAS  Google Scholar 

  • Smith, M. K., Hamill, S. D., Langdon, P. W., Giles, J. E., Doogan, V. J., and Pegg, K. G. 2006. Towards the development of a Cavendish banana resistant to race 4 of fusarium wilt: Gamma irradiation of micropropagated Dwarf Parfitt (Musa spp., AAA group, Cavendish subgroup). Aust. J. Exp. Agric. 46:107–113.

    Article  Google Scholar 

  • Tapiero, H., Townsend, D. M., and Tew, K. D. 2004. Organosulfur compounds from alliaceae in the prevention of human pathologies. Biomed. Pharmacother. 58:183–193.

    Article  PubMed  CAS  Google Scholar 

  • Viljoen, A. 2002. The status of Fusarium wilt (Panama disease) of banana in South Africa. S. Afr. J. Sci. 98:341–344.

    Google Scholar 

  • Wenke, K., Kai, M., and Piechulla, B. 2010. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506.

    Article  PubMed  CAS  Google Scholar 

  • Yabuki, Y., Mukaida, Y., Saito, Y., Oshima, K., Takahashi, T., Muroi, E., Hashimoto, K., and Uda, Y. 2010. Characterisation of volatile sulphur-containing compounds generated in crushed leaves of Chinese chive (Allium tuberosum Rottler). Food Chem. 120:343–348.

    Article  CAS  Google Scholar 

  • Yildirim, E. and Guvenc, I. 2005. Intercropping based on cauliflower: more productive, profitable and highly sustainable. Eur. J. Agron. 22:11–18.

    Article  Google Scholar 

  • Yin, M. and Tsao, S. 1999. Inhibitory effect of seven Allium plants upon three Aspergillus species. Int. J. Food Microbiol. 49:49–56.

    Article  PubMed  CAS  Google Scholar 

  • Yip, M. K., Lee, S. W., Su, K. C., Lin, Y. H., Chen, T. Y., and Feng, T. Y. 2011. An easy and efficient protocol in the production of pflp transgenic banana against Fusarium wilt. Plant Biotechnol. Rep. 5:245–254.

    Article  Google Scholar 

  • Yu, J. Q. 1999. Allelopathic suppression of Pseudomonas solanacearum infection of tomato (Lycopersicon esculentum) in a tomato-Chinese chive (Allium tuberosum) intercropping system. J. Chem. Ecol. 25:2409–2417.

    Article  CAS  Google Scholar 

  • Zeng, R. S. 2008. Allelopathy in Chinese ancient and modern agriculture, pp. 39–59, pp. 39–59, in R. S. Zeng, A. U. Mallik, and S. M. Luo (eds.), Allelopathy in Sustainable Agriculture and Forestry. Springer, New York.

    Chapter  Google Scholar 

Download references

Acknowledgments

This research was supported by the National 973 project of China (2011CB100400), National Natural Science Foundation of China (31070388, 31028018, 31100286), Guangdong Province Universities and Colleges Pearl River Scholar Funded Scheme (2010), Guangdong Natural Science Foundation of China (S2011040004336), and Ph.D. Programs Foundation (20104404110004) and Postdoctoral Science Foundation (201104341, 20100480762) of the Ministry of Education of China to R.S.Z. A six-month sabbatical leave awarded to AUM from Lakehead University, enabled him to conduct this research at the host laboratory of South China Agricultural University.

Author information

Authors and Affiliations

  1. State Key Laboratory of Conservation and Utilization of Subtropical Agricultural Bio-resources, South China Agricultural University, Guangzhou, 510642, China

    Hui Zhang, Azim Mallik & Ren Sen Zeng

  2. Department of Biology, Lakehead University, Thunder Bay, Ontario, Canada, P7B 5E1

    Azim Mallik

  3. Key Laboratory of Tropical Agro-environment, Ministry of Agriculture, South China Agricultural University, Guangzhou, 510642, China

    Ren Sen Zeng

Authors
  1. Hui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Azim Mallik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ren Sen Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ren Sen Zeng.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, H., Mallik, A. & Zeng, R.S. Control of Panama Disease of Banana by Rotating and Intercropping with Chinese Chive (Allium Tuberosum Rottler): Role of Plant Volatiles. J Chem Ecol 39, 243–252 (2013). https://doi.org/10.1007/s10886-013-0243-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-013-0243-x

Keywords

Search

Navigation