The effect of some defense inducing volatile compounds against chickpea Ascochyta blight

Document Type : Research paper-Persian

Authors

Assistant professor of Plant Pathology, Department of Plant Protection, College of Agriculture, Razi University, Kermanshah, Iran

Abstract

Background and Objectives
Chickpea (Cicer arietinum L.) is the third most important legume crop in the world. Ascochyta blight caused by Ascochyta rabiei (Pass.) Lab. is one of the most important threats for producing chickpea in most of the growing areas. The pathogen invades all aerial parts of the plant and causes severe yield and quality losses. The present study aims to evaluate the effect of some defense inducing volatile compounds in inhibiting A. rabiei, as well as the effect of these compounds on some chickpea growth traits at the presence of the pathogen.
Materials and Methods
First, six volatile compounds including methyl salicylate, 2,3-butanediol, methyl-jasmonate, acetoin, indole and 3-pentanol were prepared in sterile distilled water (100 μM) containing 0.2% Tween 20, and were used for laboratory and greenhouse studies. The in vitro antifungal activity of volatile compounds was tested on chickpea seed meal dextrose agar (CDA) medium. Then, a five-millimeter agar disk containing the mycelium of the pathogen was placed on the surface of CDA medium in 9 cm diameter Petri dishes. The Petri dishes were inverted and 100 μl of the emulsion of each volatile compound was placed inside the lid. The Petri dishes were sealed and kept at the same inverted position to avoid the dropping of volatile compounds over the culture medium. A greenhouse experiment with nine treatments (including six volatile compounds, chlorothalonil fungicide, healthy and diseased controls) was conducted in a completely randomized design. In addition, the emulsions of volatile compounds were sprayed on the leaf surfaces 12 days after sowing chickpea seeds (variety Bivanij). After 48 hours, the conidial suspension of the pathogen in water (2 x 104 conidia/mL) was sprayed to the surface of chickpea seedlings. Disease severity and plant growth indices including shoot fresh weight, shoot dry weight, root fresh weight and root dry weight were measured two weeks after inoculation. Statistical analyses were performed by SAS software (version 9.3). The means were compared by Duncan's test at a statistical probability level of 5%.
Results
All volatile compounds inhibited the mycelial growth of A. rabiei on CDA with the highest (64.91%) and lowest (4.67%) inhibition obtained by 3-pentanol and methyl jasmonate, respectively. In the greenhouse test, all volatile compounds, except methyl jasmonate, reduced the incidence of blight symptoms compared to the diseased control. The highest disease reduction was obtained by chlorothalonil (86.04%) and methyl salicylate (55.81%). At the presence of the pathogen, all volatile compounds increased root fresh weight, root dry weight and shoot fresh weight, and increased shoot dry weight with the exception of 3-pentanol and methyl jasmonate. Compared to the diseased control, the effect of indole on root fresh and dry weight and shoot dry weight, as well as the effect of methyl salicylate on shoot fresh weight was more than other compounds. Methyl jasmonate had the least improving effect on growth traits compared to other volatile compounds.
Discussion
The volatile compounds used in this study inhibited A. rabiei in both in vitro and greenhouse tests. They also improved chickpea growth parameters at the presence of the pathogen. The use of volatile compounds could be considered as a new and promising strategy for the integrated management of Ascochyta blight.
 

Keywords

References

Ahmad, S., Khan, M.A., Ahmad, I., Iqbal, Z., Ashraf, E., et al. 2021. Efficacy of fungicides, plant extracts and biocontrol agents against Ascochyta blight (Ascochyta rabiei) of chickpea (Cicer arietinum L.) under field conditions. Plant Science Today, 8(2): 255–262.
Ali, G.S., Norman, D. and El-Sayed, A.S. 2015. Soluble and volatile metabolites of plant growth-promoting rhizobacteria (PGPRS): Role and practical applications in inhibiting pathogens and activating induced systemic resistance (ISR) In: Bais, H. and Sherrier, J. (Eds.), Plant Microbe Interactions, pp. 241–284.
Bailly, A., Groenhagen, U., Schulz, S., Geisler, M., Eberl, L., et al. 2014. The inter-kingdom volatile signal indole promotes root development by interfering with auxin signalling. The Plant Journal, 80(5): 758–771.
Baite, M.S., and Dubey, S.C. 2018. Pathogenic variability of Ascochyta rabiei causing blight of chickpea in India. Physiological and Molecular Plant Pathology, 102: 122–127.
Batterman, S.A. 1995. Sampling and analysis of biological volatile organic compounds In: Burge, H.A. (Ed.), Bioaerosols. CRC Press, Boca Raton, pp. 249–268.
Ben Mohamed, L., Cherif, M., Harrabi, M., Galbraith, R.F., and Strange, R.N. 2010. Effects of sowing date on severity of blight caused by Ascochyta rabiei and yield components of five chickpea cultivars grown under two climatic conditions in Tunisia. European Journal of Plant Pathology, 126(3): 293–303.
Benzohra, E.E., Bendahmane, B.S., Labdi, M., and Benkada, M.Y. 2012. Determination of pathotypes and physiological races in Ascochyta rabiei, the agent of ascochyta blight in chickpea (Cicer arietinum L.) in Algeria. African Journal of Agricultural Reseearch, 7(7): 1214–1219.
Benzohra, I.E., Bendahmane, B.S., Labdi, M., and Bnekada, M.Y. 2013. In vitro biocontrol using the antagonist Trichoderma harzianum against the algerian isolates of Ascochyta rabiei ( Pass.) Labr., the agent of Ascochyta blight in chickpea (Cicer arietinum L.). International Journal of Microbiological Research 2(2): 124–128.
Benzohra, I.E., Bendahmane, B.S., Benkada, M.Y., Mégateli, M., and Belaidi, H. 2020. Use of three synthetic fungicides to reduce the incidence of Ascochyta blight (Ascochyta rabiei) in chickpea (Cicer arietinum L.): A susceptible cultivars case. Indian Journal of Agricultural Research, 54: 459–464.
Bhattacharyya, D., Garladinne, M., and Lee, Y. 2015. Volatile indole produced by rhizobacterium Proteus vulgaris JBLS202 stimulates growth of Arabidopsis thaliana through auxin, cytokinin, and brassinosteroid pathways. Journal of Plant Growth Regulation, 34(1): 158–168.
Bhattacharyya, P.N., and Jha, D.K. 2012. Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World Journal of Microbiology and Biotechnology, 28(4): 1327–1350.
Castulo-Rubio, D.Y., Alejandre-Ramírez, N.A., Orozco-Mosqueda, M.d.C., Santoyo, G., Macías-Rodríguez, L.I., et al. 2015. Volatile organic compounds produced by the rhizobacterium Arthrobacter agilis UMCV2 modulate Sorghum bicolor (strategy II plant) morphogenesis and SbFRO1 transcription in vitro. Journal of Plant Growth Regulation, 34(3): 611–623.
Chang, K.F., Ahmed, H.U., Hwang, S.F., Gossen, B.D., Strelkov, S.E., et al. 2007. Sensitivity of field populations of Ascochyta rabiei to chlorothalonil, mancozeb and pyraclostrobin fungicides and effect of strobilurin fungicides on the progress of ascochyta blight of chickpea. Canadian journal of plant science, 87(4): 937–944.
Chen, W., Coyne, C.J., Peever, T.L., and J. Muehlbauer, F. 2004. Characterization of chickpea differentials for pathogenicity assay of ascochyta blight and identification of chickpea accessions resistant to Didymella rabiei. Plant Pathology, 53(6): 759–769.
Choi, H.K., Song, G.C., Yi, H.-S., and Ryu, C.-M. 2014. Field Evaluation of the bacterial volatile derivative 3-pentanol in priming for induced resistance in pepper. Journal of Chemical Ecology, 40(8): 882–892.
Chongo, G., Buchwaldt, L., Gossen, B.D., Lafond, G.P., May, W.E., et al. 2003. Foliar fungicides to manage ascochyta blight Ascochyta rabiei of chickpea in Canada. Canadian Journal of Plant Pathology, 25(2): 135–142.
Chung, J.H., Song, G.C., and Ryu, C.M. 2016. Sweet scents from good bacteria: Case studies on bacterial volatile compounds for plant growth and immunity. Plant Molecular Biology, 90(6): 677–687.
Cortes-Barco, A.M., Goodwin, P.H., and Hsiang, T. 2010. Comparison of induced resistance activated by benzothiadiazole, (2R,3R)-butanediol and an isoparaffin mixture against anthracnose of Nicotiana benthamiana. Plant Pathology, 59(4): 643–653.
Davidson, J.A., and Kimber, R.B.E. 2007. Integrated disease management of ascochyta blight in pulse crops. European Journal of Plant Pathology, 119(1): 99–110.
Dhakshinamoorthy, D., Sundaresan, S., Iyadurai, A., Subramanian, K.S., Janavi, G.J., et al. 2020. Hexanal vapor induced resistance against major postharvest pathogens of banana (Musa acuminata L.). The Plant Pathology Journal, 36(2): 133–147.
El-Hasan, A., Walker, F., Schöne, J., and Buchenauer, H. 2007. Antagonistic effect of 6-pentyl-alpha-pyrone produced by Trichoderma harzianum toward Fusarium moniliforme. Journal of Plant Diseases and Protection, 114(2): 62–68.
Ennouri, A., Lamiri, A., Essahli, M., and Krimi Bencheqroun, S. 2020. Chemical composition of essential oils and their antifungal activity in controlling Ascochyta rabiei. Journal of Agricultural Science and Technology, 22(5): 1371–1381.
Faheem, M., Raza, W., Zhong, W., Nan, Z., Shen, Q., et al. 2015. Evaluation of the biocontrol potential of Streptomyces goshikiensis YCXU against Fusarium oxysporum f. sp. niveum. Biological Control, 81: 101–110.
Farag, M.A., Zhang, H., and Ryu, C.-M. 2013. Dynamic chemical communication between plants and bacteria through airborne signals: Induced resistance by bacterial volatiles. Journal of Chemical Ecology, 39(7): 1007–1018.
Farag, M.A., Ryu, C.-M., Sumner, L.W., and Paré, P.W. 2006. GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry, 67(20): 2262–2268.
Farahani, S., Talebi, R., Maleki, M., Mehrabi, R., and Kanouni, H. 2019. Pathogenic diversity of Ascochyta rabiei isolates and identification of resistance sources in core collection of chickpea germplasm. The Plant Pathology Journal, 35(4): 321–329.
Fincheira, P., and Quiroz, A. 2018. Microbial volatiles as plant growth inducers. Microbiological Research, 208: 63–75.
Gan, Y.T., Siddique, K.H.M., MacLeod, W.J., and Jayakumar, P. 2006. Management options for minimizing the damage by ascochyta blight (Ascochyta rabiei) in chickpea (Cicer arietinum L.). Field Crops Research, 97(2–3): 121–134.
Garbeva, P., Hol, W.H.G., Termorshuizen, A.J., Kowalchuk, G.A., and Boer, W.d. 2011. Fungistasis and general soil biostasis - a new synthesis. Soil Biology & Biochemistry, 43(3): 469–477.
Gu, Y.-Q., Mo, M.-H., Zhou, J.-P., Zou, C.-S., and Zhang, K.-Q. 2007. Evaluation and identification of potential organic nematicidal volatiles from soil bacteria. Soil Biology and Biochemistry, 39(10): 2567–2575.
Han, S.H., Lee, S.J., Moon, J.H., Park, K.H., Yang, K.Y., et al. 2006. GacS-dependent production of 2R, 3R-butanediol by Pseudomonas chlororaphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Molecular Plant Microbe Interactions, 19(8): 924–930.
Huang, C.-H., Vallad, G.E., Zhang, S., Wen, A., Balogh, B., et al. 2012. Effect of application frequency and reduced rates of acibenzolar-s-methyl on the field efficacy of induced resistance against bacterial spot on tomato. Plant Disease, 96(2): 221–227.
Huang, Y., He, Y., Ye, B.C., and Li, C. 2017. Rhizospheric Bacillus subtilis exhibits biocontrol effect against Rhizoctonia solani in pepper (Capsicum annuum). BioMed Research International, 2017: 1–9.
Javaid, A., Munir, R., Khan, I.H., and Shoaib, A. 2020. Control of the chickpea blight, Ascochyta rabiei, with the weed plant, Withania somnifera. Egyptian Journal of Biological Pest Control, 30(1): 1–8.
Kai, M., Effmert, U., Berg, G., and Piechulla, B. 2006. Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Archives of Microbiology, 187(5): 351–360.
Kai, M., Haustein, M., Molina, F., Petri, A., Scholz, B., et al. 2009. Bacterial volatiles and their action potential. Applied Microbiology and Biotechnology, 81(6): 1001–1012.
Kalyanasundaram, G.T., Syed, N., and Subburamu, K. 2021. Recent developments in plant growth-promoting rhizobacteria (PGPR) for sustainable agriculture In: Viswanath, B. (Ed.), Recent Developments in Applied Microbiology and Biochemistry. Elsevier, pp. 181–192.
Kim, Y.C., and Anderson, A.J. 2020. Integration of bacterial volatile organic compounds with plant health In: Ryu, C.-M., Weisskopf, L. and Piechulla, B. (Eds.), Bacterial Volatile Compounds as Mediators of Airborne Interactions, pp. 201–213.
Larsen, T.O., and Frisvad, J.C. 1994. Production of volatiles and presence of mycotoxins in conidia of common indoor penicillia and aspergilli In: Samson, R.A., Flannigan, B., Flannigan, M.E., Verhoeff, A.P., Adan, O.C.G. and Hoekstra, E.S. (Eds.), Health Implications of Fungi in Indoor Environments. Elsevier Science, Amsterdam, pp. 251–279.
Lee, B., Farag, M.A., Park, H.B., Kloepper, J.W., Lee, S.H., et al. 2012. Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PloS One, 7(11): e48744.
Li, X., Wang, X., Shi, X., Wang, B., Li, M., et al. 2020. Antifungal Effect of volatile organic compounds from Bacillus velezensis CT32 against Verticillium dahliae and Fusarium oxysporum. Processes, 8(12): 1–14.
Liu, N., Xu, S., Yao, X., Zhang, G., Mao, W., et al. 2016. Studies on the control of Ascochyta blight in field peas (Pisum sativum L.) caused by Ascochyta pinodes in Zhejiang Province, China. Frontiers in Microbiology, 7: 481.
Manjunatha, L., Saabale, P.R., Srivastava, A.K., Dixit, G.P., Yadav, L.B., et al. 2018. Present status on variability and management of Ascochyta rabiei infecting chickpea. Indian Phytopathology, 71(1): 9–24.
Meldau, D.G., Meldau, S., Hoang, L.H., Underberg, S., Wunsche, H., et al. 2013. Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. The Plant Cell, 25(7): 2731–2747.
Nene, Y., Reddy, M., Haware, M., Ghanekar, A., Amin, K., et al. 2012. Field Diagnosis of Chickpea Diseases and their Control. Information Bulletin No. 28. International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, India, pp. 60.
Nene, Y.L. 2008. A review of Ascochyta blight of chickpea. Tropical Pest Management, 28(1): 61–70.
Nizam, S., Singh, K., and Verma, P.K. 2010. Expression of the fluorescent proteins DsRed and EGFP to visualize early events of colonization of the chickpea blight fungus Ascochyta rabiei. Current Genetics, 56(4): 391–399.
Ossowicki, A., Jafra, S., and Garbeva, P. 2017. The antimicrobial volatile power of the rhizospheric isolate Pseudomonas donghuensis P482. PloS One, 12(3): e0174362.
Owati, A.S., Agindotan, B., Pasche, J.S. and Burrows, M. 2017. The Detection and Characterization of QoI-Resistant Didymella rabiei Causing Ascochyta Blight of Chickpea in Montana. Frontiers in Plant Science, 8: 1165.
Parida, S.K., Gayacharan, Rani, U., Singh, S., Basandrai, A.K., et al. 2020. Identification of novel resistant sources for ascochyta blight (Ascochyta rabiei) in chickpea. PloS One, 15(10): e0240589.
Piechulla, B., Lemfack, M.C., and Kai, M. 2017. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant, Cell and Environment, 40(10): 2042–2067.
Pieterse, C.M.J., Leon-Reyes, A., Van der Ent, S., and Van Wees, S.C.M. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology, 5(5): 308–316.
Raza, W., and Shen, Q. 2020. Volatile organic compounds mediated plant-microbe interactions in soil In: Sharma, V. and Al-Ani, L.K.T. (Eds.), Molecular Aspects of Plant Beneficial Microbes in Agriculture, pp. 209–219.
Rudrappa, T., Biedrzycki, M.L., Kunjeti, S.G., Donofrio, N.M., Czymmek, K.J., et al. 2010. The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Communicative and Integrative Biology, 3(2): 130–138.
Ryu, C.M., Farag, M.A., Hu, C.H., Reddy, M.S., Kloepper, J.W., et al. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiology, 134(3): 1017–1026.
Ryu, C.M., Farag, M.A., Hu, C.H., Reddy, M.S., Wei, H.X., et al. 2003. Bacterial volatiles promote growth in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 100(8): 4927–4932.
Safari, E., Sharifi, R., and Abbassi, S. 2020. Inhibition of wheat take-all disease using defenses-inducing compounds. Journal of Applied Research in Plant Protection, 9(3): 1–10 (In Farsi with English summary).
Santoro, M., Cappellari, L., Giordano, W., and Banchio, E. 2015. Production of volatile organic compounds in PGPR In: Cassán, F.D., Okon, Y. and Creus, C.M. (Eds.), Handbook for Azospirillum: Technical Issues and Protocols, pp. 307–317.
Schulz, S., and Dickschat, J.S. 2007. Bacterial volatiles: the smell of small organisms. Natural Product Reports, 24(4): 814–842.
Seydi, L. 2014. Evaluation of some chickpea lines for resistance to Ascochyta rabiei causal agent of blight. M.Sc. Thesis. Razi University, Kermanshah, Iran.
Sharifi, R., and Ryu, C.-M. 2016. Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both? Frontiers in Microbiology, 7: doi:10.3389/fmicb.2016.00196.
Sharifi, R., and Ryu, C.M. 2018. Revisiting bacterial volatile-mediated plant growth promotion: lessons from the past and objectives for the future. Annals of Botany, 122(3): 349–358.
Sharifi, R., Ahmadzadeh, M., Behboudi, K., and Ryu, C. 2013. Role of Bacillus subtilis volatiles in induction of systemic resistance in Arabidopsis. Iranian Journal of Plant Protection Science, 44(1): 91–101 (In Farsi with English summary).
Sharma, M., Pande, S., and Rathore, A. 2010. Effect of growth stages of chickpea on the genetic resistance of Ascochyta blight. European Journal of Plant Pathology, 128(3): 325–331.
Song, G., and Ryu, C.-M. 2013. Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. International Journal of Molecular Sciences, 14(5): 9803–9819.
Tadesse, M., Turoop, L., and Ojiewo, C.O. 2017. Survey of chickpea Cicer arietinum L) Ascochyta blight (Ascochyta rabiei Pass.) disease status in production regions of Ethiopia. Plant, 5(1): 23.
Tahir, H.A., Gu, Q., Wu, H., Niu, Y., Huo, R., et al. 2017a. Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Scientific Reports, 7: 40481.
Tahir, H.A.S., Gu, Q., Wu, H., Raza, W., Hanif, A., et al. 2017b. Plant growth promotion by volatile organic compounds produced by Bacillus subtilis SYST2. Frontiers in Microbiology, 8: 171.
Tyc, O., Song, C., Dickschat, J.S., Vos, M. and Garbeva, P. 2017. The ecological role of volatile and soluble secondary metabolites produced by soil bacteria. Trends in Microbiology, 25(4): 280–292.
Vafaei, S., Rezaee, S., Moghadam, A.A., and Zamanizadeh, H. 2017. Screening of Chickpea germ plasms for selection of resistant genotypes to Ascochyta blight. Applied Entomology and Phytopathology, 85(1): 97–110 (In Farsi with English summary).
Veselova, M.A., Plyuta, V.A., and Khmel, I.A. 2019. Volatile compounds of bacterial origin: Structure, biosynthesis, and biological activity. Microbiology, 88(3): 261–274.
Vespermann, A., Kai, M. and Piechulla, B. 2007. Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Applied and Environmental Microbiology, 73(17): 5639–5641.
Wang, K., Liu, J., Zhan, Y., and Liu, Y. 2019. A new slow-release formulation of methyl salicylate optimizes the alternative control of Sitobion avenae (Fabricius) (Hemiptera: Aphididae) in wheat fields. Pest Management Science, 75(3): 676–682.
Whillans, F.D., and Lamont, G.S. 1995. Fungal volatile metabolites released into indoor air environments: variation with fungal species and growth media., pp. 47–50 In: Morawska, L., Bofinger, N.D. and Maroni, M. (Eds.), Proceedings of the International workshop Indoor Air—An Integrated Approach, Gold Coast Australia.
Yuan, J., Raza, W., Shen, Q., and Huang, Q. 2012. Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. cubense. Applied and Environmental Microbiology, 78(16): 5942–5944.
Yuan, J., Zhao, M., Li, R., Huang, Q., Raza, W., et al. 2017. Microbial volatile compounds alter the soil microbial community. Environmental Science and Pollution Research International, 24(28): 22485–22493.
Zhang, H., Xie, X., Kim, M.S., Kornyeyev, D.A., Holaday, S., et al. 2008. Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant Journal, 56(2): 264–273.
Zhang, H., Sun, Y., Xie, X., Kim, M.S., Dowd, S.E., et al. 2009. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant Journal, 58(4): 568–577.
Zhao, L.-j., Yang, X.-n., Li, X.-y., Mu, W., and Liu, F. 2011. Antifungal, insecticidal and herbicidal properties of volatile components from Paenibacillus polymyxa strain BMP-11. Agricultural Sciences in China, 10(5): 728–736.
Zou, C.-S., Mo, M.-H., Gu, Y.-Q., Zhou, J.-P., and Zhang, K.-Q. 2007. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biology and Biochemistry, 39(9): 2371–2379.
Plant Protection (Scientific Journal of Agriculture)
Volume 44, Issue 3
September 2021
Pages 43-58

Files

Share

How to cite

Statistics