Research in Plant Disease (식물병연구)

The Korean Society of Plant Pathology (한국식물병리학회)
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Aromatic Agriculture: Volatile Compound-Based Plant Disease Diagnosis and Crop Protection

향기농업: 휘발성 물질을 이용한 식물병 진단과 방제

  • Riu, Myoungjoo (Molecular Phytobacteriology Laboratory, KRIBB) ;
  • Son, Jin-Soo (Molecular Phytobacteriology Laboratory, KRIBB) ;
  • Oh, Sang-Keun (Department of Applied Biology, College of Agriculture and Life Sciences, Chungnam National University) ;
  • Ryu, Choong-Min (Molecular Phytobacteriology Laboratory, KRIBB)
  • 류명주 (한국생명공학연구원 분자식물세균실험실) ;
  • 손진수 (한국생명공학연구원 분자식물세균실험실) ;
  • 오상근 (충남대학교 농업생명과학대학 응용생물학과) ;
  • 류충민 (한국생명공학연구원 분자식물세균실험실)
  • Received : 2022.03.24
  • Accepted : 2022.03.28
  • Published : 2022.03.31
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Abstract

Volatiles exist ubiquitously in nature. Volatile compounds produced by plants and microorganisms confer inter-kingdom and intra-kingdom communications. Autoinducer signaling molecules from contact-based chemical communication, such as bacterial quorum sensing, are relayed through short distances. By contrast, biogenic volatiles derived from plant-microbe interactions generate long-distance (>20 cm) alarm signals for sensing harmful microorganisms. In this review, we discuss prior work on volatile compound-mediated diagnosis of plant diseases, and the use of volatile packaging and dispensing approaches for the biological control of fungi, bacteria, and viruses. In this regard, recent developments on technologies to analyze and detect microbial volatile compounds are introduced. Furthermore, we survey the chemical encapsulation, slow-release, and bio-nano techniques for volatile formulation and delivery that are expected to overcome limitations in the application of biogenic volatiles to modern agriculture. Collectively, technological advances in volatile compound detection, packaging, and delivery provide great potential for the implementation of ecologically-sound plant disease management strategies. We hope that this review will help farmers and young scientists understand the nature of microbial volatile compounds, and shift paradigms on disease diagnosis and management to aromatic (volatile-based) agriculture.

휘발성물질은 자연에서 어디에나 존재한다. 생태학적으로 식물이나 미생물이 생산하는 휘발성물질은 식물-미생물이나 미생물-미생물간 대화에 중요한 역할을 수행한다. 정족수 인식신호는 세균과 세균 사이의 짧은 거리에서만 영향을 미치지만 휘발성물질은 20 cm 이상의 거리에서 생명체 간 신호전달이 가능하다. 이번 리뷰에서는 휘발성물질을 이용한 식물병진단과 진균, 세균, 바이러스병의 생물적방제의 최신 결과를 소개하였다. 더불어 이러한 휘발성물질을 농업에 적용하기 위한 다양한 기술들도 소개하였다. 휘발성물질의 캡슐화와 서방형 제제화 그리고 바이오나노 융합기술은 기존의 휘발성 물질 적용 한계를 넘게 해 줄 것이다. 종합하면 휘발성물질은 식물병을 효과적으로 방제할 수 있는 새로운 방법이다. 이번 리뷰를 통하여 농민들과 젊은 연구자들이 휘발성물질에 대한 이해를 높이고 향기농업으로의 전환을 앞당기는 계기가 되기를 희망한다.

Keywords

Acknowledgement

This research was supported by grants from a project of the National Research Foundation of Korea (NRF) funded by the Ministry of Science & ICT (NRF-2020M3E9A1111636), and from the KRIBB initiative program, South Korea.

References

  1. Aksenov, A. A., Pasamontes, A., Peirano, D. J., Zhao, W., Dandekar, A. M., Fiehn, O. et al. 2014. Detection of Huanglongbing disease using differential mobility spectrometry. Anal. Chem. 86: 2481-2488. https://doi.org/10.1021/ac403469y
  2. Amavizca, E., Bashan, Y., Ryu, C.-M., Farag, M. A., Bebout, B. M. and de-Bashan, L. E. 2017. Enhanced performance of the microalga Chlorella sorokiniana remotely induced by the plant growthpromoting bacteria Azospirillum brasilense and Bacillus pumilus. Sci. Rep. 7: 41310. https://doi.org/10.1038/srep41310
  3. Attaran, E., Rostas, M. and Zeier, J. 2008. Pseudomonas syringae elicits emission of the terpenoid (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene in Arabidopsis leaves via jasmonate signaling and expression of the terpene synthase TPS4. Mol. Plant-Microbe Interact. 21: 1482-1497. https://doi.org/10.1094/MPMI-21-11-1482
  4. Audrain, B., Farag, M. A., Ryu, C.-M. and Ghigo, J.-M. 2015. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol. Rev. 39: 222-233. https://doi.org/10.1093/femsre/fuu013
  5. Avalos, M., van Wezel, G. P., Raaijmakers, J. M. and Garbeva, P. 2018. Healthy scents: microbial volatiles as new frontier in antibiotic research? Curr. Opin. Microbiol. 45: 84-91. https://doi.org/10.1016/j.mib.2018.02.011
  6. Bakry, A. M., Abbas, S., Ali, B., Majeed, H., Abouelwafa, M. Y., Mousa, A. et al. 2016. Microencapsulation of oils: a comprehensive review of benefits, techniques, and applications. Compr. Rev. Food Sci. Food Saf. 15: 143-182. https://doi.org/10.1111/1541-4337.12179
  7. Banchio, E., Xie, X., Zhang, H. and Pare, P. W. 2009. Soil bacteria elevate essential oil accumulation and emissions in sweet basil. J. Agric. Food Chem. 57: 653-657. https://doi.org/10.1021/jf8020305
  8. Beck, J. J., Porter, N., Cook, D., Gee, W. S., Griffith, C. M., Rands, A. D. et al. 2015. In-field volatile analysis employing a hand-held portable GC-MS: emission profiles differentiate damaged and undamaged yellow starthistle flower heads. Phytochem. Anal. 26: 395-403. https://doi.org/10.1002/pca.2573
  9. Blake, R. S., Monks, P. S. and Ellis, A. M. 2009. Proton-transfer reaction mass spectrometry. Chem. Rev. 109: 861-896. https://doi.org/10.1021/cr800364q
  10. Blasioli, S., Biondi, E., Samudrala, D., Spinelli, F., Cellini, A., Bertaccini, A. et al. 2014. Identification of volatile markers in potato brown rot and ring rot by combined GC-MS and PTR-MS techniques: study on in vitro and in vivo samples. J. Agric. Food Chem. 62: 337-347. https://doi.org/10.1021/jf403436t
  11. Boland, W. 1995. The chemistry of gamete attraction: chemical structures, biosynthesis, and (a)biotic degradation of algal pheromones. Proc. Natl. Acad. Sci. U. S. A. 92: 37-43. https://doi.org/10.1073/pnas.92.1.37
  12. Broberg, M., Lee, G. W., Nykyri, J., Lee, Y. H., Pirhonen, M. and Palva, E. T. 2014. The global response regulator ExpA controls virulence gene expression through RsmA-mediated and RsmA-independent pathways in Pectobacterium wasabiae SCC3193. Appl. Environ. Microbiol. 80: 1972-1984. https://doi.org/10.1128/AEM.03829-13
  13. Buckley, A. M. and Greenblatt, M. 1994. The sol-gel preparation of silica gels. J. Chem. Educ. 71: 599. https://doi.org/10.1021/ed071p599
  14. Bui, H. X., Hadi, B. A. R., Oliva, R. and Schroeder, N. E. 2020. Beneficial bacterial volatile compounds for the control of root-knot nematode and bacterial leaf blight on rice. Crop Prot. 135: 104792. https://doi.org/10.1016/j.cropro.2019.04.016
  15. Castelyn, H. D., Appelgryn, J. J., Mafa, M. S., Pretorius, Z. A. and Visser, B. 2014. Volatiles emitted by leaf rust infected wheat induce a defence response in exposed uninfected wheat seedlings. Australas. Plant Pathol. 44: 245-254. https://doi.org/10.1007/s13313-014-0336-1
  16. Cellini, A., Biondi, E., Buriani, G., Farneti, B., Rodriguez-Estrada, M. T., Braschi, I. et al. 2016. Characterization of volatile organic compounds emitted by kiwifruit plants infected with Pseudomonas syringae pv. actinidiae and their effects on host defences. Trees 30: 795-806. https://doi.org/10.1007/s00468-015-1321-1
  17. Cellini, A., Buriani, G., Rocchi, L., Rondelli, E., Savioli, S., Rodriguez Estrada, M. T. et al. 2018. Biological relevance of volatile organic compounds emitted during the pathogenic interactions between apple plants and Erwinia amylovora. Mol. Plant Pathol. 19: 158-168. https://doi.org/10.1111/mpp.12509
  18. Cellini, A., Spinelli, F., Donati, I., Ryu, C.-M. and Kloepper, J. W. 2021. Bacterial volatile compound-based tools for crop management and quality. Trends Plant Sci. 26: 968-983. https://doi.org/10.1016/j.tplants.2021.05.006
  19. Chan, A. S., Valle, J. D., Lao, K., Malapit, C., Chua, M. and So, R. C. 2009. Evaluation of silica-gel microcapsule for the controlled release of insect repellent, N,N-diethyl-2-methoxybenzaimide, on cotton. Philipp. J. Sci. 138: 13-21.
  20. Chinchilla, D., Bruisson, S., Meyer, S., Zuhlke, D., Hirschfeld, C., Joller, C. et al. 2019. A sulfur-containing volatile emitted by potato-associated bacteria confers protection against late blight through direct anti-oomycete activity. Sci. Rep. 9: 18778. https://doi.org/10.1038/s41598-019-55218-3
  21. Cho, G., Kim, J., Park, C. G., Nislow, C., Weller, D. M. and Kwak, Y.-S. 2017. Caryolan-1-ol, an antifungal volatile produced by Streptomyces spp., inhibits the endomembrane system of fungi. Open Biol. 7: 170075. https://doi.org/10.1098/rsob.170075
  22. 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. J. Chem. Ecol. 40: 882-892. https://doi.org/10.1007/s10886-014-0488-z
  23. 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 Mol. Biol. 90: 677-687. https://doi.org/10.1007/s11103-015-0344-8
  24. Contreras, J. A., Murray, J. A., Tolley, S. E., Oliphant, J. L., Tolley, H. D., Lammert, S. A. et al. 2008. Hand-portable gas chromatograph-toroidal ion trap mass spectrometer (GC-TMS) for detection of hazardous compounds. J. Am. Soc. Mass Spectr. 19: 1425-1434. https://doi.org/10.1016/j.jasms.2008.06.022
  25. Cortes-Barco, A. M., Goodwin, P. H. and Hsiang, T. 2010a. Comparison of induced resistance activated by benzothiadiazole, (2R,3R)-butanediol and an isoparaffin mixture against anthracnose of Nicotiana benthamiana. Plant Pathol. 59: 643-653. https://doi.org/10.1111/j.1365-3059.2010.02283.x
  26. Cortes-Barco, A. M., Hsiang, T. and Goodwin, P. H. 2010b. Induced systemic resistance against three foliar diseases of Agrostis stolonifera by (2R,3R)-butanediol or an isoparaffin mixture. Ann. Appl. Biol. 157: 179-189. https://doi.org/10.1111/j.1744-7348.2010.00417.x
  27. D'Alessandro, M., Erb, M., Ton, J., Brandenburg, A., Karlen, D., Zopfi, J. et al. 2014. Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ. 37: 813-826. https://doi.org/10.1111/pce.12220
  28. Dandurishvili, N., Toklikishvili, N., Ovadis, M., Eliashvili, P., Giorgobiani, N., Keshelava, R. et al. 2011. Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants. J. Appl. Microbiol. 110: 341-352. https://doi.org/10.1111/j.1365-2672.2010.04891.x
  29. Deng, C., Zhang, X. and Li, N. 2004. Investigation of volatile biomarkers in lung cancer blood using solid-phase microextraction and capillary gas chromatography-mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 808: 269-277. https://doi.org/10.1016/j.jchromb.2004.05.015
  30. Elmassry, M. M. and Piechulla, B. 2020. Volatilomes of bacterial infections in humans. Front. Neurosci. 14: 257. https://doi.org/10.3389/fnins.2020.00257
  31. Farag, M. A., Song, G. C., Park, Y.-S., Audrain, B., Lee, S., Ghigo, J.-M. et al. 2017. Biological and chemical strategies for exploring inter- and intra-kingdom communication mediated via bacterial volatile signals. Nat. Protoc. 12: 1359-1377. https://doi.org/10.1038/nprot.2017.023
  32. Fatima, S. and Anjum, T. 2017. Identification of a potential ISR determinant from Pseudomonas aeruginosa PM12 against Fusarium wilt in tomato. Front. Plant Sci. 8: 848. https://doi.org/10.3389/fpls.2017.00848
  33. Feron, G., Mauvais, G., Martin, F., Semon, E. and Blin-Perrin, C. 2007. Microbial production of 4-hydroxybenzylidene acetone, the direct precursor of raspberry ketone. Lett. Appl. Microbiol. 45: 29-35. https://doi.org/10.1111/j.1472-765X.2007.02147.x
  34. Frost, C. J., Appel, H. M., Carlson, J. E., De Moraes, C. M., Mescher, M. C. and Schultz, J. C. 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 10: 490-498. https://doi.org/10.1111/j.1461-0248.2007.01043.x
  35. Garbeva, P. and Weisskopf, L. 2020. Airborne medicine: bacterial volatiles and their influence on plant health. New Phytol. 226: 32-43. https://doi.org/10.1111/nph.16282
  36. Ghosh, S. K. 2006. Functional coatings and microencapsulation: a general perspective. In: Functional Coatings, ed. by S. K. Ghosh, pp. 1-28. Wiley-VCH Verlag, Weinheim, Germany.
  37. Gong, A.-D., Wu, N.-N., Kong, X.-W., Zhang, Y.-M., Hu, M.-J., Gong, S.-J. et al. 2019. Inhibitory effect of volatiles emitted from Alcaligenes faecalis N1-4 on Aspergillus flavus and aflatoxins in storage. Front. Microbiol. 10: 1419. https://doi.org/10.3389/fmicb.2019.01419
  38. Han, S. H., Lee, S. J., Moon, J. H., Park, K. H., Yang, K. Y., Cho, B. H. 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. Mol. Plant-Microbe Interact. 19: 924-930. https://doi.org/10.1094/mpmi-19-0924
  39. Hao, H.-T., Zhao, X., Shang, Q.-H., Wang, Y., Guo, Z.-H., Zhang, Y.-B. et al. 2016. Comparative digital gene expression analysis of the Arabidopsis response to volatiles emitted by Bacillus amyloliquefaciens. PLoS ONE 11: e0158621. https://doi.org/10.1371/journal.pone.0158621
  40. Havenga, W. J. and Rohwer, E. R. 2000. The use of SPME and GC-MS for the chemical characterisation and assessment of PAH pollution in aqueous environmental samples. Int. J. Environ. Anal. Chem. 78: 205-221. https://doi.org/10.1080/03067310008041342
  41. Heil, M. 2014. Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol. 204: 297-306. https://doi.org/10.1111/nph.12977
  42. Heuskin, S., Lorge, S., Lognay, G., Wathelet, J.-P., Bera, F., Leroy, P. et al. 2012. A semiochemical slow-release formulation in a biological control approach to attract hoverflies. J. Environ. Ecol. 3: 72-85.
  43. Huang, C.-J., Tsay, J.-F., Chang, S.-Y., Yang, H.-P., Wu, W.-S. and Chen, C.-Y. 2012. Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag. Sci. 68: 1306-1310. https://doi.org/10.1002/ps.3301
  44. Huang, J., Cardoza, Y. J., Schmelz, E. A., Raina, R., Engelberth, J. and Tumlinson, J. H. 2003. Differential volatile emissions and salicylic acid levels from tobacco plants in response to different strains of Pseudomonas syringae. Planta 217: 767-775. https://doi.org/10.1007/s00425-003-1039-y
  45. Jyothi, N. V. N., Prasanna, P. M., Sakarkar, S. N., Prabha, K. S., Ramaiah, P. S. and Srawan, G. Y. 2010. Microencapsulation techniques, factors influencing encapsulation efficiency. J. Microencapsul. 27: 187-197. https://doi.org/10.3109/02652040903131301
  46. Kai, M. and Piechulla, B. 2009. Plant growth promotion due to rhizobacterial volatiles: an effect of CO2? FEBS Lett. 583: 3473-3477. https://doi.org/10.1016/j.febslet.2009.09.053
  47. Kim, K.-S., Lee, S. and Ryu, C.-M. 2013. Interspecific bacterial sensing through airborne signals modulates locomotion and drug resistance. Nat. Commun. 4: 1809. https://doi.org/10.1038/ncomms2789
  48. Kishimoto, K., Matsui, K., Ozawa, R. and Takabayashi, J. 2005. Volatile C6-aldehydes and Allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol. 46: 1093-1102. https://doi.org/10.1093/pcp/pci122
  49. Kishimoto, K., Matsui, K., Ozawa, R. and Takabayashi, J. 2006. Components of C6-aldehyde-induced resistance in Arabidopsis thaliana against a necrotrophic fungal pathogen, Botrytis cinerea. Plant Sci. 170: 715-723. https://doi.org/10.1016/j.plantsci.2005.11.002
  50. Kishimoto, K., Matsui, K., Ozawa, R. and Takabayashi, J. 2007. Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J. Gen. Plant Pathol. 73: 35-37. https://doi.org/10.1007/s10327-006-0314-8
  51. Koiv, V., Andresen, L., Broberg, M., Frolova, J., Somervuo, P., Auvinen, P. et al. 2013. Lack of RsmA-mediated control results in constant hypervirulence, cell elongation, and hyperflagellation in Pectobacterium wasabiae. PLoS One 8: e54248. https://doi.org/10.1371/journal.pone.0054248
  52. Kong, H. G., Shin, T. S., Kim, T. H. and Ryu, C.-M. 2018. Stereoisomers of the bacterial volatile compound 2,3-butanediol differently elicit systemic defense responses of pepper against multiple viruses in the field. Front. Plant Sci. 9: 90. https://doi.org/10.3389/fpls.2018.00090
  53. Lammers, A., Lalk, M. and Garbeva, P. 2022. Air ambulance: antimicrobial power of bacterial volatiles. Antibiotics (Basel) 11: 109. https://doi.org/10.3390/antibiotics11010109
  54. Ledger, T., Rojas, S., Timmermann, T., Pinedo, I., Poupin, M. J., Garrido, T. et al. 2016. Volatile-mediated effects predominate in Paraburkholderia phytofirmans growth promotion and salt stress tolerance of Arabidopsis thaliana. Front. Microbiol. 7: 1838.
  55. Lee, B., Farag, M. A., Park, H. B., Kloepper, J. W., Lee, S. H. and Ryu, C.-M. 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: e48744. https://doi.org/10.1371/journal.pone.0048744
  56. Lemfack, M. C., Gohlke, B.-O., Toguem, S. M. T., Preissner, S., Piechulla, B. and Preissner, R. 2017. mVOC 2.0: a database of microbial volatiles. Nucleic Acids Res. 46: D1261-D1265. https://doi.org/10.1093/nar/gkx1016
  57. Li, Z., Paul, R., Ba Tis, T., Saville, A. C., Hansel, J. C., Yu, T. et al. 2019. Non-invasive plant disease diagnostics enabled by smartphone-based fingerprinting of leaf volatiles. Nat. Plants 5: 856-866. https://doi.org/10.1038/s41477-019-0476-y
  58. Lindinger, W. and Jordan, A. 1998. Proton-transfer-reaction mass spectrometry (PTR-MS): on-line monitoring of volatile organic compounds at pptv levels. Chem. Soc. Rev. 27: 347-375. https://doi.org/10.1039/a827347z
  59. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. and Fernie, A. R. 2006. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1: 387-396. https://doi.org/10.1038/nprot.2006.59
  60. Lyu, A., Yang, L., Wu, M., Zhang, J. and Li, G. 2020. High efficacy of the volatile organic compounds of Streptomyces yanglinensis 3-10 in suppression of Aspergillus contamination on peanut kernels. Front. Microbiol. 11: 142. https://doi.org/10.3389/fmicb.2020.00142
  61. Massberg, D. and Hatt, H. 2018. Human olfactory receptors: novel cellular functions outside of the nose. Physiol. Rev. 98: 1739-1763. https://doi.org/10.1152/physrev.00013.2017
  62. Massawe, V. C., Hanif, A., Farzand, A., Mburu, D. K., Ochola, S. O., Wu, L. et al. 2018. Volatile compounds of endophytic Bacillus spp. have biocontrol activity against Sclerotinia sclerotiorum. Phytopathology 108: 1373-1385. https://doi.org/10.1094/phyto-04-18-0118-r
  63. Miekisch, W., Schubert, J. K. and Noeldge-Schomburg, G. F. E. 2004. Diagnostic potential of breath analysis: focus on volatile organic compounds. Clin. Chim. Acta 347: 25-39. https://doi.org/10.1016/j.cccn.2004.04.023
  64. Naznin, H. A., Kiyohara, D., Kimura, M., Miyazawa, M., Shimizu, M. and Hyakumachi, M. 2014. Systemic resistance induced by volatile organic compounds emitted by plant growth-promoting fungi in Arabidopsis thaliana. PLoS One 9: e86882. https://doi.org/10.1371/journal.pone.0086882
  65. Ojaghian, M. R., Wang, L., Xie, G.-L. and Zhang, J.-Z. 2019. Effect of volatiles produced by Trichoderma spp. on expression of glutathione transferase genes in Sclerotinia sclerotiorum. Biol. Control 136: 103999. https://doi.org/10.1016/j.biocontrol.2019.103999
  66. Peng, G., Zhao, X., Li, Y., Wang, R., Huang, Y. and Qi, G. 2019. Engineering Bacillus velezensis with high production of acetoin primes strong induced systemic resistance in Arabidopsis thaliana. Microbiol. Res. 227: 126297. https://doi.org/10.1016/j.micres.2019.126297
  67. Poveda, J. 2021. Beneficial effects of microbial volatile organic compounds (MVOCs) in plants. Appl. Soil Ecol. 168: 104118. https://doi.org/10.1016/j.apsoil.2021.104118
  68. Prosen, H. and Zupancic-Kralj, L. 1999. Solid-phase microextraction. TrAC Trends Anal. Chem. 18: 272-282. https://doi.org/10.1016/S0165-9936(98)00109-5
  69. Rajer, F. U., Wu, H., Xie, Y., Xie, S., Raza, W., Tahir, H. A. S. et al. 2017. Volatile organic compounds produced by a soil-isolate, Bacillus subtilis FA26 induce adverse ultra-structural changes to the cells of Clavibacter michiganensis ssp. sepedonicus, the causal agent of bacterial ring rot of potato. Microbiology (Reading) 163: 523-530. https://doi.org/10.1099/mic.0.000451
  70. Raza, W., Ling, N., Liu, D., Wei, Z., Huang, Q. and Shen, Q. 2016a. Volatile organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiol. Res. 192: 103-113. https://doi.org/10.1016/j.micres.2016.05.014
  71. Raza, W., Ling, N., Yang, L., Huang, Q. and Shen, Q. 2016b. Response of tomato wilt pathogen Ralstonia solanacearum to the volatile organic compounds produced by a biocontrol strain Bacillus amyloliquefaciens SQR-9. Sci. Rep. 6: 24856. https://doi.org/10.1038/srep24856
  72. Rezende, D. C., Fialho, M. B., Brand, S. C., Blumer, S. and Pascholati, S. F. 2015. Antimicrobial activity of volatile organic compounds and their effect on lipid peroxidation and electrolyte loss in Colletotrichum gloeosporioides and Colletotrichum acutatum mycelia. Afr. J. Microbiol. Res. 9: 1527-1535. https://doi.org/10.5897/AJMR2015.7425
  73. Rosenberg, M., Kopelman, I. J. and Talmon, Y. 1990. Factors affecting retention in spray-drying microencapsulation of volatile materials. J. Agric. Food Chem. 38: 1288-1294. https://doi.org/10.1021/jf00095a030
  74. Rudrappa, T., Biedrzycki, M. L., Kunjeti, S. G., Donofrio, N. M., Czymmek, K. J., Pare, P. W. et al. 2010. The rhizobacterial elicitor acetoin induces systemic resistance in Arabidopsis thaliana. Commun. Integr. Biol. 3: 130-138. https://doi.org/10.4161/cib.3.2.10584
  75. Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Kloepper, J. W. and Pare, P. W. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134: 1017-1026. https://doi.org/10.1104/pp.103.026583
  76. Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Wei, H.-X., Pare, P. W. et al. 2003. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 100: 4927-4932. https://doi.org/10.1073/pnas.0730845100
  77. Santoro, M. V., Zygadlo, J., Giordano, W. and Banchio, E. 2011. Volatile organic compounds from rhizobacteria increase biosynthesis of essential oils and growth parameters in peppermint (Mentha piperita). Plant Physiol. Biochem. 49: 1177-1182. https://doi.org/10.1016/j.plaphy.2011.07.016
  78. Santos, F. J. and Galceran, M. T. 2003. Modern developments in gas chromatography-mass spectrometry-based environmental analysis. J. Chromatogr. A 1000: 125-151. https://doi.org/10.1016/S0021-9673(03)00305-4
  79. Scala, A., Allmann, S., Mirabella, R., Haring, M. A. and Schuurink, R. C. 2013. Green leaf volatiles: a plant's multifunctional weapon against herbivores and pathogens. Int. J. Mol. Sci. 14: 17781-17811. https://doi.org/10.3390/ijms140917781
  80. Schulz-Bohm, K., Gerards, S., Hundscheid, M., Melenhorst, J., de Boer, W. and Garbeva, P. 2018. Calling from distance: attraction of soil bacteria by plant root volatiles. ISME J. 12: 1252-1262. https://doi.org/10.1038/s41396-017-0035-3
  81. Schulz-Bohm, K., Martin-Sanchez, L. and Garbeva, P. 2017. Microbial volatiles: small molecules with an important role in intra- and inter-kingdom interactions. Front. Microbiol. 8: 2484. https://doi.org/10.3389/fmicb.2017.02484
  82. Schulz, S. and Dickschat, J. S. 2007. Bacterial volatiles: the smell of small organisms. Nat. Prod. Rep. 24: 814-842. https://doi.org/10.1039/b507392h
  83. Sharifi, R., Lee, S.-M. and Ryu, C.-M. 2018. Microbe-induced plant volatiles. New Phytol. 220: 684-691. https://doi.org/10.1111/nph.14955
  84. 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? Front. Microbiol. 7: 196. https://doi.org/10.3389/fmicb.2016.00196
  85. Sharifi, R. and Ryu, C.-M. 2018. Biogenic volatile compounds for plant disease diagnosis and health improvement. Plant Pathol. J. 34: 459-469. https://doi.org/10.5423/PPJ.RW.06.2018.0118
  86. Sholberg, P. and Randall, P. 2005. Hexanal vapor for postharvest decay control and aroma production in stored pome fruit. Phytopathology 95: S96.
  87. Sholberg, P. and Randall, P. 2007. Fumigation of stored pome fruit with hexanal reduces blue and gray mold decay. HortScience 42: 611-616. https://doi.org/10.21273/hortsci.42.3.611
  88. Song, G. C., Riu, M. and Ryu, C.-M. 2019. Beyond the two compartments Petri-dish: optimising growth promotion and induced resistance in cucumber exposed to gaseous bacterial volatiles in a miniature greenhouse system. Plant Methods 15: 9. https://doi.org/10.1186/s13007-019-0395-y
  89. Song, G. C. 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. Int. J. Mol. Sci. 14: 9803-9819. https://doi.org/10.3390/ijms14059803
  90. Soottitantawat, A., Yoshii, H., Furuta, T., Ohkawara, M. and Linko, P. 2003. Microencapsulation by spray drying: influence of emulsion size on the retention of volatile compounds. J. Food Sci. 68: 2256-2262. https://doi.org/10.1111/j.1365-2621.2003.tb05756.x
  91. Spinelli, F., Cellini, A., Vanneste, J. L., Rodriguez-Estrada, M. T., Costa, G., Savioli, S. et al. 2012. Emission of volatile compounds by Erwinia amylovora: biological activity in vitro and possible exploitation for bacterial identification. Trees 26: 141-152. https://doi.org/10.1007/s00468-011-0667-2
  92. Spinelli, F., Noferini, M., Vanneste, J. L. and Costa, G. 2010. Potential of the electronic-nose for the diagnosis of bacterial and fungal diseases in fruit trees. EPPO Bull. 40: 59-67. https://doi.org/10.1111/j.1365-2338.2009.02355.x
  93. Sri, S., Seethadevi, A., Suria Prabha, K., Muthuprasanna, P. and Pavitra, P. 2012. Microencapsulation: a review. Int. J. Pharm. Bio Sci. 3: P509-P531.
  94. Tahir, H. A. S., Gu, Q., Wu, H., Niu, Y., Huo, R. and Gao, X. 2017. Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci. Rep. 7: 40481. https://doi.org/10.1038/srep40481
  95. Tyagi, S., Lee, K.-J., Shukla, P. and Chae, J.-C. 2020. Dimethyl disulfide exerts antifungal activity against Sclerotinia minor by damaging its membrane and induces systemic resistance in host plants. Sci. Rep. 10: 6547. https://doi.org/10.1038/s41598-020-63382-0
  96. Ul Hassan, M. N., Zainal, Z. and Ismail, I. 2015. Green leaf volatiles: biosynthesis, biological functions and their applications in biotechnology. Plant Biotechnol. J. 13: 727-739. https://doi.org/10.1111/pbi.12368
  97. Vandendriessche, T., Keulemans, J., Geeraerd, A., Nicolai, B. M. and Hertog, M. L. A. T. M. 2012. Evaluation of fast volatile analysis for detection of Botrytis cinerea infections in strawberry. Food Microbiol. 32: 406-414. https://doi.org/10.1016/j.fm.2012.08.002
  98. Velazquez-Becerra, C., Macias-Rodriguez, L. I., Lopez-Bucio, J., Flores-Cortez, I., Santoyo, G., Hernandez-Soberano, C. et al. 2013. The rhizobacterium Arthrobacter agilis produces dimethylhexadecylamine, a compound that inhibits growth of phytopathogenic fungi in vitro. Protoplasma 250: 1251-1262. https://doi.org/10.1007/s00709-013-0506-y
  99. Weise, T., Kai, M., Gummesson, A., Troeger, A., von Reuss, S., Piepenborn, S. et al. 2012. Volatile organic compounds produced by the phytopathogenic bacterium Xanthomonas campestris pv. vesicatoria 85-10. Beilstein J. Org. Chem. 8: 579-596. https://doi.org/10.3762/bjoc.8.65
  100. Weisskopf, L., Schulz, S. and Garbeva, P. 2021. Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions. Nat. Rev. Microbiol. 19: 391-404. https://doi.org/10.1038/s41579-020-00508-1
  101. Xiao, Z., Liu, W., Zhu, G., Zhou, R. and Niu, Y. 2014. A review of the preparation and application of flavour and essential oils microcapsules based on complex coacervation technology. J. Sci. Food Agric. 94: 1482-1494. https://doi.org/10.1002/jsfa.6491
  102. Xie, S., Zang, H., Wu, H., Uddin Rajer, F. and Gao, X. 2018. Antibacterial effects of volatiles produced by Bacillus strain D13 against Xanthomonas oryzae pv. oryzae. Mol. Plant Pathol. 19: 49-58. https://doi.org/10.1111/mpp.12494
  103. Yang, M., Lu, L., Pang, J., Hu, Y., Guo, Q., Li, Z. et al. 2019. Biocontrol activity of volatile organic compounds from Streptomyces alboflavus TD-1 against Aspergillus flavus growth and aflatoxin production. J. Microbiol. 57: 396-404. https://doi.org/10.1007/s12275-019-8517-9
  104. Yu, Y. T., Liu, L. N., Zhu, X. L. and Kong, X. Z. 2012. Microencapsulation of dodecyl acetate by complex coacervation of whey protein with acacia gum and its release behavior. Chin. Chem. Lett. 23: 847-850. https://doi.org/10.1016/j.cclet.2012.05.006
  105. Zada, A., Falach, L. and Byers, J. A. 2009. Development of sol-gel formulations for slow release of pheromones. Chemoecology 19: 37-45. https://doi.org/10.1007/s00049-009-0007-9
  106. Zhang, C., Zhang, M., Yan, Z., Wang, F., Yuan, X., Zhao, S. et al. 2021. CO2 is a key constituent of the plant growth-promoting volatiles generated by bacteria in a sealed system. Plant Cell Rep. 40: 59-68. https://doi.org/10.1007/s00299-020-02610-3
  107. Zhang, Y., Li, T., Liu, Y., Li, X., Zhang, C., Feng, Z. et al. 2019. Volatile organic compounds produced by Pseudomonas chlororaphis subsp. aureofaciens SPS-41 as biological fumigants to control Ceratocystis fimbriata in postharvest sweet potatoes. J. Agric. Food Chem. 67: 3702-3710. https://doi.org/10.1021/acs.jafc.9b00289
  108. Zhao, P., Li, P., Wu, S., Zhou, M., Zhi, R. and Gao, H. 2019. Volatile organic compounds (VOCs) from Bacillus subtilis CF-3 reduce anthracnose and elicit active defense responses in harvested litchi fruits. AMB Express 9: 119. https://doi.org/10.1186/s13568-019-0841-2
  109. Zhou, J.-Y., Li, X., Zheng, J.-Y. and Dai, C.-C. 2016. Volatiles released by endophytic Pseudomonas fluorescens promoting the growth and volatile oil accumulation in Atractylodes lancea. Plant Physiol. Biochem. 101: 132-140. https://doi.org/10.1016/j.plaphy.2016.01.026