Bacterial Volatiles Induce Systemic Resistance in Arabidopsis
Open accessAbstract
Plant growth-promoting rhizobacteria, in association with plant roots, can trigger induced systemic resistance (ISR). Considering that low-molecular weight volatile hormone analogues such as methyl jasmonate and methyl salicylate can trigger defense responses in plants, we examined whether volatile organic compounds (VOCs) associated with rhizobacteria can initiate ISR. In Arabidopsis seedlings exposed to bacterial volatile blends from Bacillus subtilis GB03 and Bacillus amyloliquefaciens IN937a, disease severity by the bacterial pathogen Erwinia carotovora subsp. carotovora was significantly reduced compared with seedlings not exposed to bacterial volatiles before pathogen inoculation. Exposure to VOCs from rhizobacteria for as little as 4 d was sufficient to activate ISR in Arabidopsis seedlings. Chemical analysis of the bacterial volatile emissions revealed the release of a series of low-molecular weight hydrocarbons including the growth promoting VOC (2R,3R)-(-)-butanediol. Exogenous application of racemic mixture of (RR) and (SS) isomers of 2,3-butanediol was found to trigger ISR and transgenic lines of B. subtilis that emitted reduced levels of 2,3-butanediol and acetoin conferred reduced Arabidopsis protection to pathogen infection compared with seedlings exposed to VOCs from wild-type bacterial lines. Using transgenic and mutant lines of Arabidopsis, we provide evidence that the signaling pathway activated by volatiles from GB03 is dependent on ethylene, albeit independent of the salicylic acid or jasmonic acid signaling pathways. This study provides new insight into the role of bacteria VOCs as initiators of defense responses in plants.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Together these compounds function as signaling molecules and elicitors of tolerance to abiotic stressors in a process termed induced systemic tolerance (IST) as well as in triggering the host plant immune system in a process termed induced systemic resistance (ISR).
“Together these compounds function as signaling molecules (Fig. 7) and elicitors of tolerance to abiotic stressors (drought, salinity or nutrient imbalance) in a process termed induced systemic tolerance (IST) (Yang et al., 2009) as well as in triggering the host plant immune system in a process termed induced systemic resistance (ISR) (Ryu et al., 2004).”
From Intensify production, transform biomass to energy and novel goods and protect soils in Europe—A vision how to mobilize marginal lands (2018) · cites this paper as Ryu et al., 2004
Induction of ISR and subsequent signaling cascades results in accelerated responses to pathogen intrusion.
“Induction of ISR and subsequent signaling cascades results in accelerated responses to pathogen intrusion (Ryu et al., 2004;Van der Ent et al., 2009).”
From Intensify production, transform biomass to energy and novel goods and protect soils in Europe—A vision how to mobilize marginal lands (2018) · cites this paper as Ryu et al., 2004
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The enhancement of plant growth by free-living bacteria
Glick, B. R. (1995) · Canadian Journal of Microbiology · doi:10.1139/m95-015 · Cited by 2,669 · see citing works
SYSTEMIC RESISTANCE INDUCED BY RHIZOSPHERE BACTERIA
van Loon, L. C., Bakker, P. A. H. M., & Pieterse, C. M. J. (1998) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.36.1.453 · Cited by 2,366 · see citing works
Isochorismate synthase is required to synthesize salicylic acid for plant defence
Wildermuth, M. C., Dewdney, J., Wu, G., & Ausubel, F. M. (2001) · Nature · doi:10.1038/35107108 · Cited by 2,360 · see citing works
Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature
Keßler, A., & Baldwin, I. T. (2001) · Science · doi:10.1126/science.291.5511.2141 · Cited by 2,191 · see citing works
Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H., & Hunt, D. M. (1996) · The Plant Cell · doi:10.1105/tpc.8.10.1809 · Cited by 2,060 · see citing works
Bacterial volatiles promote growth in Arabidopsis
Ryu, C., Farag, M. A., Hu, C., Reddy, M. S., Wei, H., Paré, P. W., & Kloepper, J. W. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0730845100 · Cited by 1,661 · see citing works
Self-citationCOI1 : An Arabidopsis Gene Required for Jasmonate-Regulated Defense and Fertility
Xie, D., Feys, B., James, S., Nieto‐Rostro, M., & Turner, J. G. (1998) · Science · doi:10.1126/science.280.5366.1091 · Cited by 1,657 · see citing works
Cao, H., Bowling, S. A., Gordon, A., & Dong, X. (1994) · The Plant Cell · doi:10.1105/tpc.6.11.1583 · Cited by 1,495 · see citing works
EIN2, a Bifunctional Transducer of Ethylene and Stress Responses in Arabidopsis
Alonso, J. M., Hirayama, T., Roman, G., Nourizadeh, S., & Ecker, J. R. (1999) · Science · doi:10.1126/science.284.5423.2148 · Cited by 1,297 · see citing works
Plant Volatiles as a Defense against Insect Herbivores
Paré, P. W., & Tumlinson, J. H. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.121.2.325 · Cited by 1,197 · see citing works
Airborne signalling by methyl salicylate in plant pathogen resistance
Shulaev, V., Silverman, P., & Raskin, I. (1997) · Nature · doi:10.1038/385718a0 · Cited by 823 · see citing works
Pieterse, C. M. J., Wees, S. C. M. V., Hoffland, E., van Pelt, J. A., & van Loon, L. C. (1996) · The Plant Cell · doi:10.1105/tpc.8.8.1225 · Cited by 777 · see citing works
van Peer, R. (1991) · Phytopathology · doi:10.1094/phyto-81-728 · Cited by 774 · see citing works
Delaney, T. P., Friedrich, L., & Ryals, J. A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.14.6602 · Cited by 772 · see citing works
Herbivory-induced volatiles elicit defence genes in lima bean leaves
Arimura, G., Ozawa, R., Shimoda, T., Nishioka, T., Boland, W., & Takabayashi, J. (2000) · Nature · doi:10.1038/35020072 · Cited by 763 · see citing works
Plant resistance towards insect herbivores: a dynamic interaction
Gatehouse, J. A. (2002) · New Phytologist · doi:10.1046/j.1469-8137.2002.00519.x · Cited by 704 · see citing works
Induced resistance in plants and the role of pathogenesis-related proteins
van Loon, L. C. (1997) · European Journal of Plant Pathology · doi:10.1023/a:1008638109140 · Cited by 691 · see citing works
Salicylic acid and disease resistance in plants
Durner, J., Shah, J., & Klessig, D. F. (1997) · Trends in Plant Science · doi:10.1016/s1360-1385(97)86349-2 · Cited by 671 · see citing works
A Mutation in Arabidopsis That Leads to Constitutive Expression of Systemic Acquired Resistance
Bowling, S. A., Guo, A., Cao, H., Gordon, A., Klessig, D. F., & Dong, X. (1994) · The Plant Cell · doi:10.1105/tpc.6.12.1845 · Cited by 637 · see citing works
Raupach, G. S., & Kloepper, J. W. (1998) · Phytopathology · doi:10.1094/phyto.1998.88.11.1158 · Cited by 634 · see citing works
Self-citationWei, G. (1991) · Phytopathology · doi:10.1094/phyto-81-1508 · Cited by 616 · see citing works
Maurhofer, M. (1994) · Phytopathology · doi:10.1094/phyto-84-139 · Cited by 537 · see citing works
Croft, K., Jüttner, F., & Slusarenko, A. J. (1993) · PLANT PHYSIOLOGY · doi:10.1104/pp.101.1.13 · Cited by 528 · see citing works
Shah, J., Tsui, F., & Klessig, D. F. (1997) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi.1997.10.1.69 · Cited by 524 · see citing works
Fatty acid-derived signals in plants
Weber, H. H. (2002) · Trends in Plant Science · doi:10.1016/s1360-1385(02)02250-1 · Cited by 470 · see citing works
New roles for cis -jasmone as an insect semiochemical and in plant defense
Birkett, M. A., Campbell, C. A. M., Chamberlain, K., Guerrieri, E., Hick, A. J., Martin, J. L., Matthes, M. C., Napier, J. A., Pettersson, J., Pickett, J. A., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.160241697 · Cited by 454 · see citing works
Plant growth-promoting rhizobacteria as biological control agents
Kloepper, J. W. (1992) · Cited by 360 · see citing works
Self-citationKloepper, J. W., Rodríguez-Kábana, R., Zehnder, G. W., Murphy, J. F., Sikora, E. J., & Fernández, C. (1999) · Australasian Plant Pathology · doi:10.1071/ap99003 · Cited by 320 · see citing works
Self-citationLeeman, M. (1996) · Phytopathology · doi:10.1094/phyto-86-149 · Cited by 299 · see citing works
Liu, L. (1995) · Phytopathology · doi:10.1094/phyto-85-843 · Cited by 289 · see citing works
Benhamou, N., Kloepper, J. W., & Tuzun, S. (1998) · Planta · doi:10.1007/s004250050242 · Cited by 286 · see citing works
Self-citationBent, A. F. (1992) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-5-372 · Cited by 284 · see citing works
Fermentative Metabolism of Bacillus subtilis : Physiology and Regulation of Gene Expression
Ramos, H. C., Hoffmann, T., Marino, M., Nedjari, H., Presecan, E., Dreesen, O., Glaser, P., & Jahn, D. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.11.3072-3080.2000 · Cited by 265 · see citing works
Raupach, G. S. (1996) · Plant Disease · doi:10.1094/pd-80-0891 · Cited by 260 · see citing works
Signalling in Rhizobacteria‐Induced Systemic Resistance in Arabidopsis thaliana
Pieterse, C. M. J., Wees, S. C. M. V., Ton, J., van Pelt, J. A., & van Loon, L. C. (2002) · Plant Biology · doi:10.1055/s-2002-35441 · Cited by 249 · see citing works
Plant Growth-Promoting Rhizobacterial Mediated Protection in Tomato Against Tomato mottle virus
Murphy, J. F., Zehnder, G. W., Schuster, D. J., Sikora, E. J., Polston, J. E., & Kloepper, J. W. (2000) · Plant Disease · doi:10.1094/pdis.2000.84.7.779 · Cited by 249 · see citing works
Self-citationC6-Green leaf volatiles trigger local and systemic VOC emissions in tomato
Farag, M. A., & Paré, P. W. (2002) · Phytochemistry · doi:10.1016/s0031-9422(02)00240-6 · Cited by 242 · see citing works
Self-citationLiechti, R., & Farmer, E. E. (2002) · Science · doi:10.1126/science.1071547 · Cited by 223 · see citing works
Fidantsef, A. L., Stout, M. J., Thaler, J. S., Duffey, S. S., & Bostock, R. M. (1999) · Physiological and Molecular Plant Pathology · doi:10.1006/pmpp.1998.0192 · Cited by 219 · see citing works
Hoffman, T. K., Schmidt, J., Zheng, X., & Bent, A. F. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.3.935 · Cited by 212 · see citing works
Zehnder, G. W., Yao, C., Murphy, J. F., Sikora, E., & Kloepper, J. W. (2000) · BioControl · doi:10.1023/a:1009923702103 · Cited by 209 · see citing works
Self-citationAlström, S. (1991) · The Journal of General and Applied Microbiology · doi:10.2323/jgam.37.495 · Cited by 207 · see citing works
Schmelz, E. A., Alborn, H. T., & Tumlinson, J. H. (2001) · Planta · doi:10.1007/s004250100603 · Cited by 193 · see citing works
Methyljasmonate-induced changes in the polypeptide pattern of senescing barley leaf segments
Weidhase, R. A., Kramell, H.-M., Lehmann, J., Liebisch, H. W., Lerbs, W., & Parthier, B. (1987) · Plant Science · doi:10.1016/0168-9452(87)90191-9 · Cited by 188 · see citing works
Plant–plant interactions mediated by volatiles emitted from plants infested by spider mites
Arimura, G., Ozawa, R., Horiuchi, J.-I., Nishioka, T., & Takabayashi, J. (2001) · Biochemical Systematics and Ecology · doi:10.1016/s0305-1978(01)00049-7 · Cited by 161 · see citing works
Dı́az, M., Achkor, H., Titarenko, E., & Martı́nez, M. C. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00426-5 · Cited by 152 · see citing works
Raupach, G. S., & Kloepper, J. W. (2000) · Plant Disease · doi:10.1094/pdis.2000.84.10.1073 · Cited by 140 · see citing works
Self-citationTon, J., Davison, S., Wees, S. C. M. V., van Loon, L. C., & Pieterse, C. M. J. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.125.2.652 · Cited by 108 · see citing works
Induced Resistance in the Biocontrol of Pythium aphanidermatum by Pseudomonas spp. on Cucumber
Zhou, T., & Paulitz, T. C. (1994) · Journal of Phytopathology · doi:10.1111/j.1439-0434.1994.tb00007.x · Cited by 93 · see citing works
Forlani, G., Mantelli, M., & Nielsen, E. (1999) · Phytochemistry · doi:10.1016/s0031-9422(98)00550-0 · Cited by 38 · see citing works
Plant growth enhancement by rhizobacteria
Cleyet-Marel, J.-C., Larcher, M., Bertrand, H., Rapior, S., & Pinochet, X. (2001) · HAL · Cited by 36 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
THE ROLE OF ROOT EXUDATES IN RHIZOSPHERE INTERACTIONS WITH PLANTS AND OTHER ORGANISMS
Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., & Vivanco, J. M. (2006) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.57.032905.105159 · Cited by 4,682 · see citing works
Structure and functions of the bacterial microbiota of plants
Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L., & Schulze-Lefert, P. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120106 · Cited by 3,308 · see citing works
Induced systemic resistance by beneficial microbes
Pieterse, C. M. J., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C. M., & Bakker, P. A. H. M. (2014) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-082712-102340 · Cited by 3,272 · see citing works
Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture
Bhattacharyya, P. N., & Jha, D. K. (2011) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-011-0979-9 · Cited by 2,922 · see citing works
Mendes, R., Garbeva, P., & Raaijmakers, J. M. (2013) · FEMS Microbiology Reviews · doi:10.1111/1574-6976.12028 · Cited by 2,836 · see citing works
Hardoim, P. R., van Overbeek, L. S., Berg, G., Pirttilä, A. M., Compant, S., Campisano, A., Döring, M., & Sessitsch, A. (2015) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00050-14 · Cited by 2,740 · see citing works
Compant, S., Duffy, B., Nowak, J., Clément, C., & Barka, E. A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.9.4951-4959.2005 · Cited by 2,640 · see citing works
Biological control of soil-borne pathogens by fluorescent pseudomonads
Haas, D., & Défago, G. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1129 · Cited by 2,611 · see citing works
Regulation and function of root exudates
Badri, D. V., & Vivanco, J. M. (2008) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2009.01926.x · Cited by 2,169 · see citing works
Soil beneficial bacteria and their role in plant growth promotion: a review
Hayat, R., Ali, S., Amara, U., Khalid, R., & Ahmed, I. (2010) · Annals of Microbiology · doi:10.1007/s13213-010-0117-1 · Cited by 2,064 · see citing works
Rhizosphere bacteria help plants tolerate abiotic stress
Yang, J., Kloepper, J. W., & Ryu, C.-M. (2009) · Trends in Plant Science · doi:10.1016/j.tplants.2008.10.004 · Cited by 1,852 · see citing works
Self-citationInduced Systemic Resistance and Promotion of Plant Growth by Bacillus spp.
Kloepper, J. W., Ryu, C., & Zhang, S. (2004) · Phytopathology · doi:10.1094/phyto.2004.94.11.1259 · Cited by 1,715 · see citing works
Self-citationProperties of bacterial endophytes and their proposed role in plant growth
Hardoim, P. R., van Overbeek, L. S., & van Elsas, J. D. (2008) · Trends in Microbiology · doi:10.1016/j.tim.2008.07.008 · Cited by 1,711 · see citing works
The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms
Raaijmakers, J., Paulitz, T., Steinberg, C., Alabouvette, C., & Moënne-Loccoz, Y. (2009) · Plant and Soil · doi:10.1007/s11104-008-9568-6 · Cited by 1,674 · see citing works
Priming: Getting Ready for Battle
Conrath, U., Beckers, G. J. M., Flors, V., García‐Agustín, P., Jakab, G., Mauch, F., Newman, M., Pieterse, C. M. J., Poinssot, B., Pozo, M. J., et al. (2006) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-19-1062 · Cited by 1,534 · see citing works
Bhardwaj, D., Ansari, M. W., Sahoo, R. K., & Tuteja, N. K. (2014) · Microbial Cell Factories · doi:10.1186/1475-2859-13-66 · Cited by 1,228 · see citing works
Root-Secreted Malic Acid Recruits Beneficial Soil Bacteria
Rudrappa, T., Czymmek, K. J., Paré, P. W., & Bais, H. P. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.127613 · Cited by 1,147 · see citing works
Plant-driven selection of microbes
Hartmann, A., Schmid, M., van Tuinen, D., & Berg, G. (2008) · Plant and Soil · doi:10.1007/s11104-008-9814-y · Cited by 1,091 · see citing works
Mycorrhiza-Induced Resistance and Priming of Plant Defenses
Jung, S. C., Martínez‐Medina, A., Lopez-Raez, J. A., & Pozo, M. J. (2012) · Journal of Chemical Ecology · doi:10.1007/s10886-012-0134-6 · Cited by 1,016 · see citing works
Defense Priming: An Adaptive Part of Induced Resistance
Mauch‐Mani, B., Baccelli, I., Luna, E., & Flors, V. (2017) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042916-041132 · Cited by 1,006 · see citing works
Plant immune responses triggered by beneficial microbes
Wees, S. C. M. V., der Ent, S. V., & Pieterse, C. M. J. (2008) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2008.05.005 · Cited by 919 · see citing works
Plant responses to plant growth-promoting rhizobacteria
van Loon, L. C. (2007) · European Journal of Plant Pathology · doi:10.1007/s10658-007-9165-1 · Cited by 915 · see citing works
Pii, Y., Mimmo, T., Tomasi, N., Terzano, R., Cesco, S., & Crecchio, C. (2015) · Biology and Fertility of Soils · doi:10.1007/s00374-015-0996-1 · Cited by 913 · see citing works
Etesami, H., & Maheshwari, D. K. (2018) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.03.013 · Cited by 904 · see citing works
Bacterial volatiles: the smell of small organisms
Schulz, S., & Dickschat, J. S. (2007) · Natural Product Reports · doi:10.1039/b507392h · Cited by 901 · see citing works
Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J. L., & Thonart, P. (2007) · Environmental Microbiology · doi:10.1111/j.1462-2920.2006.01202.x · Cited by 859 · see citing works
Biological Control of Plant Pathogens
Pal, K. K., & Gardener, B. M. (2006) · The Plant Health Instructor · doi:10.1094/phi-a-2006-1117-02 · Cited by 1,328 · see citing works
Overview of the Antimicrobial Compounds Produced by Members of the Bacillus subtilis Group
Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C., & Mahillon, J. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00302 · Cited by 830 · see citing works
<i>Bacillus</i> species as versatile weapons for plant pathogens: a review
Shafi, J., Tian, H., & Ji, M. (2017) · Biotechnology & Biotechnological Equipment · doi:10.1080/13102818.2017.1286950 · Cited by 821 · see citing works
Choudhary, D. K., & Johri, B. N. (2008) · Microbiological Research · doi:10.1016/j.micres.2008.08.007 · Cited by 789 · see citing works
Emerging microbial biocontrol strategies for plant pathogens
Syed-Ab-Rahman, S. F., Singh, E., Pieterse, C. M. J., & Schenk, P. M. (2017) · Plant Science · doi:10.1016/j.plantsci.2017.11.012 · Cited by 748 · see citing works
Role of microorganisms in adaptation of agriculture crops to abiotic stresses
Grover, M., Ali, S. Z., Sandhya, V., Rasul, A., & Venkateswarlu, B. (2010) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-010-0572-7 · Cited by 684 · see citing works
Diversity and Natural Functions of Antibiotics Produced by Beneficial and Plant Pathogenic Bacteria
Raaijmakers, J. M., & Mazzola, M. (2012) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-081211-172908 · Cited by 682 · see citing works
Venturi, V., & Keel, C. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.01.005 · Cited by 678 · see citing works
The role of microbial signals in plant growth and development
Ortiz‐Castro, R., Contreras‐Cornejo, H. Á., Macías‐Rodríguez, L., & López‐Bucio, J. (2009) · Plant Signaling & Behavior · doi:10.4161/psb.4.8.9047 · Cited by 637 · see citing works
Vardharajula, S., Ali, S. Z., Grover, M., Reddy, G., & Bandi, V. (2010) · Journal of Plant Interactions · doi:10.1080/17429145.2010.535178 · Cited by 621 · see citing works
Signal Crosstalk and Induced Resistance: Straddling the Line Between Cost and Benefit
Bostock, R. M. (2005) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.41.052002.095505 · Cited by 611 · see citing works
Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: A review
Numan, M., Bashir, S., Khan, Y. W., Mumtaz, R., Shinwari, Z. K., Khan, A. L., Khan, A., & Al-Harrasi, A. (2018) · Microbiological Research · doi:10.1016/j.micres.2018.02.003 · Cited by 607 · see citing works
Bacillus subtilis biofilm induction by plant polysaccharides
Beauregard, P. B., Chai, Y., Vlamakis, H. C., Losick, R. M., & Kolter, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218984110 · Cited by 604 · see citing works
Perspectives and Challenges of Microbial Application for Crop Improvement
Timmusk, S., Behers, L., Muthoni, J., Muraya, A. M., & Aronsson, A.-C. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00049 · Cited by 593 · see citing works
Metabolites from symbiotic bacteria
Piel, J. (2008) · Natural Product Reports · doi:10.1039/b703499g · Cited by 579 · see citing works
Induced Systemic Resistance for Improving Plant Immunity by Beneficial Microbes
Yu, Y., Gui, Y., Li, Z., Jiang, C., Guo, J., & Niu, D. (2022) · Plants · doi:10.3390/plants11030386 · Cited by 570 · see citing works
Ma, Y., Oliveira, R. S., Freitas, H. M. D. O., & Zhang, C. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.00918 · Cited by 569 · see citing works
Oleńska, E., Małek, W., Wójcik, M., Święcicka, I., Thijs, S., & Vangronsveld, J. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.140682 · Cited by 566 · see citing works
Induced systemic resistance (ISR) in plants: mechanism of action
Choudhary, D. K., Prakash, A., & Johri, B. N. (2007) · Indian Journal of Microbiology · doi:10.1007/s12088-007-0054-2 · Cited by 551 · see citing works
Bacillus velezensis: A Valuable Member of Bioactive Molecules within Plant Microbiomes
Rabbee, M. F., Ali, M. S., Choi, J., Hwang, B. S., Jeong, S. C., & Baek, K.-H. (2019) · Molecules · doi:10.3390/molecules24061046 · Cited by 550 · see citing works
Induced Systemic Resistance by Fluorescent Pseudomonas spp.
Bakker, P. A. H. M., Pieterse, C. M. J., & van Loon, L. C. (2007) · Phytopathology · doi:10.1094/phyto-97-2-0239 · Cited by 529 · see citing works
Zhang, H., Kim, M., Sun, Y., Dowd, S. E., Shi, H., & Paré, P. W. (2008) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-21-6-0737 · Cited by 527 · see citing works
A Review on Biological Control of Fungal Plant Pathogens Using Microbial Antagonists
Heydari, A., & Pessarakli, M. (2010) · Journal of Biological Sciences · doi:10.3923/jbs.2010.273.290 · Cited by 527 · see citing works
Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions
Weisskopf, L., Schulz, S., & Garbeva, P. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00508-1 · Cited by 523 · see citing works
Mhlongo, M. I., Piater, L. A., Madala, N. E., Labuschagne, N., & Dubery, I. A. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00112 · Cited by 522 · see citing works
Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis
Zhang, H., Kim, M.-S., Krishnamachari, V., Payton, P., Sun, Y., Grimson, M., Farag, M. A., Ryu, C.-M., Allen, R., Melo, I. S., et al. (2007) · Planta · doi:10.1007/s00425-007-0530-2 · Cited by 515 · see citing works
Self-citationTikunov, Y. M., Lommen, A., Vos, C. H. R. D., Verhoeven, H. A., Bino, R. J., Hall, R. D., & Bovy, A. G. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.068130 · Cited by 511 · see citing works
Chemical diversity of microbial volatiles and their potential for plant growth and productivity
Kanchiswamy, C. N., Malnoy, M., & Maffei, M. E. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00151 · Cited by 490 · see citing works
Plant-growth-promoting rhizobacteria to improve crop growth in saline soils: a review
PAUL, D. Z., & Lade, H. S. (2014) · Agronomy for Sustainable Development · doi:10.1007/s13593-014-0233-6 · Cited by 475 · see citing works
Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., Hutzler, P., Schmid, M., Breusegem, F. V., Eberl, L., et al. (2006) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2005.01471.x · Cited by 474 · see citing works
Microbial Volatile Emissions as Insect Semiochemicals
Davis, T. S., Crippen, T. L., Hofstetter, R. W., & Tomberlin, J. K. (2013) · Journal of Chemical Ecology · doi:10.1007/s10886-013-0306-z · Cited by 471 · see citing works
Choi, J., Huh, S. U., Kojima, M., Sakakibara, H., Paek, K.-H., & Hwang, I. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.07.011 · Cited by 470 · see citing works
Xiang, L., Harindintwali, J. D., Wang, F., Redmile-Gordon, M. A., Chang, S. X., Fu, Y., He, C., Muhoza, B., Brahushi, F., Bolan, N. S., et al. (2022) · Environmental Science & Technology · doi:10.1021/acs.est.2c02976 · Cited by 460 · see citing works
Induced resistance to control postharvest decay of fruit and vegetables
Romanazzi, G., Sanzani, S. M., Bi, Y., Tian, S., Gutiérrez–Martínez, P., & Alkan, N. (2016) · Postharvest Biology and Technology · doi:10.1016/j.postharvbio.2016.08.003 · Cited by 459 · see citing works
Role of bacterial volatile compounds in bacterial biology
Audrain, B., Farag, M. A., Ryu, C., & Ghigo, J. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuu013 · Cited by 457 · see citing works
Self-citationPlant growth-promoting rhizobacteria
Podile, A. R., & Kishore, G. K. (2006) · Kluwer Academic Publishers eBooks · doi:10.1007/978-1-4020-4538-7_6 · Cited by 455 · see citing works
Microbial Volatiles: Small Molecules with an Important Role in Intra- and Inter-Kingdom Interactions
Bohm, K., Martín-Sánchez, L., & Garbeva, P. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.02484 · Cited by 454 · see citing works
Cho, S. M., Kang, B. R., Han, S. H., Anderson, A. J., Park, J. Y., Lee, Y., Cho, B. H., Yang, K., Ryu, C., & Kim, Y. C. (2008) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-21-8-1067 · Cited by 444 · see citing works
Self-citationJasmonate signaling in plant interactions with resistance-inducing beneficial microbes
Van der Ent, S., Van Wees, S. C. M., & Pieterse, C. M. J. (2009) · Phytochemistry · doi:10.1016/j.phytochem.2009.06.009 · Cited by 443 · see citing works
Kaushal, M., & Wani, S. P. (2015) · Annals of Microbiology · doi:10.1007/s13213-015-1112-3 · Cited by 437 · see citing works
Plant Growth Promotion by Volatile Organic Compounds Produced by Bacillus subtilis SYST2
Tahir, H. A. S., Gu, Q., Wu, H., Raza, W., Hanif, A., Wu, L., Colman, M. V., & Gao, X. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00171 · Cited by 436 · see citing works
Fan, B., Wang, C., Song, X., Ding, X., Wu, L., Wu, H., Gao, X., & Borriss, R. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02491 · Cited by 436 · see citing works
Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani
Kai, M., Effmert, U., Berg, G., & Piechulla, B. (2006) · Archives of Microbiology · doi:10.1007/s00203-006-0199-0 · Cited by 426 · see citing works
Lee, S., Kong, H. G., Song, G. C., & Ryu, C. (2020) · The ISME Journal · doi:10.1038/s41396-020-00785-x · Cited by 425 · see citing works
Self-citationJi, S. H., Gururani, M. A., & Chun, S. (2013) · Microbiological Research · doi:10.1016/j.micres.2013.06.003 · Cited by 394 · see citing works
Blom, D., Fabbri, C., Connor, E. C., Schiestl, F. P., Klauser, D., Böller, T., Eberl, L., & Weisskopf, L. (2011) · Environmental Microbiology · doi:10.1111/j.1462-2920.2011.02582.x · Cited by 380 · see citing works
Farag, M. A., Ryu, C., Sumner, L. W., & Paré, P. W. (2006) · Phytochemistry · doi:10.1016/j.phytochem.2006.07.021 · Cited by 360 · see citing works
Self-citationMolecular Aspects of Plant Growth Promotion and Protection byBacillus subtilis
Blake, C., Nordgaard, M., & Kovács, Á. T. (2020) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-08-20-0225-cr · Cited by 360 · see citing works
Costs and trade-offs associated with induced resistance
Walters, D. R., & Heil, M. (2007) · Physiological and Molecular Plant Pathology · doi:10.1016/j.pmpp.2007.09.008 · Cited by 359 · see citing works
Upadhyay, S. K., Srivastava, A. K., Rajput, V. D., Chauhan, P. K., Bhojiya, A. A., Jain, D., Chaubey, G., Dwivedi, P., Sharma, B., & Minkina, T. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.916488 · Cited by 357 · see citing works
Zhang, H., Xie, X., Kim, M., Kornyeyev, D., Holaday, S., & Paré, P. W. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03593.x · Cited by 356 · see citing works
Endophytic Actinobacteria Induce Defense Pathways in Arabidopsis thaliana
Conn, V. M., Walker, A. R., & Franco, C. M. M. (2008) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-21-2-0208 · Cited by 355 · see citing works
Gao, Z., Zhang, B., Liu, H., Han, J., & Zhang, Y. (2016) · Biological Control · doi:10.1016/j.biocontrol.2016.11.007 · Cited by 353 · see citing works
Sniffing on Microbes: Diverse Roles of Microbial Volatile Organic Compounds in Plant Health
Bitas, V., Kim, H.-S., Bennett, J. W., & Kang, S. (2013) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-10-12-0249-cr · Cited by 351 · see citing works
Mumm, R., & Dicke, M. (2010) · Canadian Journal of Zoology · doi:10.1139/z10-032 · Cited by 324 · see citing works
Maksimov, I. V., Абизгильдина, Р. Р., & Пусенкова, Л. И. (2011) · Applied Biochemistry and Microbiology · doi:10.1134/s0003683811040090 · Cited by 322 · see citing works
Volatile organic compounds emitted by Trichoderma species mediate plant growth
Lee, S., Yap, M., Behringer, G., Hung, R., & Bennett, J. W. (2016) · Fungal Biology and Biotechnology · doi:10.1186/s40694-016-0025-7 · Cited by 316 · see citing works
Tran, H. T. T., Ficke, A., Asiimwe, T., Höfte, M., & Raaijmakers, J. M. (2007) · New Phytologist · doi:10.1111/j.1469-8137.2007.02138.x · Cited by 312 · see citing works
Small molecules below‐ground: the role of specialized metabolites in the rhizosphere
Massalha, H., Korenblum, E., Tholl, D., & Aharoni, A. (2017) · The Plant Journal · doi:10.1111/tpj.13543 · Cited by 310 · see citing works
Lee, B., Farag, M. A., Park, H. B., Kloepper, J. W., Lee, S.-H., & Ryu, C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048744 · Cited by 300 · see citing works
Self-citationKaushal, M., & Wani, S. P. (2016) · Agriculture Ecosystems & Environment · doi:10.1016/j.agee.2016.06.031 · Cited by 297 · see citing works
van de Mortel, J. E., de Vos, R. C. H., Dekkers, E., Pineda, A., Guillod, L., Bouwmeester, K., van Loon, J. J. A., Dicke, M., & Raaijmakers, J. M. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.207324 · Cited by 290 · see citing works
Rhizobacterial Volatiles Affect the Growth of Fungi and Arabidopsis thaliana
Vespermann, A., Kai, M., & Piechulla, B. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01078-07 · Cited by 290 · see citing works
Farag, M. A., Zhang, H., & Ryu, C. (2013) · Journal of Chemical Ecology · doi:10.1007/s10886-013-0317-9 · Cited by 287 · see citing works
Self-citationHa-Tran, D. M., Nguyen, T. T. M., Hung, S.-H. W., Huang, E. Y., & Huang, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22063154 · Cited by 284 · see citing works
Use of Plant-Associated Bacillus Strains as Biofertilizers and Biocontrol Agents in Agriculture
Borriss, R. (2011) · Springer eBooks · doi:10.1007/978-3-642-20332-9_3 · Cited by 284 · see citing works
Belowground volatiles facilitate interactions between plant roots and soil organisms
Wenke, K., Kai, M., & Piechulla, B. (2009) · Planta · doi:10.1007/s00425-009-1076-2 · Cited by 281 · see citing works
Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens
Saraf, M. S., Pandya, U., & Thakkar, A. (2013) · Microbiological Research · doi:10.1016/j.micres.2013.08.009 · Cited by 279 · see citing works
Pathogen Biocontrol Using Plant Growth-Promoting Bacteria (PGPR): Role of Bacterial Diversity
Wang, H., Liu, R., You, M. P., Barbetti, M. J., & Chen, Y. (2021) · Microorganisms · doi:10.3390/microorganisms9091988 · Cited by 275 · see citing works
Aloo, B. N., Makumba, B. A., & Mbega, E. R. (2018) · Microbiological Research · doi:10.1016/j.micres.2018.10.011 · Cited by 272 · see citing works
Chapter 6 Rhizobacteria-Induced Systemic Resistance
Vleesschauwer, D. D., & Höfte, M. (2009) · Advances in botanical research · doi:10.1016/s0065-2296(09)51006-3 · Cited by 271 · see citing works
Kishimoto, K., Matsui, K., Ozawa, R., & Takabayashi, J. (2005) · Plant and Cell Physiology · doi:10.1093/pcp/pci122 · Cited by 270 · see citing works
Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields
Bahaji, A., Li, J., Sánchez‐López, Á. M., Baroja‐Fernández, E., Muñoz, F. J., Ovečka, M., Almagro, G., Montero, M., Ezquer, I., Etxeberria, E., et al. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.06.006 · Cited by 269 · see citing works
D’Alessandro, M., Erb, M., Ton, J., Brandenburg, A., Karlen, D., Zopfi, J., & Turlings, T. C. J. (2013) · Plant Cell & Environment · doi:10.1111/pce.12220 · Cited by 264 · see citing works
- Authors
- Ryu, C.-M., Farag, M. A., Hu, C.-H., Reddy, M. S., Kloepper, J. W., & Paré, P. W.
- Affiliations
- Texas Tech University (US)
- Department of Entomology and Plant Pathology, Auburn University, 209 Life Sciences Building, Auburn, Alabama 36849 (C.-M.R., C.-H.H., M.S.R., J.W.K.); and Department of Chemistry and Biochemistry, Texas Tech University, 1 Chemistry Drive; Lubbock, Texas 79409 (M.A.F., P.W.P.)
- Venue
- PLANT PHYSIOLOGY
- Publisher
- Oxford University Press (OUP)
- Published
- 2004-03-01
- Volume
- 134
- Issue
- 3
- Pages
- 1017-1026
- ISSN
- 0032-0889 (ISSN-L)
- 1532-2548
- PMC
- PMC389924
- OpenAlex
- W2123767496
- Cited by
- 1,308
- References
- 51
- Citations by year
- 2026: 50 · 2025: 59 · 2024: 64 · 2023: 75 · 2022: 96 · 2021: 96 · 2020: 102 · 2019: 80 · 2018: 78 · 2017: 84 · 2016: 77 · 2015: 68 · 2014: 64 · 2013: 55 · 2012: 47
- FWCI
- 25.28
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- PLANT PHYSIOLOGY (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Agriculture
- Welch Foundation
- Ohio State University
- Herman Frasch Foundation for Chemical Research
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Pathogenic Bacteria Studies
- Keywords
- bacterial volatiles, induced systemic resistance, plant growth-promoting rhizobacteria, Bacillus subtilis, Bacillus amyloliquefaciens, Erwinia carotovora subsp. carotovora, 2,3-butanediol, acetoin, ethylene signaling, plant defense response, Arabidopsis thaliana, low molecular weight hydrocarbons
- MeSH terms
- Butylene Glycols, Mutation, Plant Diseases, Rhizobiaceae, Symbiosis, Volatilization, Signal Transduction, Arabidopsis, Plants, Genetically Modified
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
