The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Furthermore, we have proved that LJ02-induced long-range resistance is an appropriate indicator to examine the biocontrol ability, especially the SAR-inducing activity, of different BCAs using solid rhizosphere medium. Front. doi: 10.1016/0003-2697(77)90262-7, Faheem, M., Raza, W., Zhong, W., Nan, Z., Shen, Q. R., and Xu, Y. C. (2015). The number of CFU was recorded on each plate after 3 days. Briefly, 20 L of the LJ02FB was dropped onto the leaves including cotyledon under sterile condition at trefoil stage. The main function of SOD is eliminating the cellular superoxide radical (O2), and the increase of SOD activity can lead to the accumulation of H2O2. Plant Physiol. It was reported that purified surfactin, mycosubtilin, and plipastatin could be perceived by grapevine plant cells to stimulate grapevine innate immune responses including SA-mediated pathways (Farace et al., 2015). vesicatoria, but also elevated resistance against the soil bacterium, Ralstonia solanacearum. HPLC chromatogram of SA standard (A) and sample (B), temporal changes of free SA (C) and conjugated SA (D) in cucumber leaves of control and treatment group. One strain was selected and named LJ02. Each treatment was repeated three times and cultured at 28C for 9 days. doi: 10.1128/Iai.74.1.239-247.2006. A., et al. We extracted the free SA and the sugar-conjugated SA from LJ02FB-treated plant leaves and monitored the trend of SA accumulation in the cucumber leaves in time-course experiments.
Another interesting finding in our study is that the SA signaling pathways induced by beneficial bacterium such as LJ02 is likely to function from leaves (aboveground, AG) to roots (belowground, BG; Figure 7B). doi: 10.1146/annurev.arplant.57.032905.105346, Chen, X. H., Koumoutsi, A., Scholz, R., Schneider, K., Vater, J., Sussmuth, R., et al. Plant Physiol. LJ02 produces acid from xylose, sorbitol, L-arabinose, starch, inositol, sucrose, glucose, galactose, ribose, glycogen, and glycerol. Time course of changes in SOD activity (A), PPO activity (B), POD activity (C), and PAL activity (D) in cucumber leaves of control and treatment group. (2003). Besides, the long-range elicitation of SA induction in roots may be involved in aforementioned long-range resistance. Food Chem. 8, 63. doi: 10.1186/1475-2859-8-63, Bargabus, R. L., Zidack, N. K., Sherwood, J. E., and Jacobsen, B. J. Gram staining and microscopic observation showed that LJ02 is Gram-positive, endospore-forming and rod-shaped bacterium with a width of 0.70.9 m and a length of 1.83.0 m, indicative of a typical bacillus morphology (Figure 2). 53, 763775. Biocontrol. Generally, it was believed that beneficial bacteria can make the plant more tolerant to pathogens by stimulating ISR, which was shown to protect above-ground plant tissues and acts through roots to leaves (Van der Ent et al., 2009). Annu. Lebeis, S. L., Paredes, S. H., Lundberg, D. S., Breakfield, N., Gehring, J., Mcdonald, M., et al. Plant Sci. This further promoted us to note that LJ02 could induce a long-range defense response from leaves to roots in unknown mechanisms. except 16S rRNA gene sequence (Yamamoto and Harayama, 1995). Acetyl salicylic acid alleviates chilling-induced damage in muskmelon seedlings. Subsequently, we found that when we separated the LJ02FB into LJ02BC and LJ02FS, LJ02BC played very important roles in inducing the production of free SA in both upper uninoculated leaves and in roots. Our work demonstrated that the content of free SA in cucumber leaves was kept at a relatively higher level after spraying the LJ02FB. We proved that induced rhizosphere secretions in solid MS medium by treating plant leaves with BCAs was an effective method to examine the anti-fungal and long-range resistance activities of potential BCAs. Sci. Previous experiments had the same results after they inoculated the pathogens on various plants (Verberne et al., 2000). 42, 185209. Can. (2009). The main mechanisms of BCAs include the production of antibiotics, competition, plant growth promotion, and the induction of SAR and ISR (Ramarathnam et al., 2011). Rev. doi: 10.1146/annurev.phyto.42.040803.140421, Esterbauer, H., Schwarzl, E., and Hayn, M. (1977). doi: 10.1016/j.biocontrol.2014.11.012, Farace, G., Fernandez, O., Jacquens, L., Coutte, F., Krier, F., Jacques, P., et al. Copyright 2015 Li, Gu, Li, Xu, Wei and Wang. Plant Sci. Bacteriol. Plant Signal. Also the SA accumulation triggered by MAMPs is a major component of the MAMP-triggered signaling mechanism (Tsuda et al., 2008). doi: 10.1111/j.1462-2920.2012.02860.x, Durrant, W. E., and Dong, X. This is possibly caused by the degradation of functional elicitors in LJ02FS. 
(2009). doi: 10.1016/j.plaphy.2011.03.018, Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Rev. doi: 10.1111/j.1365-3059.2007.01684.x, Song, W., Ma, X., Tan, H., and Zhou, J. A one-way ANOVA was performed (*P < 0.05; **P < 0.01). Therefore, we intended to identify the LJ02 based on its phylogeny, morphology, physiological, and biochemical properties. Biochem. Actually, it was reported that PAL and PPO are the main SAR-related enzymes in plants (Jung et al., 2011). Table 2. Altogether, the isolated BCA was referred to as B. amyloliquefaciens LJ02 based on its morphological, phylogenetic, physiological, and biochemical characterizations.
Moreover, we determined that TJ02FB-treated cucumber leaves secreted resistance-related substance into rhizosphere against a range of fungi pathogens, suggesting that LJ02 could elicit a long-range systemic resistance in cucumber against pathogens. doi: 10.1016/j.foodchem.2014.07.087, Zipfel, C. (2014). Immun. Controlling powdery mildew caused by Sphaerotheca fuliginea in cucumber by foliar sprays of phosphate and potassium salts. Figure 1. Bergeys Manual of Systematic Bacteriology. Plant Microbe Interact. It was reported that foliar attack by the whitefly not only elicited AG resistance against a leaf pathogen, Xanthomonas axonopodis pv.
Phytopathol. Infect. Plant Pathol. Besides, the examination of rhizosphere secretions in solid MS medium was proved to be an effective method that identifies potential BCAs with resistance-induction and anti-fungal activities. At the first beginning, the identification of LJ02 as B. amyloliquefaciens is different from previous studies since we could not distinguish it from B. subtilis based on 16S rRNA comparison (data not shown).
doi: 10.1094/Mpmi-7-0356, Park, S. W., Kaimoyo, E., Kumar, D., Mosher, S., and Klessig, D. F. (2007). (2010). Thus, we come to the conclusion that functional SA production was enhanced in cucumber leaves to stimulate SA-mediated defense response, such as the expression of resistance-related enzymes. Figure 4. It is also positive for catalase, nitrate reduction, and VogesProskauer test and negative for oxidase, indole production and egg yolk reaction. Plant Sci. Evaluation of the biocontrol potential of Streptomyces goshikiensis YCXU against Fusarium oxysporum f. sp niveum. doi: 10.1146/annurev-phyto-073009-114447, Romero, D., De Vicente, A., Zeriouh, H., Cazorla, F. M., Fernandez-Ortuno, D., Tores, J. 28, 27312739. Plant Physiol. doi: 10.1016/j.it.2014.05.004, Keywords: powdery mildew, biocontrol agent, Bacillus amyloliquefaciens, salicylic acid, PR genes, systemic acquired resistance, Citation: Li Y, Gu Y, Li J, Xu M, Wei Q and Wang Y (2015) Biocontrol agent Bacillus amyloliquefaciens LJ02 induces systemic resistance against cucurbits powdery mildew. Ecotoxicol. To be specific, when treated with LJ02FB, cucumber seedlings produced significantly high amount of SOD, POD, PPO, and PAL. Residues and dissipation kinetics of triazole fungicides difenoconazole and propiconazole in wheat and soil in Chinese fields. 115, 14051412. Identification of a new spore wall protein from Encephalitozoon cuniculi. Spatial and temporal detection of SA with separated LJ02FB components (LJ02BC and LJ02FS). 57, 18461850. Bacillus amyloliquefaciens sp nov, nom rev. Moreover, the quantity of rhizosphere fungi was determined after treated with LJ02FB in cucumber leaves. Ahmad, R., Kim, Y. H., Kim, M. D., Kwon, S. Y., Cho, K., Lee, H. S., et al. Glasshouse experiments on biocontrol of cucumber powdery mildew (Sphaerotheca fuliginea) by the Mycoparasites verticillium lecanii and Sporothrix rugulosa. 168, 396403. Different letters are significantly difference at P < 0.01 according to Duncan multiple range test. Plant Microbe Interact. doi: 10.1099/00207713-37-1-69, Ramarathnam, R., Fernando, W. G. D., and De Kievit, T. (2011). Microbiol. Physiological and biochemical characteristics of strain LJ02. A revised medium for rapid growth and bioassays with tobacco tissue cultures. doi: 10.1016/0261-2194(95)00109-3, Robert-Seilaniantz, A., Grant, M., and Jones, J. D. (2011).
Relative expression of PR-1 gene in cucumber leaves after treated with LJ02FB (Treated) and PDB (Control). doi: 10.1007/BF03175560, Li, J., Yan, Q., Zhao, L. H., Zhang, S. M., Wang, Y. X., and Zhao, X. Y. To this end, we analyzed the level of transcription of PR-1 gene, a commonly used maker for SA-mediated expression (Tornero et al., 1997). It was also reported that enhanced resistance against phytopathogens by exogenous elicitor application is also associated with defense-related enzymes (Song et al., 2011). The cake made from sterile MS solid medium without root secretions was used as a control. As we know, only free SA is involved in the signal transduction in plant disease resistance (Park et al., 2007). Error bars indicate standard deviation among triplicates. doi: 10.1006/bcon.1996.0045, Vlot, A. C., Dempsey, D. A., and Klessig, D. F. (2009). 49, 317343. As can be seen from Figure 7A, the accumulation of free SA in upper uninoculated cucumber leaves increased rapidly after 3-day treatment as compared to control. Overexpression of polyphenol oxidase in transgenic tomato plants results in enhanced bacterial disease resistance. 35, 345351. Genetic distances were computed by Kimura 2-parameter model. A. Control 81, 101110. 87, 581585. 6, 11921194. doi: 10.1111/j.1399-3054.2010.01348.x, PubMed Abstract | CrossRef Full Text | Google Scholar, Alamri, S., Hashem, M., and Mostafa, Y. S. (2012). Therefore, we detected the diameter of inhibition zone against other pathogen fungi (F. oxysporum, B. cinerea, and Alternaria spp.) doi: 10.1007/s10526-004-0451-y, Jung, W. J., Mabood, F., Souleimanov, A., and Smith, D. L. (2011). The tree was constructed by MEGA5.1 by the neighbor-joining method. Crit. doi: 10.1016/j.phytochem.2009.06.009, Verberne, M. C., Verpoorte, R., Bol, J. F., Mercado-Blanco, J., and Linthorst, H. J. Error bars indicate standard deviation among triplicates. B. subtilis is known to produce cyclic lipopeptides such as surfactins, iturins and fengycins (Farace et al., 2015). doi: 10.1038/77347, Verhaar, M. A., Hijwegen, T., and Zadoks, J. C. (1996).
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