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Cyanide degradation and antagonistic potential of endophytic Bacillus subtilis strain BEB1 from Bougainvillea spectabilis Willd Cyanide degradation and antagonistic potential of endophytic Bacillus subtilis strain BEB1 from...
Al-Badri, Basma Ali Salim; Al-Maawali, Samiya Saleh; Al-Balushi, Zainab Mohammed; Al-Mahmooli, Issa Hashil; Al-Sadi, Abdullah Mohammed; Velazhahan, Rethinasamy
2020-01-01 00:00:00
ALL LIFE 2020, VOL. 13, NO. 1, 92–98 https://doi.org/10.1080/26895293.2020.1728393 Cyanide degradation and antagonistic potential of endophytic Bacillus subtilis strain BEB1 from Bougainvillea spectabilis Willd Basma Ali Salim Al-Badri, Samiya Saleh Al-Maawali, Zainab Mohammed Al-Balushi, Issa Hashil Al-Mahmooli, Abdullah Mohammed Al-Sadi and Rethinasamy Velazhahan Department of Crop Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, Al-Khoud, Sultanate of Oman ABSTRACT ARTICLE HISTORY Received 8 January 2020 Bacterial endophytes were isolated from the leaves of Bougainvillea spectabilis Willd. and screened Accepted 6 February 2020 for their in vitro antagonistic activity against three important phytopathogenic fungi viz., Neocos- mospora keratoplastica, Stemphylium vesicarium and Rhizoctonia solani. Among the 36 endophytic KEYWORDS bacterial isolates screened, three isolates designated as BEB1, BEB5 and BEB6 inhibited the mycelial Cyanogenic plants; growth of all the three plant pathogenic fungi tested and recorded more than 10% growth inhibition. detoxification; endophytic Scanning electron microscopic observations of hyphae of the pathogenic fungi at the periphery of bacteria; Nyctaginaceae; the inhibition zone in the dual culture plate revealed morphological abnormalities such as shrinkage, Phytoanticipins pit formation and loss of turgidity. These isolates were identified as Bacillus subtilis (BEB1) and Bacillus cereus (BEB5 and BEB6) based on the MALDI Biotyper analysis. The Bacillus subtilis strain BEB1, which exhibited the highest level of antagonism, was tested for its sensitivity to cyanide and potential to degrade NaCN. The results revealed that this strain was capable of growing in a medium containing 5 mM of NaCN with a degradation efficiency of 53.8%. This endophyte is valuable for exploitation as a biocontrol agent to control diseases especially in the cyanogenic plants and bioremediation of cyanide from the industrial effluent. Introduction Moller 2014). The presence of HCN in the leaves of Bougainvillea spectabilis Willd. (Nyctaginaceae) has Preformed antimicrobial compounds, also known as been reported (Chillawar 2017). Despite the toxicity of ‘Phytoanticipins’, are present in a diverse group of cyanogenic glycosides, many pathogens establish com- plants (VanEtten et al. 1994;Pedrasand Yaya 2015; patible relationship with these cyanogenic plants and Oros and Kallai 2019). These compounds include cause diseases. It is well established that endophytic cyanogenic glycosides, saponins, glucosinolates and bacteria are commonly associated with higher plants phenolics (Osbourn 1996). Phytoanticipins play an (Liu et al. 2017) and these microorganisms may have important role in the resistance of plants against pests potential to overcome the toxic effects of HCN. The and pathogens (Gleadow and Moller 2014;Piasecka aims of this research were to i) isolate and character- et al. 2015). The cyanogenic glycosides are a group ize endophytic bacteria from B. spectabilis, ii) evalu- of amino acid- derived secondary metabolites that are ate their antagonistic activity against plant pathogenic present in the form of inactive precursors in plants fungi and iii) to test their sensitivity to cyanide. and in response to pathogen infection or tissue damage these are activated to form hydrocyanic acid (HCN) Materials and methods by the hydrolytic enzymes of plants (Poulton 1990; Gleadow and Moller 2014). Over 2000 plant species Plant material such as cassava, sorghum, flax, rubber, lima bean, Healthy leaves of Bougainvillea spectabilis Willd. were cocoyam, apple, apricot and white clover have been collected from the Botanic garden, Sultan Qaboos Uni- reported to contain cyanoglycosides (Poulton 1990; versity, Muscat, Sultanate of Oman. Francisco and Pinotti 2000;Vetter 2000;Gleadow and CONTACT Rethinasamy Velazhahan velazhahan@squ.edu.om Department of Crop Sciences, College of Agricultural and Marine Sciences, Sultan Qaboos University, P.O. Box 34, Al-Khoud, Muscat 123, Sultanate of Oman © 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. ALL LIFE 93 Fungal cultures Scanning electron microscopy Three phytopathogenic fungal species viz., Neocosmo- To study the morphological changes in the hyphae spora keratoplastica (D. Geiser, O’Donnell, Short & of phytopathogenic fungi at the inhibition zone in Ning Zhang) Sand.-Den. & Crous (ID 2114), Stem- dual culture plates, 0.5 cm pieces of agar medium phylium vesicarium (Wallr.) E.G. Simmons (ID 2392) containing mycelium were taken from the periphery and Rhizoctonia solani Kuhn (ID 2004) obtained from and samples for the scanning electron microscopy the Department of Crop Sciences, College of Agricul- were prepared as described by Goldstein et al. tural and Marine Sciences, Sultan Qaboos University (2003). The prepared samples were then exam- were used for the antifungal testing. ined with a JEOL JSM-7800F scanning electron microscope. Bacterial endophyte isolation Identification of endophytic bacteria Toisolateendophyticbacteria, theleaveswererinsed with distilled water and dried on sterile filter papers. The bacterial isolates showing antagonistic activity The leaves were cut into small segments (0.5 cm) and were identified using a MALDI Biotyper (Bruker surface sterilized with 1% NaOCl for 3 min, followed Daltronics, MA, USA) with Bruker inbuilt MALDI- by washing with sterile distilled water three times, Biotyper database by following the manufacturer’s each for 1 min. The surface-sterilized plant tissues (1 g) instructions. The score values < 1.7 were considered were ground in 1 ml of sterile distilled water by using unacceptable identification, scores between 1.70 and a sterilized mortar and pestle and 100 μl aliquots of 1.99 were considered low-confidence identification the extracts were plated on Nutrient agar (NA) (Oxoid and scores of ≥ 2.00 were considered high-confidence Ltd., Hampshire, UK) in Petri plates. The plates were identification. incubated at 28 °C for 2 days. The efficiency of the sur- face sterilization was verified by plating 100 μl aliquots Cyanide degradation potential of endophytic ofthesteriledistilledwaterusedinthe finalrinse bacteria onto NA plates. The bacterial colonies appearing on the plates were purified by streak-plate technique and To study the effect of cyanide on the growth of single colonies on the NA plates were selected and endophytic bacteria, B. subtilis strain BEB1, which transferred to fresh NA medium. exhibited the highest level of antagonism, was grown in Nutrient broth containing different concentrations Antagonistic potential of bacterial endophytes of NaCN (1, 5, 10, 15, 20 and 25 mM) for 72 h with shaking at 28°C. The absorbance of the cul- The endophytic bacterial isolates were evaluated for tures was measured at 660 nm using a spectropho- their inhibitory eeff cts on phytopathogeic fungi using tometer. The residual cyanide in the nutrient broth a dual culture technique (Al-Hussini et al. 2019). was determined as described by Kandasamy et al. Briefly, a 7-mm diameter mycelial plug of the test fungi (2015) and the cyanide degradation efficiency (CDE) taken from an actively growing culture was placed on of the bacteria was calculated by using the formula: one side of the Petri dish (9-mm diameter) contain- CDE (%) = IC-RC/IC × 100; where, IC = initial con- ing PDA medium. The antagonist was streaked on centration of cyanide in the growth medium and theoppositesideabout1cmawayfromtheedge of RC = residual concentration of cyanide in the growth the Petri plate and perpendicular to the fungal disc. medium. Three replications were maintained for each bacte- rial isolate. Petri dishes inoculated with fungal discs alone served as control. The plates were incubated at Statistical analysis room temperature (25 ± 2°C) for 3–5 days or until the mycelial growth in the control completely cov- The data were subjected to analysis of variance using ered thePetri plate. Afterincubation,theradialgrowth Minitab 17 (State College, PA, USA) and the treatment of the pathogens was recorded and percent growth means were compared by least significant difference inhibition was calculated (Shifa et al. 2015). test (P ≤ 0.05). 94 B. A. S. AL-BADRI ET AL. Table 1. In vitro antagonistic activity of endophytic bacteria isolated from Bougainvillea spectabilis. Inhibition % Bacterial isolate Neocosmospora keratoplastica Rhizoctonia solani Stemphylium vesicarium BEB1 51.0 a 24.6 a 56.3 a BEB2 17.8 b 8.7 a 18.2 b BEB3 25.0 ab 12.7 a 9.1 b BEB5 39.2 ab 12.7 a 13.6 b BEB6 28.6 ab 16.6 a 13.6 b Data are mean of 3 replications. Means with different letters are significantly (P ≤ 0.05) different. Results and discussion A total of 36 morphologically distinct endophytic bac- terial isolates were obtained from the surface-sterilized leaf tissues of B. spectabilis. No bacterial colonies were observed from the distilled water collected from the last wash during surface sterilization procedure. Of the 36 endophytic bacterial isolates, vfi e isolates desig- nated as BEB1, BEB2, BEB3, BEB5 and BEB6 inhibited the mycelial growth of N. keratoplastica, S. vesicarium and R. solani in vitro (Table 1). Among them, BEB1, BEB5 and BEB6 recorded more than 10% growth inhi- bition of all the three plant pathogenic fungi tested. The isolate BEB1 exhibited the highest antagonistic activity against all the three plant pathogenic fungi. The in vitro antagonistic activity of BEB1 against N. keratoplastica, R. solani and S. vesicarium is shown in Figure 1. The inhibition zone formation might be duetothe releaseofvariousdiffusibleextracellular antifungal metabolites by these endophytes (Leifert et al. 1995; Fira et al. 2018). The varying degree of antagonism of the endophytic bacterial isolates against plant pathogenic fungi in the dual culture assay in the presentstudymightbedue tothetypeand levelof production of antifungal metabolites by these bacterial Figure 1. In vitro antagonistic activity of Bacillus subtilis BEB1 endophytes. against Neocosmospora keratoplastica, Rhizoctonia solani and Stemphylium vesicarium.A) N. keratoplastica alone, B) N. kerato- Based on the MALDI Biotyper analysis, the three plastica + B. subtilis BEB1, C) R. solani alone, D) R. solani + B. sub- bacterial isolates that showed more than 10% growth tilis BEB1, E) S. vesicarium alone, F) S. vesicarium + B. subtilis BEB1 inhibition of plant pathogenic fungi were identified as Bacillus subtilis (BEB1) and Bacillus cereus (BEB5 and BEB6). These bacterial isolates had score val- Sporothrix ofl cculosa caused complete plasmolysis of ues of > 2.0. Scanning electron microscopic obser- Sphaerotheca pannosa var. rosae,the rosepowdery vations of hyphae of the pathogens at the margin of mildew fungus. The shrinkage of the hyphae indicates the inhibition zone in the dual culture plate revealed a possible loss of cytoplasmic contents (Garg et al. morphological abnormalities such as hyphal shrink- 2010). The observed loss of turgidity of hyphae of age, pit formation and loss of turgor in comparison the pathogenic fungi in the inhibition zone suggests to the control hyphae (Figure 2). These results are in alterations in the permeability of the cell membrane agreement with the findings of Hajlaoui et al. ( 1992) (Halo et al. 2018). The hyphal malformations may be who reported that the yeast like antagonistic fungus ALL LIFE 95 Figure 2. Scanning electron micrographs showing morphological changes in the hyphae of Neocosmospora keratoplastica, Rhizoctonia solani and Stemphylium vesicarium due to antagonistic effect of Bacillus subtilis BEB1. A) N. keratoplastica alone, B) N. keratoplastica + B. subtilis BEB1, C) R. solani alone, D) R. solani + B. subtilis BEB1, E) S. vesicarium alone, F) S. vesicarium + B. subtilis BEB1. attributed to production of antibiotic substances by Luque-Almagro et al. 2016). The cyanide is converted Bacillus sp. (Kotze et al. 2011). into carbon dioxide and ammonia via an NADH- linked cyanide oxygenase system (Kunz et al. 1994; The B. subtilis strain BEB1, which exhibited the highest level of antagonism towards phytopathogenic Luque-Almagro et al. 2005). The fungi, which infect fungitested,wascapableofgrowinginamediumcon- cyanogenic plants, employ different mechanisms to taining NaCN (Figure 3). The B. subtilis strain BEB1 tolerate HCN. For example, the ascomycete fungus caused 53.8 and 29.4% degradation of cyanide when Microcyclus ulei (P. Henn.) v. Arx, which infects rubber grown in a medium containing NaCN at concentra- tree, employs cyanide-resistant respiration to tolerate tions of 5 and 10 mM, respectively (Figure 4). The uti- HCN (Lieberei, 1988). Many fungal pathogens infect- lization of cyanide as a nitrogen source by a few species ing cyanogenic plants are known to produce cyanide- of Pseudomonas for their growth has been reported detoxifying enzyme namely cyanide hydratase, which (Harris and Knowles 1983;Rollinsonet al. 1987; converts HCNintoformamide (Fry andMillar 1972; 96 B. A. S. AL-BADRI ET AL. 1991). A wide range of microorganisms is known to metabolize cyanides (Harris et al. 1987; Mirizadeh et al. 2014). Treatmentofindustrialeuffl entswith such biological agents may be an alternative and environmentally friendly method to degrade cyanide. Kandasamy et al. (2015) isolated cyanide tolerant strains of Bacillus pumilus, Bacillus cereus and Pseu- domonas putida from cassava factory wastewater and demonstrated that B. pumilus and P. putida could remove 63 and 61 per cent of cyanide at 5 mM. Razanamahandry et al. (2019) reported that the bacte- Figure 3. Growth of Bacillus subtilis BEB1 at different concentra- ria isolated from mining wastewater and thiocyanate tions of NaCN. The absorbance of the bacterial cultures was deter- containing wastewater showed biodegradation of free mined 72 h after inoculation. Values followed by different letters cyanide. are significantly different according to LSD test (P < 0.05). Bacillus spp. are extensively used as plant growth- promoting bacteria because of their ability to suppress plant pathogens and augment plant health (Jayaraj et al. 2005;Huetal. 2014). Bacillus species are known to produce antibiotics such as mycobacillins, iturins, bacillomycins, surfactins, mycosubtilins, fungistatins, subsporins and fengycins (Fira et al. 2018). The Food and Drug Administration (FDA) of the United States has approved the ‘generally regarded as safe’ (GRAS) status to B. subtilis (Harwood and Wipat 1996). Hence, the endophyte B. subtilis BEB1, which showed high levels of antagonistic activity against plant pathogenic fungi and cyanide detoxification potential is valu- Figure 4. Degradation of NaCN by Bacillus subtilis BEB1. The able for exploitation as a biocontrol agent to con- cyanide content in the growth medium was determined 72 h after trol diseases especially in the cyanogenic plants and inoculation. Values followed by different letters are significantly different according to LSD test (P < 0.05). bioremediation of cyanide from the industrial waste effluents. Fry and Evans 1977;Wangetal. 1992). The produc- tion of cyanide hydratase by Gloeocercospora sorghi Acknowledgements Bain & Edgerton ex Deighton, the sorghum pathogen The authors thank the Central Analytical and Applied Research (Wang et al. 1992)and Fusarium lateritium Nees, the Unit (CAARU) and the College of Medicine, Sultan Qaboos sweet potato pathogen (Cluness et al. 1993)hasbeen University for MALDI-Biotyper analysis and Scanning Elec- reported. The tolerance of B. subtilis strain BEB1 to tron Microscope imaging, respectively. cyanideinthisstudymaybedueto theproductionof enzymes that metabolize cyanide as well as due to its potential to form endospores (Earl et al. 2008). Disclosure statement Euffl entsfromindustriesinvolvedinmetalplating, The authors declare that they have no conflict of interest. coal coking, coal gasification, ore leaching, aluminum electrolysis, manufacturing of pharmaceuticals, plas- tics and synthetic fibers contain large amounts of cyanides (Dumestre et al. 1997). To minimize health Authors’ contributions and environmental risks, the cyanide content in these RV, AMA designed the study, BASA, SSA, ZMA, IHA con- effluents has to be reduced to very low levels (0.1 mg of ducted lab experiments, RV, AMA supervised the research CN per liter) before discharging (Smith and Mudder project, BASA, RV, AMA wrote the manuscript. ALL LIFE 97 Funding GoldsteinJ,Newbury DE,JoyDC,Lyman CE,EchlinP,Lifshin E, Sawyer L, Michael JR. 2003. Scanning electron microscopy This research was supported by the Sultan Qaboos Uni- and X-Ray Microanalysis, 3rd Edition. US: Springer. p. 689. versity research grants IG/AGR/CROP/18/01 and CR/AGR/ Hajlaoui MR, Benhamou N, Belanger NR. 1992.Cytochemi- CROP/19/01. cal study of the antagonistic activity of Sporothrix ofl cculosa on rose powdery mildew, Sphaerotheca pannosa var. rosae. Phytopathology. 82:583–589. Compliance with ethical standards Halo BA, Al-Yahyai RA, Al-Sadi AM. 2018. Aspergillus terreus Ethical approval inhibits growth and induces morphological abnormalities in Pythium aphanidermatum and suppresses Pythium- This article is original and not published elsewhere. All authors induced damping-off of cucumber. Front Microbiol. discussed the results, read and approved the final manuscript. 9:95. The authors confirm that there are no ethical issues in publica- Harris RE, Bunch AW, Knowles CJ. 1987. Microbial cyanide tion of the manuscript. and nitrile metabolism. Sci Prog. 71:293–304. Harris RE, Knowles CJ. 1983.Isolation andgrowthofa Pseu- ORCID domonas species that utilizes cyanide as a source of nitrogen. J Gen Microbiol. 129:1005–1011. Rethinasamy Velazhahan http://orcid.org/0000-0002-9263- Harwood CR, Wipat A. 1996. Sequencing and functional anal- ysis of the genome of Bacillus subtilis strain 168. FEBS Lett. 389:84–87. References Hu X,RobertsDP,XieL,MaulJE, YuC, LiY, JiangM,Liao Al-Hussini HS, Al-Rawahi AY, Al-Marhoon AA, Al-Abri SA, X, Che Z, Liao X. 2014. Formulation of Bacillus subtilis Al-Mahmooli IH, Al- Sadi AM, Velazhahan R. 2019.Bio- BY-2 suppresses Sclerotinia sclerotiorum on oilseed rape in logical control of damping-off of tomato caused by Pythium the field. Biol Control. 70:54–64. aphanidermatum by using native antagonistic rhizobacteria Jayaraj J, Radhakrishnan NV, Kannan R, Sakthivel K, Sug- isolated from Omani soil. J Plant Pathol. 101:315–322. anya D, Venkatesan S, Velazhahan R. 2005.Development Chillawar R. 2017. Quantitative estimation of hydrocyanic acid of new formulations of Bacillus subtilis for management of (HCN) in some cyanogenic plants with the help of microbial tomato damping-off caused by Pythium aphanidermatum. glycosidase enzyme. Int J Appl Res. 3:265–266. Biocontrol Sci Technol. 15:55–65. Cluness MJ, Turner PD, Clements E, Brown DT, O’Reilly C. Kandasamy S, Dananjeyan B, Krishnamurthy K, Benckiser 1993. Purification and properties of cyanide hydratase from G. 2015. Aerobic cyanide degradation by bacterial iso- Fusarium lateritium and analysis of the corresponding chy1 lates from cassava factory wastewater. Braz J Microbiol. 46: gene. J Gen Microbiol. 139:1807–1815. 659–666. Dumestre A, Chone T, Portal JM, Gerard M, Berthelin J. 1997. KotzeC,Van NiekerkJ,MostertL,HalleenF,FourieP. Cyanide degradation under alkaline conditions by a strain 2011. Evaluation of biocontrol agents for grapevine pruning of Fusarium solani isolated from contaminated soils. Appl woundprotectionagainsttrunkpathogeninfection.Phy- Environ Microbiol. 63:2729–2734. topathol Mediterr. 50:S247–S263. EarlAM,LosickR,KolterR. 2008.Ecologyandgenomicsof Kunz DA, Wang CS, Chan JL. 1994.Alternative routesof Bacillus subtilis. Trends Microbiol. 16:269–275. enzymic cyanide metabolism in Pseudomonas uo fl rescens Fira D, Dimkic I, Beric T, Lozo J, Stankovic S. 2018.Biological NCIMB 11764. Microbiology. 140:1705–1712. control of plant pathogens by Bacillus species. J Biotechnol. LeifertC,LiH,Chidburee S,HampsonS,WorkmanS,SigeeD, 285:44–55. Epton HA, Harbour A. 1995. Antibiotic production and bio- Francisco IA, Pinotti MHP. 2000. Cyanogenic glycosides in control activity by Bacillus subtilis CL27 and Bacillus pumilus plants. Braz Arch Biol Technol. 43:487–492. CL45. J Appl Bacteriol. 78:97–108. Fry WE, Evans PH. 1977. Association of formamide hydro- Lieberei R. 1988.Relationshipofcyanogeniccapacityofthe lyase with fungal pathogenicity to cyanogenic plants. Phy- rubber tree Hevea brasiliensis to susceptibility to Microcy- topathology. 77:1001–1006. clus ulei, the agent causing South American leaf blight. J Fry WE, Millar RL. 1972. Cyanide degradation by an Phytopathol. 122:54–67. enzyme from Stemphylium loti.ArchBiochem Biophys. Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, 151:468–474. Pieterse CMJ, Schenk PM. 2017.Innerplantvalues:diversity, Garg H, Li H, Sivasithamparam K, Kuo J, Barbetti MJ. 2010.The colonization and benefits from endophytic bacteria. Front infection processes of Sclerotinia sclerotiorum in cotyledon Microbiol. 8:2552. tissue of a resistant and a susceptible genotype of Brassica Luque-Almagro VM, Huertas MJ, Martinez-Luque M, napus. Ann Bot. 106:897–908. Moreno-Vivian C, Roldan MD, Garcia-Gil LJ, Castillo F, Gleadow RM, Moller BL. 2014. Cyanogenic glycosides: synthe- Blasco R. 2005. Bacterial degradation of cyanide and its sis, physiology, and phenotypic plasticity. Annu Rev Plant metal complexes under alkaline conditions. Appl Environ Biol. 65:155–185. Microbiol. 71:940–947. 98 B. A. S. AL-BADRI ET AL. Luque-AlmagroVM,Moreno-VivianC,RoldanMD. 2016. Maaza M, Ntwampe SKO. 2019. Performance of various Biodegradation of cyanide wastes from mining and jewellery cyanide degrading bacteria on the biodegradation of free industries. Curr Opin Biotechnol. 38:9–13. cyanide in water. J Hazard Mater. 380:120900. MirizadehS,YaghmaeiS,NejadZG. 2014. Biodegradation of Rollinson G, Jones R, Meadows MP, Harris RE, Knowles CJ. cyanide by a new isolated strain under alkaline conditions 1987. The growth of a cyanide-utilizing strain of Pseu- and optimization by response surface methodology (RSM). domonas uo fl rescens in liquid culture on nickel cyanide J Env Health Sci Eng. 12:85. as asourceofnitrogen. FEMS MicrobiolLett. 40: Oros G, Kallai Z. 2019. Phytoanticipins: The Constitutive 199–205. Defense compounds as potential Botanical Fungicides. In: Shifa H, Gopalakrishnan C, Velazhahan R. 2015.Ecffi acyof JogaiahS,AbdelrahmanM, editors. Bioactivemoleculesin Bacillus subtilis G1 in suppression of stem rot caused by plant defense. Cham: Springer; p. 179–229. Sclerotium rolfsii and growth promotion of groundnut. Int Osbourn AE. 1996. Preformed antimicrobial compounds and J Agric Environ Biotechnol. 8:91–98. plant defense against fungal attack. Plant Cell. 8:1821–1831. SmithA,MudderTI. 1991. The chemistry and treatment of Pedras MSC, Yaya EE. 2015. Plant chemical defenses: are all cyanidation wastes. London, United Kingdom: Mining Jour- constitutive antimicrobial metabolites phytoanticipins? Nat nal Books Ltd. Prod Commun. 10:209–218. VanEtten HD, Mansfield JW, Bailey JA, Farmer EE. 1994.Two Piasecka A, Jedrzejczak-Rey N, Bednarek P. 2015.Secondary classes of plant antibiotics: Phytoalexins versus “phytoan- metabolites in plant innate immunity: conserved function of ticipins.”. Plant Cell. 6:1191–1192. divergent chemicals. New Phytol. 206:948–964. Vetter J. 2000. Plant cyanogenic glycosides. Toxicon. 38:11–36. Poulton JE. 1990. Cyanogenesis in plants. Plant Physiol. Wang P, Matthews DE, VanEtten HD. 1992.Purification and characterization of cyanide hydratase from the phy- 94:401–405. Razanamahandry LC, Onwordi CT, Saban W, Bashir AKH, topathogenic fungus Gloeocercospora sorghi.ArchBiochem Mekuto L, Malenga E, Manikandan E, Fosso-Kankeu E, Biophys. 298:569–575.
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