A CRITICAL REVIEW OF RESEARCH ON EXPLOITATION OF MICROBIAL ANTAGONISTS FOR THE CONTROL OF BACTERIAL DISEASES IN CROP PLANTS

Muhammad T. Malik, Ateeq U. Rehman, Syed A.H. Naqvi, Ammarah Hasnain, Ummad U.D. Umar, Hajra Azeem, Muhammad Shahid, Muhammad Umair

Abstract


Biological control is described as the suppression of one or more populations of plant pathogens using introduced or resident living species rather than disease-resistant host plants. This can be accomplished by the use of microbial biological control agents (MBCAs) where they biologically control plant pathogens interacting with their hosts via a range of modes of action. Overuse of pesticides has had a negative impact on the climate in recent decades that gave rise to human health issues. This posed a dire need to explore alternative strategies that are comparatively safe, environmental, and monetarily feasible. The employment of MBCAs is found to be a highly effective way to regulate several diseases of the exiting flora caused mainly by nematode infestation and bacterial or fungal pathogens. Microbial inoculants suppress a particular form of plant disease or regulate soils so that plant-associated species and native soil can work together to suppress the disease. Microbes, such as bacteria, protozoa, algae, and fungi, frequently interact with plants in several ways including protocooperation, mutualism, commensalism, rivalry, neutralism, amensalism, predation, and parasitism. These interactions are cascades of highly regulated metabolic events that combine various kinds of action. Compounds such as enzymes, signaling compounds, and other interfering metabolites are released in situ at low levels during the interaction. Pseudomonas, Erwinia, Bacillus, Agrobacterium, Rahnella, Lysobacter, Myxobacteria, Enterobacter, and Streptomyces are some of the bacterial genera that have major biocontrol potential to mitigate crop plant diseases. Several species, including P. fluorescens, P. putida, P. cepacia, P. aureofaciens, P. tolaasii, P. fluorescens (strains A1, BK1, TL3B1, A506, and B10), Erwinia herbicola, B. cereus (strain UW85), Agrobacterium radiobacter (strain K84), Rahnella aquatilis have been proved beneficial against various crop diseases. Likewise, Trichoderma harzianum, Glomus fasciculatum, G. macrocarpum, and Pisolithus tinctorius are known to induce plant defense response against phytotoxic effects caused by different pathogenic strains. This review highlights the role of MBCAs against pathogenic microorganisms and their mode of action in terms of the ability to enhance plant defense systems for their improved growth.

Keywords


Microbes, Bacteria, microbial diversity, Disease suppression, Biocontrol, Biological mediated management, Bacterial diseases

Full Text:

PDF

References


Akhurst, R. and G. Dunphy. 1993. Tripartite interactions between symbiotically associated entomopathogenic bacteria, nematodes, and their insect hosts. Pp. 1-23.

Akhurst, R. J. 1983. Taxonomic Study of Xenorhabdus, a Genus of Bacteria Symbiotically Associated with Insect Pathogenic Nematodes. International Journal of Systematic Bacteriology, 33: 38-45.

Anderson, A. J., P. H. Tari and C. S. Tepper. 1988. Molecular Studies on the Role of a Root Surface Agglutinin in Adherence and Colonization by Pseudomonas putida. Applied and Environmental Microbiology, 54: 375-380.

Arseneault, T. and M. Filion. 2017. Biocontrol through antibiosis: exploring the role played by subinhibitory concentrations of antibiotics in soil and their impact on plant pathogens. Canadian Journal of Plant Pathology, 39: 267-274.

Bardin, M., S. Ajouz, M. Comby, M. Lopez-Ferber, B. Graillot, M. Siegwart and P. C. Nicot. 2015. Is the efficacy of biological control against plant diseases likely to be more durable than that of chemical pesticides? Frontiers in Plant Science, 6: 566.

Baute, M. A., G. Deffieux, J. Vercauteren, R. Baute and A. Badoc. 1993. Enzymic activity degrading 1,4-α-d-glucans to ascopyrones P and T in Pezizales and Tuberales. Phytochemistry, 33: 41-45.

Baute, M. A., R. Baute and G. Deffieux. 1988. Fungal enzymic activity degrading 1,4-α-d-glucans to. 1,5-d-anhydrofructose. Phytochemistry, 27: 3401-3403.

Benhamou, N. and I. Chet. 1997. Cellular and Molecular Mechanisms Involved in the Interaction between Trichoderma harzianum and Pythium ultimum. Applied and environmental microbiology, 63: 2095-2099.

Biermann, B. and R. G. Linderman. 1983. Use of vesicular-arbuscular mycorrhizal roots, intraradical vesicles and extraradical vesicles as inoculum. New Phytologist, 95: 97-105.

Borges, R. C. F., M. Rossato, G. M. R. Albuquerque, M. A. Ferreira, A. C. M. Brasileiro, M. E. N. Fonseca and L. S. Boiteux. 2018. Crown gall caused by Agrobacterium tumefaciens species complex: a novel nursery disease of Tectona grandis in Brazil. Journal of Plant Pathology, 101: 445-445.

Borges, R. C., M. Rossato, G. M. R. Albuquerque, M. A. Ferreira, A. C. Brasileiro, M. E. N. Fonseca and L. S. Boiteux. 2019. Crown gall caused by Agrobacterium tumefaciens species complex: a novel nursery disease of Tectona grandis in Brazil. Journal of Plant Pathology, 101: 445-445.

Buddenhagen, I. 1962. Designations of races in Pseudomonas solanacearum. Phytopathology, 52: 726.

Buddenhagen, I. and A. Kelman. 1964. Biological and Physiological Aspects of Bacterial Wilt Caused by Pseudomonas Solanacearum. Annual Review of Phytopathology, 2: 203-230.

Catska, V. 1994. Interrelationships between vesicular-arbuscular mycorrhiza and rhizosphere microflora in apple replant disease. Biologia plantarum, 36: 99-104.

Chen, G., Y. Zhang, J. Li, G. B. Dunphy, Z. K. Punja and J. M. Webster. 1996. Chitinase Activity of Xenorhabdusand Photorhabdus Species, Bacterial Associates of Entomopathogenic Nematodes. Journal of Invertebrate Pathology, 68: 101-108.

Di Francesco, A., L. Ugolini, S. D. Aquino, E. Pagnotta and M. Mari. 2017. Biocontrol of Monilinia laxa by Aureobasidium pullulans strains: Insights on competition for nutrients and space. International Journal of Food Microbiology, 248: 32-38.

Duchesne, L. C. 1994. Role of ectomycorrhizal fungi in biocontrol. APS Press, St. Paul, Minnesota, USA.

Elad, Y. 1985. Influence of Trace Amounts of Cations and Siderophore-Producing Pseudomonads on Chlamydospore Germination of Fusarium oxysporum. Phytopathology, 75: 1047.

Elad, Y. 2000. Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. Crop Protection, 19: 709-714.

Eltom Eltayeb, F. M. 2017. Biological Control of Root Knot Disease of Tomato caused by Meloidogyne javanica using Pseudomonas fluorescens Bacteria. International Journal of Current Microbiology and Applied Sciences, 6: 1176-1182.

European Food Safety Authority. 2017. Peer review of the pesticide risk assessment of the active substance Mild Pepino mosaic virus.: (isolate)VX1. EFSA J. 15:4650.

Fischer, U., M. Kuhlmann, A. Pecinka, R. Schmidt and M. F. Mette. 2008. Local DNA features affect RNA-directed transcriptional gene silencing and DNA methylation. The Plant Journal, 53: 1-10.

Fitter, A. H. and J. Garbaye. 1994. Interactions between mycorrhizal fungi and other soil organisms. Plant and Soil, 159: 123-132.

Forst, S. and K. Nealson. 1996. Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiological reviews, 60: 21-43.

Garcia-Garrido, J. M. and J. A. Ocampo. 1989. Effect of VA mycorrhizal infection of tomato on damage caused by Pseudomonas syringae. Soil Biology and Biochemistry, 21: 165-167.

Ghorbanpour, M., M. Omidvari, P. Abbaszadeh-Dahaji, R. Omidvar and K. Kariman. 2018. Mechanisms underlying the protective effects of beneficial fungi against plant diseases. Biological Control, 117: 147-157.

Girlanda, M., S. Perotto, Y. Moenne-Loccoz, R. Bergero, A. Lazzari, G. Defago, P. Bonfante and A. M. Luppi. 2001. Impact of Biocontrol Pseudomonas fluorescens CHA0 and a Genetically Modified Derivative on the Diversity of Culturable Fungi in the Cucumber Rhizosphere. Applied and Environmental Microbiology, 67: 1851-1864.

Glare, T., J. Caradus, W. Gelernter, T. Jackson, N. Keyhani, J. Köhl, P. Marrone, L. Morin and A. Stewart. 2012. Have biopesticides come of age? Trends in Biotechnology, 30: 250-258.

Gohlke, J., C. J. Scholz, S. Kneitz, D. Weber, J. Fuchs, R. Hedrich and R. Deeken. 2013. DNA Methylation Mediated Control of Gene Expression Is Critical for Development of Crown Gall Tumors. PLoS Genetics, 9: e1003267.

Haas, D. and G. Défago. 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology, 3: 307-319.

He, P., S. Chintamanani, Z. Chen, L. Zhu, B. N. Kunkel, J. R. Alfano, X. Tang and J. M. Zhou. 2004. Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine. The Plant Journal, 37: 589-602.

Heimpel, G. E. and N. J. Mills. 2017. Biological control. Cambridge University Press.

Heitefuss, R. 2014. Vanky K. Illustrated Genera of Smut Fungi, 3rdedn. St. Paul, MN, USA, APS Press, 2013. 288 pp, 116 black and white illustrations, $ 139.00. Journal of Phytopathology, 162: 626-626.

Hernández-León, R., D. Rojas-Solís, M. Contreras-Pérez, M. d. C. Orozco-Mosqueda, L. I. Macías-Rodríguez, H. Reyes-de la Cruz, E. Valencia-Cantero and G. Santoyo. 2015. Characterization of the antifungal and plant growth-promoting effects of diffusible and volatile organic compounds produced by Pseudomonas fluorescens strains. Biological Control, 81: 83-92.

Hoffland, E. 1996. Comparison of Systemic Resistance Induced by Avirulent and Nonpathogenic Pseudomonas Species. Phytopathology, 86: 757.

Hoitink, H. A. J. and M. J. Boehm. 1999. Biocontrol with in the context of soil microbial communities: A Substrate-Dependent Phenomenon. Annual Review of Phytopathology, 37: 427-446.

Iavicoli, A., E. Boutet, A. Buchala and J. P. Métraux. 2003. Induced Systemic Resistance in Arabidopsis thaliana in Response to Root Inoculation with Pseudomonas fluorescens CHA0. Molecular Plant-Microbe Interactions, 16: 851-858.

Jeffries, P. 1995. Biology and ecology of mycoparasitism. Canadian Journal of Botany, 73: 1284-1290.

Karlsson, M., L. Atanasova, D. F. Jensen and S. Zeilinger. 2017. Necrotrophic Mycoparasites and Their Genomes. The Fungal Kingdom. ASM Press, pp. 1005-1026.

Keel, C. 1989. Iron Sufficiency, a Prerequisite for the Suppression of Tobacco Black Root Rot by Pseudomonas fluorescens Strain CHA0 under Gnotobiotic Conditions. Phytopathology, 79: 584.

Kiss, L. 2003. A review of fungal antagonists of powdery mildews and their potential as biocontrol agents. Pest Management Science, 59: 475-483.

Kloepper, J. W., J. Leong, M. Teintze and M. N. Schroth. 1980. Pseudomonas siderophores: A mechanism explaining disease-suppressive soils. Current Microbiology, 4: 317-320.

Köhl, J., R. Kolnaar and W. J. Ravensberg. 2019. Mode of Action of Microbial Biological Control Agents Against Plant Diseases: Relevance Beyond Efficacy. Frontiers in Plant Science, 10.

Larkin, R. P. and M. T. Brewer. 2020. Effects of Crop Rotation and Biocontrol Amendments on Rhizoctonia Disease of Potato and Soil Microbial Communities. Agriculture, 10: 128.

Lee, C. W., M. Efetova, J. C. Engelmann, R. Kramell, C. Wasternack, J. Ludwig-Müller, R. Hedrich and R. Deeken. 2009. Agrobacterium tumefaciens Promotes Tumor Induction by Modulating Pathogen Defense in Arabidopsis thaliana. The Plant Cell, 21: 2948-2962.

Li, J., G. Chen, J. M. Webster and E. Czyzewska. 1995. Antimicrobial Metabolites from a Bacterial Symbiont. Journal of Natural Products, 58: 1081-1086.

Linderman, R. 1994. Role of VAM fungi in biocontrol. Mycorrhizae and plant health.

Lindsay, W. L. 1979. Chemical equilibria in soils. John Wiley and Sons Ltd.

Loper, J. E. 1991. Current ReviewSiderophores in Microbial Interactions on Plant Surfaces. Molecular Plant-Microbe Interactions, 4: 5.

Lugtenberg, B. and F. Kamilova. 2009. Plant-Growth-Promoting Rhizobacteria. Annual Review of Microbiology, 63: 541-556.

Lugtenberg, B., D. E. Rozen and F. Kamilova. 2017. Wars between microbes on roots and fruits. F1000Research, 6: 343.

Lwin, M. and S. Ranamukhaarachchi. 2006. Development of biological control of Ralstonia solanacearum through antagonistic microbial populations. International Journal of Agriculture and Biology, 8: 657-660.

Magori, S. and V. Citovsky. 2012. The Role of the Ubiquitin-Proteasome System in Agrobacterium tumefaciens-Mediated Genetic Transformation of Plants. Plant Physiology, 160: 65-71.

Mauch-Mani, B., I. Baccelli, E. Luna and V. Flors. 2017. Defense Priming: An Adaptive Part of Induced Resistance. Annual Review of Plant Biology, 68: 485-512.

McInerney, B. V., R. P. Gregson, M. J. Lacey, R. J. Akhurst, G. R. Lyons, S. H. Rhodes, D. R. J. Smith, L. M. Engelhardt and A. H. White. 1991. Biologically Active Metabolites from Xenorhabdus Spp., Part 1. Dithiolopyrrolone Derivatives with Antibiotic Activity. Journal of Natural Products, 54: 774-784.

McInerney, B. V., W. C. Taylor, M. J. Lacey, R. J. Akhurst and R. P. Gregson. 1991. Biologically Active Metabolites from Xenorhabdus Spp., Part 2. Benzopyran-1-one Derivatives with Gastroprotective Activity. Journal of Natural Products, 54: 785-795.

McKellar, M. E. and E. B. Nelson. 2003. Compost-Induced Suppression of Pythium Damping-Off Is Mediated by Fatty-Acid-Metabolizing Seed-Colonizing Microbial Communities. Applied and Environmental Microbiology, 69: 452-460.

McNeely, D., R. M. Chanyi, J. S. Dooley, J. E. Moore and S. F. Koval. 2017. Biocontrol of Burkholderia cepacia complex bacteria and bacterial phytopathogens by Bdellovibrio bacteriovorus. Canadian Journal of Microbiology, 63: 350-358.

Milgroom, M. G. and P. Cortesi. 2004. Biological control of chestnut blight with hypovirulence: A Critical Analysis. Annual Review of Phytopathology, 42: 311-338.

Moore LW, B. H., Burr T 2001. Gram negative bacteria: Agrobacterium. In: Schaad NW (ed) Laboratory Guide for Identification of Plant Pathogenic Bacteria. APS Press, St. Paul: 15–34.

Morris, P. F. and E. W. B. Ward. 1992. Chemoattraction of zoospores of the soybean pathogen, Phytophthora sojae, by isoflavones. Physiological and Molecular Plant Pathology, 40: 17-22.

Morton, J. B., and Benny, G. L. . 1990. Revised classification of arbuscular mycorrhizal fungi (zygomycetes): a new order glomales, two new suborders, glomineae and gigasporineae and gigasporaceae, with an amendation of glomaceae. Mycotaxon: 471-491.

Muñoz-Galván, S., S. Jimeno, R. Rothstein and A. Aguilera. 2013. Histone H3K56 Acetylation, Rad52, and Non-DNA Repair Factors Control Double-Strand Break Repair Choice with the Sister Chromatid. PLoS Genetics, 9: e1003237.

Neilands, J. B. 1981. Microbial Iron Compounds. Annual Review of Biochemistry, 50: 715-731.

Notz, R., M. Maurhofer, U. Schnider-Keel, B. Duffy, D. Haas and G. Défago. 2001. Biotic Factors Affecting Expression of the 2,4-Diacetylphloroglucinol Biosynthesis Gene phlA in Pseudomonas fluorescens Biocontrol Strain CHA0 in the Rhizosphere. Phytopathology, 91: 873-881.

Nurnberger, T., F. Brunner, B. Kemmerling and L. Piater. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunological Reviews, 198: 249-266.

Nygren, K., M. Dubey, A. Zapparata, M. Iqbal, G. D. Tzelepis, M. B. Durling, D. F. Jensen and M. Karlsson. 2018. The mycoparasitic fungus Clonostachys rosea responds with both common and specific gene expression during interspecific interactions with fungal prey. Evolutionary Applications, 11: 931-949.

O’Brien, P. A. 2017. Biological control of plant diseases. Australasian Plant Pathology, 46: 293-304.

Odum, E. P. 1953. Fundamentals of ecology. xii, 387 pp. W. B. Saunders Co., Philadelphia, Pennsylvania, and London, England.

Olorunleke, F. E., G. K. H. Hua, N. P. Kieu, Z. Ma and M. Höfte. 2015. Interplay between orfamides, sessilins and phenazines in the control of Rhizoctonia diseases by Pseudomonas sp. CMR12a. Environmental Microbiology Reports, 7: 774-781.

Ongena, M. and P. Jacques. 2008. Bacillus lipopeptides: versatile weapons for plant disease biocontrol. Trends in Microbiology, 16: 115-125.

Ongena, M., F. Duby, F. Rossignol, M. L. Fauconnier, J. Dommes and P. Thonart. 2004. Stimulation of the Lipoxygenase Pathway Is Associated with Systemic Resistance Induced in Bean by a Nonpathogenic Pseudomonas Strain. Molecular Plant-Microbe Interactions, 17: 1009-1018.

Ordentlich, A., Y. Elad and I. Chet. 1988. The role of chitinase of Serratia marcescens in biocontrol of Sclerotium rolfsii. Phytopathology, 78: 84-88.

O'Sullivan, D. J. and F. O'Gara. 1992. Traits of fluorescent Pseudomonas spp. involved in suppression of plant root pathogens. Microbiological Reviews, 56: 662-676.

Palumbo, J. D., G. Y. Yuen, C. C. Jochum, K. Tatum and D. Y. Kobayashi. 2005. Mutagenesis of β-1,3-Glucanase Genes in Lysobacter enzymogenes Strain C3 Results in Reduced Biological Control Activity Toward Bipolaris Leaf Spot of Tall Fescue and Pythium Damping-Off of Sugar Beet. Phytopathology, 95: 701-707.

Pieterse, C. M. J., C. Zamioudis, R. L. Berendsen, D. M. Weller, S. C. M. Van Wees and P. A. H. M. Bakker. 2014. Induced Systemic Resistance by Beneficial Microbes. Annual Review of Phytopathology, 52: 347-375.

Puławska, J., A. Willems and P. Sobiczewski. 2006. Rapid and specific identification of four Agrobacterium species and biovars using multiplex PCR. Systematic and Applied Microbiology, 29: 470-479.

Raaijmakers, J. M. and M. Mazzola. 2012. Diversity and Natural Functions of Antibiotics Produced by Beneficial and Plant Pathogenic Bacteria. Annual Review of Phytopathology, 50: 403-424.

Reithner, B., E. Ibarra-Laclette, R. L. Mach and A. Herrera-Estrella. 2011. Identification of Mycoparasitism-Related Genes in Trichoderma atroviride. Applied and Environmental Microbiology, 77: 4361-4370.

Ren, J. H., H. Li, Y. F. Wang, J. R. Ye, A. Q. Yan and X. Q. Wu. 2013. Biocontrol potential of an endophytic Bacillus pumilus JK-SX001 against poplar canker. Biological Control, 67: 421-430.

Robinette, D. and A. G. Matthysse. 1990. Inhibition by Agrobacterium tumefaciens and Pseudomonas savastanoi of development of the hypersensitive response elicited by Pseudomonas syringae pv. phaseolicola. Journal of Bacteriology, 172: 5742-5749.

Romanazzi, G., S. M. Sanzani, Y. Bi, S. Tian, P. Gutiérrez Martínez and N. Alkan. 2016. Induced resistance to control postharvest decay of fruit and vegetables. Postharvest Biology and Technology, 122: 82-94.

Ross, E. W. and D. H. Marx. 1972. Susceptibility of sand pine to Phytophthora cinnamomi. Phytopathology, 62: 1197-1200.

Ryu, C. M., M. A. Farag, C. H. Hu, M. S. Reddy, J. W. Kloepper and P. W. Paré. 2004. Bacterial Volatiles Induce Systemic Resistance in Arabidopsis. Plant Physiology, 134: 1017-1026.

Sachana, M. 2018. Background Document for the Draft Working Document on The Risk Assessment of Secondary Metabolites of Microbial Biocontrol Agents. Paris: OECD.

Schenk, M. F., R. Hamelink, R. A. A. van der Vlugt, A. M. W. Vermunt, R. C. Kaarsenmaker and I. C. C. M. M. Stijger. 2010. The use of attenuated isolates of Pepino mosaic virus for cross-protection. European Journal of Plant Pathology, 127: 249-261.

Segarra, G., E. Casanova, M. Avilés and I. Trillas. 2010. Trichoderma asperellum strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron. Microbial ecology, 59: 141-149.

Shafizadeh, F., R. H. Furneaux, T. T. Stevenson and T. G. Cochran. 1978. 1,5-Anhydro-4-deoxy-d-glycero-hex-1-en-3-ulose and other pyrolysis products of cellulose. Carbohydrate Research, 67: 433-447.

Silo-Suh, L. A., B. J. Lethbridge, S. J. Raffel, H. He, J. Clardy and J. Handelsman. 1994. Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Applied and Environmental Microbiology, 60: 2023-2030.

Sneh, B. 1984. Chlamydospore Germination of Fusarium oxysporum f. sp.cucumerinumas Affected by Fluorescent and Lytic Bacteria from a Fusarium-Suppressive Soil. Phytopathology, 74: 1115.

Spadaro, D. and S. Droby. 2016. Development of biocontrol products for postharvest diseases of fruit: The importance of elucidating the mechanisms of action of yeast antagonists. Trends in Food Science & Technology, 47: 39-49.

Stevenson, T. T., R. E. Stenkamp, L. H. Jensen, T. G. Cochran, F. Shafizadeh and R. H. Furneaux. 1981. The crystal structure of 1,5-anhydro-4-deoxy-d-glycero-hex-1-en-3-ulose. Carbohydrate Research, 90: 319-325.

Syed Ab Rahman, S. F., E. Singh, C. M. J. Pieterse and P. M. Schenk. 2018. Emerging microbial biocontrol strategies for plant pathogens. Plant Science, 267: 102-111.

Tari, P. H. and A. J. Anderson. 1988. Fusarium Wilt Suppression and Agglutinability of Pseudomonas putida. Applied and Environmental Microbiology, 54: 2037-2041.

Tariq, M., A. Khan, M. Asif, F. Khan, T. Ansari, M. Shariq and M. A. Siddiqui. 2020. Biological control: a sustainable and practical approach for plant disease management. Acta Agriculturae Scandinavica, Section B, Soil & Plant Science, 70: 507-524.

Thaler, J. O., S. Baghdiguian and N. Boemare. 1995. Purification and characterization of xenorhabdicin, a phage tail-like bacteriocin, from the lysogenic strain F1 of Xenorhabdus nematophilus. Applied and Environmental Microbiology, 61: 2049-2052.

Thomashow, L. S. 2002. Antibiotic production by soil and rhizosphere microbes in situ. Manual of environmental microbiology. Pp. 638-647.

Thomashow, L. S. and D. M. Weller. 1988. Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. Journal of Bacteriology, 170: 3499-3508.

Tzfira, T. 2004. Agrobacterium T-DNA integration: molecules and models. Trends in Genetics, 20: 375-383.

Vallad, G. E. and R. M. Goodman. 2004. Systemic Acquired Resistance and Induced Systemic Resistance in Conventional Agriculture. Crop Science, 44: 1920-1934.

van Lenteren, J. C., K. Bolckmans, J. Köhl, W. J. Ravensberg and A. Urbaneja. 2018. Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl, 63: 39-59.

van Loon, L. C. 2000. Helping Plants To Defend Themselves: Biocontrol By Disease-Suppressing Rhizobacteria. Developments in Plant Genetics and Breeding. Elsevier, pp. 203-213.

van Loon, L. C., P. A. H. M. Bakker and C. M. J. Pieterse. 1998. Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology, 36: 453-483.

Weller, D. M., J. M. Raaijmakers, B. B. M. Gardener and L. S. Thomashow. 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annual Review of Phytopathology, 40: 309-348.

Whipps, J. M. 2001. Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany, 52: 487-511.

Wiesel, L., A. C. Newton, I. Elliott, D. Booty, E. M. Gilroy, P. R. J. Birch and I. Hein. 2014. Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Frontiers in Plant Science, 5: 655.

Yabuuchi E., Y. Kosako, L. Yano, H. Hotta, and Y. Nishiuchi. 1996. Validation of the Publication of New Names and New Combinations Previously Effectively Published Outside the IJSB: List No. 57. International Journal of Systematic Bacteriology, 46: 625-626.

Yu, S., K. Bojsen, B. Svensson and J. Marcussen. 1999. α-1,4-Glucan lyases producing 1,5-anhydro-d-fructose from starch and glycogen have sequence similarity to α-glucosidases. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1433: 1-15.

Yu, S., T. Ahmad, L. Kenne and M. Pedersén. 1995. α-1,4-Glucan lyase, a new class of starch/glycogen degrading enzyme. III. Substrate specificity, mode of action, and cleavage mechanism. Biochimica et Biophysica Acta (BBA) - General Subjects, 1244: 1-9.

Yu, S., T. M. I. E. Christensen, K. M. Kragh, K. Bojsen and J. Marcussen. 1997. Efficient purification, characterization and partial amino acid sequencing of two α-1,4-glucan lyases from fungi. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, 1339: 311-320.

Zheng, L., J. Zhao, X. Liang, G. Zhan, S. Jiang and Z. Kang. 2017. Identification of a Novel Alternaria alternata Strain Able to Hyperparasitize Puccinia striiformis f. sp. tritici, the Causal Agent of Wheat Stripe Rust. Frontiers in Microbiology, 8: 71.




DOI: https://doi.org/10.33866/phytopathol.033.01.0669

Refbacks

  • There are currently no refbacks.


Copyright (c) 2021 Syed Atif Hasan Naqvi, Muhammad Tariq Malik, Ateeq ur Ur Rehman, Ammarah Hasnain, Ummad ud Din Umar, Hajra Azeem, Shoaib Fareed, Safina Naz, Niaz Ahmed, Muhammad Shahid, Muhammad Zeeshan Drishak, Muhammad Nauman, Muhammad Akbar, Muhammad Umair

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

      
   
Pakistan Journal of Phytopathology
ISSN: 1019-763X (Print), 2305-0284 (Online).
© 2013 Pak. J. Phytopathol. All rights reserved.