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Waheed Akram Institute of Agricultural Sciences STUDIES ON EFFICACY AND MECHANISMS OF BACILLUS STRAINS TO INDUCE SYSTEMIC RESISTANCE IN TOMATO AGAINST FUSARIUM WILT A thesis submitted to the University of the Punjab in partial fulfillment of the requirement for the degree of doctor of philosophy in Agricultural Sciences WAHEED AKRAM INSTITUTE OF AGRICULTURAL SCIENCES UNIVERSITY OF THE PUNJAB LAHORE STUDIES ON EFFICACY AND MECHANISMS OF BACILLUS STRAINS TO INDUCE SYSTEMIC RESISTANCE IN TOMATO AGAINST FUSARIUM WILT A thesis submitted to the University of the Punjab in partial fulfillment of the requirement for the degree of doctor of philosophy in Agricultural Sciences By Waheed Akram Supervisor Dr. Tehmina Anjum Assistant Professor Co-supervisor Dr. Basharat Ali Assistant Professor INSTITUTE OF AGRICULTURAL SCIENCES UNIVERSITY OF THE PUNJAB LAHORE CERTIFICATE This is to certify that the research entitled “Studies on efficacy and mechanisms of Bacillus strains to induce systematic resistance in tomato against fusarium wilt” described in this thesis by Mr. Waheed Akram, is an original work of the author and has been carried out under my direct supervision. I have personally gone through all the data, results, materials reported in the dissertation and certify their correctness and authenticity. I further certify that the material included in this thesis has not been used in part or full in a dissertation already submitted or in the process of submission in partial or complete fulfillment of the award of any other degree from any institution. I also certify that the thesis has been prepared under my supervision according to the prescribed format and I endorse its evaluation for the award of Ph.D. degree through the official procedures of the University of the Punjab, Lahore. Supervisor Dr. Tehmina Anjum Assistant Professor Dr. Basharat Ali Assistant Professor Date: ____________ i DECLARATION CERTIFICATE This thesis which is being submitted for the degree of Ph.D. in the University of the Punjab does not contain any material which has been submitted for the award of Ph.D. Degree in any University and, to the best of my knowledge and belief, neither does this thesis contain any material published or written previously by another person, except when due reference is made to the source in the text of the thesis. (Waheed Akram) Ph.D. Scholar ii DEDICATED TO MY BELOVED PARENTS AND TEACHERS iii ACKNOWLEDGMENTS All praises and gratitude is to the splendor of Almighty ALLAH, the Beneficent and the Merciful, Whose blessings facilitated me to fulfill this research work. I pay all compliments to the Holy Prophet Muhammad (Sallal laho Alahe Wa’alhe Wasallam), the wisdom and gateway of the comprehension. First of all we are very thankful to Higher Education Commission of Pakistan for providing financial support to perform this whole research work and financial aid to researcher and supervisor. I express my cordial gratitude to my supervisors Dr. Tehmina Anjum, Assistant Professor, Institute of Agricultural Sciences, University of the Punjab, Lahore and Dr. Basharat Ali, Assistant Professor, Department of Microbiology and Molecular Genetics, University of the Punjab, Lahore for their enthusiastic concern, precious implications, regular encouragement and kind attitude during the course of this research venture. For numerous supportive suggestions during research studies, I am grateful to Dr. M. Saleem Haider, Professor and Director, Institute of Agricultural Sciences, University of the Punjab, Lahore. I may never forget support of Dr. Ahmad Ali Shahid, Associate Professor, CEMB, university of the Punjab, during my studies. Heartfelt thanks are also being extended to Dr. Amir Ali, Associate Professor, Department of Botany, University of Sargodha, Sargodha for his support from beginning of my studies and his valuable guidance in the molecular and statistical analysis. I feel enormous gratification to state my earnest admiration and gratefulness to Malik Muhammad Zaheer, Resident Officer-II, University of the Punjab, Lahore for his kind guidance, help and support during these studies. I am also grateful to my friends especially Aqeel Ahmad, my colleagues and all staff members of IAGS for their assistance and good desires throughout my research work. Sincere thanks are also for Syed Ehsan Haider Zaidi for helping in formatting this dissertation. Last but not the least, I am proud of my family members for their ethical and pecuniary support and encouraging manner to attain my goal and they extended their hands of sincerity towards me to accomplish higher targets of life. (Waheed Akram) iv Summary Plant diseases are the most common reason for reduction in agricultural crop yield. Tomato (Lycopersicon esculentum Mill.) is among the most prevalent vegetables cultivated throughout the world. Lifecycle of this crop is threatened by an inclusive array of fungal, bacterial and viral pathogens. Fusarium wilt disease of tomato is economically important due to yield and quality loss of the crop. Fungicides are the only option that farmers use against this pathogen. These fungicides are hazardous for our environment and human health as these toxify food commodities and ground water reserves. Moreover, they can never be the best option to manage the disease due to their extensive toxicity and minuscule degradability. These facts engender the need of development of some alternate measure for controlling the pathogen. Induced resistance is the potential alternate means of controlling fungal pathogens of plants. In last decade, tomato plant has become a successful model plant to investigate the induction of defense pathways after exposure to biotic and abiotic elicitors which act as a trigger of these mechanisms of resistance. Understanding these mechanisms in order to improve crop protection is a main goal for Plant Pathology. Present study was aimed on screening different native Bacillus strains to induce systemic resistance in tomato plants against fusarim wilt along with elucidation of immune responses attributable to the defense systems of plant and to search bacterial determinant/s which actually trigger systemic resistance inside the plant body. First, ten isolated strains of Fusarium oxysporum f.sp. lycopersici. (Fol) were tested for their virulence against 23 varieties of tomato. After interacting Fol strains and tomato varieties in all possible combinations, most virulent Fol strain ‘Fol7’ and three tomato varieties with varying susceptibility viz: Fine Star (72%), Rio Grande (49%) and Red Power (24%) were selected for further experimentations. Different native non-pathogenic rhizospheric Bacillus strains were procured from two different bacterial conservatories of University of the Punjab Lahore, v Pakistan. All Bacillus strains were screened to manage fusarium wilt of tomato under split root system. Two strains viz: B. fortis IAGS162 and B. subtilis IAGS174 provided most significant protection against fusarium wilt. These strains reduced >70% disease severity in comparison to the pathogen control. In this experiment, all Bacillus strains were again interacted with tomato plants in split root experiment and changes were denoted in quantities of different defense related biochemicals like total phenolics and some enzymes involved in phenylpropenoid pathway in time course manner. B. fortis IAGS162 and B. subtilis IAGS174 provided highest significant up-regulations in these biochemicals as compared to control plants. In next experiment, study was undertaken in an effort to elaborate understandings about “how a beneficial bacterium and plant host crosstalk with one another in the presence of a pathogen”. For that purpose, molecular, histological and biochemical mechanisms were elucidated. Both these strains induced tomato plants for higher expression levels of PR-genes, extensive localization of lignin, phenolics and peroxidases in stem and root tissues. GC/MS analysis of total metabolites showed extensive re-modulation of primary and secondary metabolism in tomato plants under influence of these bacterial strains. Most of the up-regulated biochemicals were belonging to pathways like primary metabolism, TCA cycle, phenylpropenoid pathway and signaling pathways. Taken all these together eventually led to protection in tomato plants against fusarium wilt along with growth promotion. Two best performing Bacillus strains were further evaluated in field studies in the form of talc based formulations. Formulation containing both Bacillus strain viz: B. fortis IAGS162 and B. subtilis IAGS174 showed maximum protection against fusarium wilt disease along with increase in growth and yield. This treatment reduced disease index up to 58% respectively on average basis in all the three tomato varieties across both seasons. To conclude this work, studies were undertaken to search out determinant/s of induced systemic resistance from these best performing bacterial strains. Initially, it was observed that ISR determinant/s were extracellular metabolites in nature secreted in media from both bacterial strains. Further experimentations clued out that two aromatic compounds viz: Benzene acetic vi acid and Phthalic acid methyl ester as ISR determinants from B. fortis IAGS162 and B. subtilis IAGS174 respectively. To assess the significance of the results obtained during various experiments data was subjected to a number of statistical analyses. These analyses include analysis of variance (ANOVA) and Duncan’s Multiple Range Test (DMRT). In conclusion, B. fortis IAGS162 and B. subtilis IAGS174 are able to mitigate
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