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Open Melnick Phd Thesis.Pdf The Pennsylvania State University The Graduate School Department of Plant Pathology ENDOPHYTIC BACILLUS SPP. OF THEOBROMA CACAO: ECOLOGY AND POTENTIAL FOR BIOLOGICAL CONTROL OF CACAO DISEASES A Dissertation in Plant Pathology by Rachel L. Melnick 2010 Rachel L. Melnick Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2010 The dissertation of Rachel L. Melnick was reviewed and approved* by the following: Paul A. Backman Professor of Plant Pathology Dissertation Advisor Chair of Committee Bryan A. Bailey Adjunct Professor of Plant Pathology Plant Pathologist at USDA-ARS SPCL Special Member Maria del Mar Jimenez-Gasco Assistant Professor of Plant Pathology Gary W. Moorman Professor of Plant Pathology Roger T. Koide Professor of Horticultural Ecology Frederick E. Gildow Professor of Plant Pathology Head of the Department of Plant Pathology *Signatures are on file in the Graduate School iii ABSTRACT Yield of Theobroma cacao, the chocolate tree, is drastically limited by disease. In South America, there are three key diseases: black pod, caused by Phytophthora spp.; frosty pod, caused by Moniliophthora roreri; and witches‟ broom, caused by Moniliophthora perniciosa. Although chemical control options exist, farmers typically only use cultural disease management such as phytosanitary pruning. Agrochemical use can be problematic in the developing countries where cacao is grown due to large risks to human health and the environment. There has been increased interest in the use of biological control for management of cacao diseases due to problems associated with pesticide use as well as consumer desire for organic chocolate. Fungal species have been the main focus for research on biological control of cacao diseases, while cacao- associated bacteria have been nearly ignored. Previous research demonstrated that a Bacillus sp. from tomato was capable of endophytically colonizing cacao foliage and reduced disease severity of Phytophthora capsici in detached leaf assays. The previous success of research utilizing bacterial endophytes lead to an investigation on endospore-forming bacterial endophytes associated with cacao tissue. The present research focused on obtaining and screening endospore-forming cacao bacterial endophytes for their ability to suppress diseases. Approximately 70 isolates were obtained and screened for characteristics of elite biological control agents, such as chitinase production, ability to colonize clean plants, and disease suppression. From these isolates, four were tested in a two-year field study on biological control of witches‟ broom disease at INIAP in Pichilingue, Ecuador. In this trial, application of Bacillus pumilus isolate ET consistently reduced disease severity of witches‟ broom, when bacteria were applied three times a year and phytosanitary pruning was conducted at the end of each season. Along with this study, it was determined that applied bacterial endophytes persisted in cacao foliage throughout the dry season (6 month period) when applied at the season onset. Bacterial endophytes persisted in the rainy season, but needed to be re-applied midway through the six month season to maintain adequate population levels. In addition to research on suppression of witches‟ broom, these four bacterial isolates were tested for their ability to suppress cacao pod disease and cherelle wilt in two cacao genotypes: „Nacional‟ and „CCN51‟. Bacillus pumilus ET reduced cherelle wilt in both genotypes, indicating the presence of a biological component associated with what was once thought to be a physiological condition. None of the four tested isolates reduced diseases on cacao pods, but application of B. pumilus ET increased the overall number of healthy pods in the iv first two months of the four month experiment. These successful field results indicate the positive potential for the use of native endophytic bacteria to manage cacao diseases. Further research was conducted to determine the modes of action of the biological control agents as well as whether endophytic bacteria could successfully be combined with endophytic Trichoderma spp. currently being tested as biological control agents of cacao diseases. Antibiosis studies indicated that B. pumilus ET was antagonistic to P. capsici and M. roreri, but not M. perniciosa in plate antagonism studies. Research was conducted using quantitative real time PCR (Q-PCR) to determine whether colonization of endophytic Bacillus spp. activated the expression of cacao expressed sequence tags (ESTs) related to defense. Research indicated that colonization of cacao seedlings with bacterial endophytes activated the expression of cacao ESTs related to plant defense, such as chitinases, pathogenesis-related proteins, and lipoxygenase. Another mode of action that was tested was to determine whether application of endophytic species displaced native endophytes, which were likely neutral in terms of plant health. Analysis of microbial communities utilizing automated ribosomal intergenic spacer analysis (ARISA) indicated that application of potential biological control agents did not impact the community of native Bacillus spp. or the overall bacterial community during the sampled periods. Overall, the suppression of disease caused by B. pumilus ET was likely due to a combination of chitinase production, induced resistance, and potentially antibiosis. Additional research demonstrated that bacterial endophytes could successfully exist with endophytic Trichoderma spp. when applied either to seeds or foliage. Bacillus spp. persisted in roots (when applied to seeds only), stems, and foliage, while Trichoderma spp. persisted in roots and stems. These species were capable of co-existing in the same niche, therefore could likely be used together in the field. In conclusion, the results reported here indicate that B. pumilus ET would likely make an excellent biological control agent, due to its multiple modes of action and ability to be combined with endophytic Trichoderma spp. v TABLE OF CONTENTS LIST OF FIGURES ................................................................................................................. ix LIST OF TABLES ................................................................................................................... xviii ACKNOWLEDGEMENTS ..................................................................................................... xx Chapter 1 Review of Literature and Research Objectives ...................................................... 1 Theobroma cacao ............................................................................................................. 1 Diseases of Cacao ............................................................................................................ 4 Introduction .............................................................................................................. 4 Ceratocystis Wilt ...................................................................................................... 4 Frosty Pod ................................................................................................................ 5 Witches‟ broom ........................................................................................................ 6 Black Pod ................................................................................................................. 9 Biological Control ............................................................................................................ 11 Modes of Action ....................................................................................................... 11 Biological Control Utilizing Induced Resistance ..................................................... 12 Biological Control of Cacao Diseases ...................................................................... 14 Research Objectives ......................................................................................................... 16 Works Cited ..................................................................................................................... 18 Chapter 2 Isolation and Screening of Endophytic Endospore-Forming Bacteria from Theobroma cacao ............................................................................................................. 25 Introduction ...................................................................................................................... 25 Material and Methods ...................................................................................................... 27 Isolation of endospore-forming bacterial endophytes from cacao tissue ................. 27 Confirmation of endospore production by bacterial endophytes ............................. 28 Determining whether isolates are members of the Bacillus cereus group clade through use of selective media ......................................................................... 28 Determining whether bacterial endophytes possess chitinase activity ..................... 28 Determining whether bacterial endophytes are directly antagonistic to cacao pathogens .......................................................................................................... 29 Sequencing of regions of the 16S rRNA gene to determine species identification of bacterial endophytes .............................................................. 29 Cacao plant material and growth conditions ...........................................................
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