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The Molecular Biology of Lichen Symbiosis and Development

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The Molecular Biology of Lichen Symbiosis and Development The Molecular Biology of Lichen Symbiosis and Development by Suzanne L. Joneson Department of Biology Duke University Date: Approved: Fran¸cois M. Lutzoni, PhD, Advisor Daniele Armaleo, PhD Fred S. Dietrich, PhD Thomas G. Mitchell, PhD Rytas Vilgalys, PhD Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2009 Abstract (Biology) The Molecular Biology of Lichen Symbiosis and Development by Suzanne L. Joneson Department of Biology Duke University Date: Approved: Fran¸cois M. Lutzoni, PhD, Advisor Daniele Armaleo, PhD Fred S. Dietrich, PhD Thomas G. Mitchell, PhD Rytas Vilgalys, PhD An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology in the Graduate School of Duke University 2009 Copyright c 2009 by Suzanne L. Joneson All rights reserved except the rights granted by the Creative Commons Attribution-Noncommercial Licence Abstract A lichen thallus is an emergent structure formed through the long-lived symbiotic growth of a filamentous fungus and uni-cellular green algae. How the symbionts find and recognize each other, resist potential attack, and proceed to form this unique body remains enigmatic. Based on other well-studied eukaryotic systems, the de- velopment of a lichen thallus must rely upon the successful identification and col- laboration of these two very different organisms. Identifying the molecular basis of microbe recognition and interactions remains one of the greatest challenges in studying symbiotic systems. In the development of stratified lichen thalli containing trebouxioid algae, the mycobiont undergoes a change in hyphal morphology when making physical contact with its photobiont. This change is characterized by a switch from apical growth to increased lateral branching, and has been proposed to be a result of thigmotropism (response to shape). This morphological change can be seen when the mycobiont Cladonia grayi contacts its symbiotic partner, the trebouxioid photobiont Aster- ochloris sp. Therefore, observations were made using environmental scanning elec- tron microscopy, glass beads, alternative phototrophs, and the development of the lichen symbiosis between C. grayi and Asterochloris sp. The results of these obser- vations confirmed that the change in growth pattern of C. grayi in lichen symbiosis is not a result of thigmotropism or fungal contact with phototrophs, but instead is diagnostic of lichen symbiosis. iv This phenotypically defined stage was next used to begin studying the genetic and molecular mechanisms underlying lichen-symbiosis development. Using suppression subtractive hybridization to determine differential gene expression, fungal and algal libraries were made of putatively upregulated genes in the pre-contact and initially post-contact stages of lichen symbiosis. The symbiotic expression levels of select genes were then verified using quantitative PCR. Fungal protein products of genes upregulated in lichen symbiosis show significant matches to proteins putatively in- volved in fungal self and non-self recognition, lipid metabolism, negative regulation of glucose repressible genes, an oxidoreductase, a dioxygenase, and a conserved hy- pothetical protein. Algal genes that are upregulated in lichen symbiosis include a chitinase-like protein, an amino acid metabolism protein, a dynamin related protein, and a protein arginine methyltransferase. Furthermore, early stages in lichen devel- opment are marked not by a drastic change in transcriptional products, but instead by an overall change in genes that are already expressed. Finally, one of the candidate fungal genes upregulated in the initial post-contact stage of lichen development, Lip3, was cloned from Cladonia grayi cDNA, and het- erologously expressed in yeast. The protein product of this gene was shown to be a functional secreted extracellular lipase. v Contents Abstract iv List of Tables x List of Figures xii Acknowledgements xiii 1 Introduction 1 1.1 Background ................................ 1 1.2 Overviewofthiswork .......................... 5 1.2.1 Phenotypic marker of the Cladonia grayi and Asterochloris sp. symbiosis ............................. 5 1.2.2 Differential gene regulation in early stages of lichen development 7 1.2.3 Heterologous expression of a lichen-forming fungal gene, in yeast 11 1.3 FutureResearch.............................. 12 2 Compatibility and thigmotropism in the lichen symbiosis: A reap- praisal. 13 2.1 Introduction................................ 13 2.2 Methods.................................. 17 2.2.1 Culturesandmedia. 17 2.2.2 GlassBeadPreparation . 19 2.2.3 Environmental Scanning Electron Microscopy (ESEM) . 20 2.3 Results................................... 21 vi 2.4 Discussion and Conclusion . 23 3 Fungal gene expression in early lichen symbiosis. 33 3.1 Introduction................................ 33 3.2 Materials ................................. 36 3.2.1 Experimentalsetup . 36 3.2.2 RNAextraction.......................... 38 3.2.3 ss–cDNAsynthesis . 39 3.2.4 Suppression subtractive hybridization and cDNA library con- struction.............................. 40 3.2.5 Clone sequencing and analysis . 41 3.2.6 Subtractionefficacy. 42 3.2.7 qPCR and cellular location prediction . 43 3.2.8 Searching the genome for gene duplication of qPCR selected geneticregions. .......................... 45 3.3 Results................................... 46 3.3.1 Library sequencing and gene annotation . 46 3.3.2 Subtractionefficacy. 47 3.3.3 qPCR results of select genes . 48 3.3.4 Stage1qPCR........................... 49 3.3.5 Stage2qPCR........................... 50 3.3.6 SSH-cDNAs used in qPCR are preliminarily from single copy genes. ............................... 50 3.4 Discussion ................................. 51 4 Gene expression of Asterochloris sp. in early developmental stages of lichen-symbiosis. 68 4.1 Introduction................................ 68 4.2 MaterialsandMethods . 72 vii 4.2.1 Databaseinquiries . 72 4.2.2 Determining stage 2 organism-of-origin for gene fragments . 73 4.2.3 Searching the genome for possible duplicate genes of qPCR selected genetic regions. 74 4.3 Results................................... 75 4.3.1 Library construction and gene annotation . 75 4.3.2 qPCR results of select genes . 76 4.3.3 Conserved protein domains. 78 4.3.4 SSH-cDNAs used in qPCR are preliminarily from single copy genes. ............................... 80 4.4 Discussion ................................. 80 5 Heterologous expression of Cladonia grayi Lip3 in yeast. 96 5.1 Introduction................................ 96 5.2 Methods.................................. 98 5.2.1 StrainsandCultivation. 98 5.2.2 Nucleotide Sequences . 98 5.2.3 PlasmidConstruction. 99 5.2.4 Searching the yeast genome with Lip3 ............. 100 5.2.5 EnzymeAssay........................... 100 5.2.6 ProteinSequence . .. .. 101 5.3 Results................................... 101 5.3.1 Nucleotide and Protein Sequences. 101 5.3.2 Searching the yeast genome with Lip3 ............. 102 5.3.3 HeterologousExpression . 102 5.4 Discussion ................................. 103 Appendices 108 viii A GenBank, UniProt, and Gene Ontology summary information for Cladonia grayi in stages 1 and 2 of lichen development. 109 A.1 Combined GenBank and UniProt summary information for stages 1 and 2 Cladonia grayi genefragments. 109 A.2 Summary of Gene Ontology (GO) organizing principles for Clado- nia grayi in stages 1 and 2 of lichen development . 140 A.3 Keys for linking GO terms to individual Clone IDs, in Cladonia grayi 145 B GenBank, UniProt, and Gene Ontology summary information for Asterochloris sp. in stages 1 and 2 of lichen development. 161 B.1 Combined GenBank and UniProt summary information for stages 1 and 2 Asterochloris sp.genefragments . 161 B.2 Summary of Gene Ontology (GO) organizing principles for Asterochlo- ris sp. in stages 1 and 2 of lichen development . 185 B.3 Keys for linking GO terms to individual Clone IDs, in Asterochloris sp.190 C GenBank, UniProt, and Gene Ontology summary information for “either” in stages 1 and 2 of lichen development. 204 C.1 Combined GenBank and UniProt summary information for stage 2 “either”genefragments . 204 C.2 Summary of Gene Ontology (GO) organizing principles for “either” in stage 2 of lichen development . 208 Bibliography 212 Biography 229 ix List of Tables 3.1 Primers used in qPCR to determine relative proportions of mycobiont and photobiont in stage 2, and differential expression of select genes instages1and2. ............................. 61 3.2 Cladonia grayi gene regions selected from stage 1 of lichen resynthesis, chosenforqPCRanalysis. 63 3.3 Cladonia grayi gene regions selected from stage 2 of lichen resynthesis, chosenforqPCRanalysis. 64 3.4 SSHefficacy................................. 65 3.5 Average aposymbiotic and symbiotic qPCR expression levels of 26 Cladonia grayi genes after 9 days (stage 1 of lichen development). 66 3.6 Average aposymbiotic and symbiotic qPCR expression levels of 27 Cladonia grayi genes after 21 days (stage 2 of lichen development) . 67 4.1 Primers used in qPCR to determine differential expression of select Asterochloris sp.genesinstages1and2 . 90 4.2 Asterochloris sp. gene regions selected from stage 1 of lichen resyn- thesis and chosen for qPCR analysis . 92 4.3 Asterochloris sp. gene regions selected from stage 2 of lichen resyn- thesis and chosen for qPCR
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