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Identification of Phloem Localized Sulfate Transporter Genes and Environmental Influences on Their Transcript Level

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Identification of Phloem Localized Sulfate Transporter Genes and Environmental Influences on Their Transcript Level Sulfate distribution in Populus tremula x P. alba: identification of phloem localized sulfate transporter genes and environmental influences on their transcript level Thesis submitted in partial fulfilment of the requirements of the degree Doctor rer. nat. of the Faculty of Forest and Environmental Sciences Albert-Ludwigs-University Freiburg im Breisgau, Germany by Jasmin Dürr Freiburg im Breisgau, Germany 2009 Dean of Faculty: Prof. Dr. H. Rennenberg Supervisor: Prof. Dr. C. Herschbach Second Reviewer: Prof. Dr. S. Fink Date of thesis’ defence: July 1st 2009 Content Abbreviations 1 Introduction....................................................................................................... 1 1.1 Sulfate transport from the soil solution into the plant shoot ............................ 4 1.2 Sulfate transport in the phloem ....................................................................... 7 1.3 Sulfur storage and mobilization ..................................................................... 11 1.4 Molecular characterization of sulfate transporters ........................................ 13 1.5 Why research on poplar? .............................................................................. 20 1.6 Aims and research questions ........................................................................ 21 2 Materials and Methods................................................................................... 23 2.1 Plant material................................................................................................. 23 2.1.1 Plant propagation................................................................................... 23 2.1.2 Planting on soil....................................................................................... 24 2.1.3 Growth conditions in the greenhouse .................................................... 24 2.1.4 Field-grown poplar trees ........................................................................ 24 2.2 Plant treatments and sampling...................................................................... 25 2.2.1 Sulfate deprivation treatment on clay culture ........................................ 25 2.2.2 Sulfate deprivation treatment on sand culture ....................................... 25 2.2.3 Plant protection ...................................................................................... 26 2.2.4 Sampling of plant material ..................................................................... 26 2.3 Molecular biological methods ........................................................................ 29 2.3.1 Preparation of RNA................................................................................ 29 2.3.2 Isolation of genomic DNA ...................................................................... 31 2.3.3 Preparation of DNA free RNA................................................................ 31 2.3.4 Determination of nucleic acid concentration and quality ....................... 32 2.3.5 Separation of DNA segments by agarose gel-electrophresis................ 32 2.3.6 Separation of RNA segments by agarose gel-electrophresis................ 33 2.3.7 Isolation of DNA segments from agarose gels and DNA purification.... 34 2.3.8 cDNA synthesis...................................................................................... 34 2.3.9 Standart DNA amplification via PCR ..................................................... 35 2.3.10 DNA ligation into plasmid....................................................................... 36 2.3.11 Preparation of competent Escherichia coli cells .................................... 36 2.3.12 Transformation of Escherichia coli strain INVαF’ .................................. 37 2.3.13 Isolation of sulfate transporter sequences............................................. 38 2.3.14 Northern blotting..................................................................................... 41 2.3.15 Quantitative real-time RT PCR .............................................................. 46 2.4 Histochemistry – in situ hybridization ............................................................ 55 2.4.1 Tissue fixation and embedding in paraffin ............................................. 56 2.4.2 Preparation of tissue slices.................................................................... 57 2.4.3 Synthesis of DIG-labeled RNA probes .................................................. 57 2.4.4 In situ hybridization with DIG labeled probes ........................................ 58 2.4.5 Immunological detection of hybridized DIG probes............................... 60 2.5 Determination of sulfate................................................................................. 61 2.5.1 Sample preparation................................................................................ 62 2.5.2 Ion chromatographic measurements ..................................................... 62 2.6 Bioinformatic analysis.................................................................................... 64 2.7 Statistical analyses and calculations............................................................. 65 3 Results............................................................................................................. 67 3.1 Populus tremula x P. alba sulfate transporter gene family............................ 67 3.1.1 Characterization of cDNAs encoding putative Populus tremula x P. alba sulfate transporters ........................................................................ 67 3.1.2 Tissue specific expression analyses of the putative Populus tremula x P. alba sulfate transporter gene family .................................................. 73 3.1.3 Structure analyses of predicted sulfate transporter amino acid sequences.............................................................................................. 77 3.2 Cellular transcript localization of SULTR1;1 and SULTR3;3a....................... 81 3.2.1 Cellular transcript localization of SULTR1;1 in leaves........................... 81 3.2.2 Cellular transcript localization of SULTR1;1 in stem and roots with secondary growth................................................................................... 83 3.2.3 Cellular transcript localization of SULTR3;3a in leaves......................... 87 3.2.4 Cellular transcript localization of SULTR3;3a in stem tissues and roots with secondary growth ........................................................................... 88 3.2.5 Transcript localization of sulfate transporter SULTR1;1 and SULTR3;3a in sink tissues, i.e. fine roots and the shoot apex.............. 91 3.3 Influence of sulfur deprivation on sulfate transporter mRNA expression...... 94 3.3.1 Influence of sulfate deprivation on sulfate transporter transcript accumulation in bark and leaf vein ........................................................ 96 3.3.2 Influence of sulfate deprivation on sulfate transporter transcript accumulation in stem wood.................................................................... 99 3.4 Seasonal influences on sulfate transporter gene expression ..................... 102 3.4.1 Seasonal influences on sulfate transporter gene expression in bark tissue.................................................................................................... 104 3.4.2 Seasonal influences on sulfate transporter gene expression in leaves107 3.4.3 Principle component, correlation and regression analysis .................. 110 4 Discussion .................................................................................................... 120 4.1 Populus tremula x P. alba sulfate transporter gene family.......................... 120 4.2 Tissue specific sulfate transporter gene expression ................................... 123 4.3 Cellular transcript localization of two sulfate transporters in minor leaf veins and the lamina ............................................................................................. 126 4.4 Sulfate transporter expression in the transport phloem and in bark ........... 128 4.5 Sulfate transporter expression in wood....................................................... 133 4.6 Sulfate transporter expression in sink tissues............................................. 134 4.7 Influence of sulfate deprivation on the sulfate transporter transcript level.. 135 4.8 Seasonal variation in sulfate transporter expression .................................. 138 4.9 Conclusion ................................................................................................... 144 5 Summary ....................................................................................................... 146 6 Zusammenfassung....................................................................................... 149 7 References .................................................................................................... 153 Acknowledgement Abbreviations A adenine aa amino acids AP alkaline phosphatase APS adenosine 5’-phosphosulfate At Arabidopsis thaliana ATP adenosine triphosphate ATPase adenosine triphosphatase BCIP 5-bromo-4-chloro-3-indolyl phosphate bp base pairs BSA bovine serum albumine C cytosine Ca calcium CaCl2 calcium chloride Ca(NO3)2 calcium nitrate CC companion cell cDNA complementary DNA Ci curie CoCl2 cobalt chloride CP crossing point CTAB cetyltrimethylammonium bromide CTP cytidine triphosphate CuCl2 copper chloride CuSO4 copper sulfate dATP deoxyadenosine triphosphate dCTP deoxycytidine
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