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Characterisation of an Intron-Split Solanales Microrna Characterisation of an intron-split Solanales microRNA Zahara Medina Calzada A thesis submitted for the degree of Doctor of Philosophy University of East Anglia School of Biological Sciences September 2017 This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with the author and that use of any information derived there from must be in accordance with current UK Copyright Law. In addition, any quotation or extract must include full attribution “Doing science is very romantic… when it works!” (the friend of a friend of mine) 2 Abstract MicroRNAs (miRNAs) are a distinct class of short endogenous RNAs with central roles in post-transcriptional regulation of gene expression that make them essential for the development and normal physiology of several groups of eukaryotes, including plants. In the last 15 years, hundreds of miRNA species have been identified in plants and great advances have been achieved in the understanding of plant miRNA biogenesis and mode of action. However, many miRNAs, generally those with less conventional features, still remain to be discovered. Likewise, further layers that regulate the pathway from miRNA biogenesis to function and turnover are starting to be revealed. In the present work we have studied the tomato miRNA “top14”, a miRNA with a non-canonical pri-miRNA structure in which an intron is in between miRNA and miRNA*. We have found that this miRNA is conserved within the economically important Solanaceae family and among other members of the Solanales order also agriculturally relevant, like in sweet potato, while its peculiar intron-split pri-miRNA structure is exclusively kept in the more closely related genera Solanum , Capsicum and Nicotiana . In these three genera, two different pri-miRNA variants were detected; one spliced and the other one retaining the intron. After testing the mature miRNA production from the wild type tomato MIRtop14 , from a version without intron and from another version without splicing capability, it was found that the intron influenced the accumulation of mature miRNA. Finally, a mRNA cleaved by this miRNA was identified; the mRNA coding for LOW PHOSPHATE ROOT (LPR), a protein which in Arabidopsis is involved in the arrest of root growth under phosphate starvation conditions. Interestingly, although LPR is widely conserved in plants, included in all the ones harbouring miRNAtop14, LPR cleavage was found to occur only in the three genera where the intron-split pri-miRNA structure is conserved. The current study indicates that MIRs encoded by less canonical loci should be included in future miRNA searches, since they may be producing mature miRNAs with a function, as seen in this investigation. Furthermore, our results suggest that this miRNA may be regulated through intron retention. In case of being confirmed, it would add to the few recently reported examples of post-transcriptional regulation of a miRNA and should encourage the research of less known layers of miRNA regulation. Finally, the study of this miRNA sheds light to the crosstalk between miRNA biogenesis and splicing and, in a broader context, to the complex interactions between the different RNA regulatory networks operating in plants. 3 Table of Contents Abstract 3 Table of Contents 4 List of Figures & Tables 8 Acknowledgements 10 Abbreviations 12 Chapter 1. Introduction 17 1.1. RNA biology overview 18 1.2. miRNAs in plants 19 1.2.1. Introduction 19 1.2.2. What is a miRNA? 19 1.2.3. miRNA life cycle 20 1.2.3.1. Transcription 20 1.2.3.2. Processing 21 1.2.3.2.1. Processing machinery 21 1.2.3.2.2. Processing patterns 22 1.2.3.3. Methylation and nuclear export 23 1.2.3.4. RISC assembly 24 1.2.3.5. Mechanism of action 25 1.2.3.6. Turnover 28 1.2.4. miRNA genes, origin and evolution 29 1.2.4.1. miRNA genes ( MIR ) and genomic organization 29 1.2.4.2. MIR origin 30 1.2.4.3. MIR evolution 34 1.3. Splicing in plants 36 1.3.1. Introduction 36 1.3.2. What is splicing? 37 1.3.3. Types of Introns 37 1.3.4. The splicing process 37 1.3.4.1. Splicing machinery 37 1.3.4.2. Splicing mechanism 38 1.3.4.3. Splicing models 40 1.3.4.4. Splicing regulation and consequences 42 4 1.3.5. Origin and evolution of introns and splicing 43 1.4. Aims and objectives 47 Chapter 2. Materials and Methods 48 2.1. General material and methods 49 2.1.1. Plant materials and growth conditions 49 2.1.2. Total RNA extraction 49 2.1.3. pGEM-t easy cloning method 49 2.1.4. Colony PCR 50 2.1.5. sRNA Northern blot 51 2.2. Material and methods chapter 3 53 2.2.1. PCR analysis of MIRtop14 genomic locus (fig. 3.2.) 53 2.2.2. Northern blot detection of miRNAtop14 in different species (fig.3.5.A) 53 2.2.3. RT-PCR analysis of pri-miRNAtop14 (fig. 3.5.B) 54 2.2.4. Northern blot detection of miRNAtop14 in different tissues (fig. 3.6) 56 2.3. Material and methods chapter 4 57 2.3.1. Cloning of Sly-pri-miRNAtop14 sequences 57 2.3.2. Cloning of Osa-MIR528 gDNA sequence 58 2.3.3. Golden gate cloning 59 2.3.4. Site-directed mutagenesis 60 2.3.5. Arabidopsis transformation (“floral dip” method) 61 2.3.6. Northern blot detection of miRNAtop14 in the three constructs (fig 4.4.A) 62 2.3.7. RT-PCR analysis of pri-miRNAtop14 in the three constructs (fig 4.4.B) 62 2.4. Material and methods chapter 5 64 2.4.1. RLM-RACE 64 2.4.2. Solanum lycopersicum RLM-RACE PCR (fig. 5.4) 65 2.4.3. Nicotiana benthamiana RLM-RACE PCR (fig 5.6) 66 2.4.4. Petunia axillaris RLM-RACE PCR (fig. 5.8) 67 Chapter 3. miRNA “top14” characterization 69 3.1. Introduction 70 5 3.1.1. Identification and characterization of miRNAs 70 3.1.2. Intron-split miRNAs 71 3.1.3. Study of miRNAtop14 72 3.2. Results 73 3.2.1. Identification of miRNAtop14 in Solanales 73 3.2.2. MIRtop14 genomic sequence and predicted pri-miRNA 76 3.2.3. miRNAtop14 primary transcript secondary structures 79 3.2.4. RNAtop14 mature miRNA and primary transcript expression detection 84 3.3. Discussion 86 3.3.1. Discovery of miRNAtop14 86 3.3.2. MIRtop14 phylogenetic study 87 3.3.3. pri-miRNA and miRNAtop14 expression 89 Chapter 4. Intron influence in miRNAtop14 biogenesis 92 4.1 Introduction 93 4.1.1. pri-miRNAs processing and splicing crosstalk 93 4.1.2. Influence of pri-miRNA introns in mature miRNA accumulation 95 4.1.3. Study of miRNAtop14 intron influence 98 4.2 Results 99 4.2.1. A system to assess intron influence in mature miRNAtop14 levels 99 4.2.2. Intron influence in S. lycopersicum miRNAtop14 levels 102 4.1. Discussion 104 Chapter 5. miRNAtop14 mRNA target: LPR 107 5.1. Introduction 108 5.1.1. miRNAs function, mode of action and roles 108 5.1.2. miRNA-target evolution 109 5.1.3 Multicopper oxidases and LPR 109 5.1.4 Study of miRNAtop14 target 113 5.2. Results 115 5.2.1. Identification of miRNAtop14 target in Solanum lycopersicum 115 5.2.1.1. RLM-RACE 115 5.2.1.2. Degradome 118 5.2.2. Identification of miRNAtop14 target in Nicotiana benthamiana 120 6 5.2.2.1. RLM-RACE 120 5.2.2.2. Degradome 125 5.2.3. miRNAtop14 targeting of LPR in other Solanales species 126 5.2.3.1. miRNAtop14-LPR complementarity in Solanales 126 5.2.3.2. miRNAtop14 targeting of LPR by cleavage in Petunia axillaris 129 5.3. Discussion 131 5.3.1. Identification of miRNAtop14 targe 131 5.3.2. miRNA-target coevolution and interaction 132 5.3.3. miRNAtop14 function in Solanales 135 Chapter 6. Summary and general discussion 138 References 146 Appendix 172 7 List of Figures & Tables Chapter 1 Figure 1.1. Processing patterns of pri-miRNAs depending on their structure 23 Figure 1.2. Plant miRNAs life cycle 24 Figure 1.3. Three possible origins of new plant MIR genes 33 Figure 1.4. Splicing mechanism 39 Figure 1.5. Types of alternative splicing and its frequency in humans and Arabidopsis 41 Figure 1.6. Models of intron gain, loss and sliding 45 Chapter 2 Table 2.1. Oligo and primers sequences used for RLM-RACE analyses 68 Chapter 3 Figure 3.1. Cladogram depicting the evolutionary relationship among all species in which MIRtop14 has been identified 74 Table 3.1. miRNAtop14 and miRNAtop14* sequences in all the species in which the miRNA has been identified 75 Figure 3.2. PCR from genomic DNA amplifying putative pri-miRNAtop14 sequence in the species Solanum lycopersicum (Sly), Nicotiana benthamiana (Nbe), Petunia axillaris (Pax) and Ipomoea nil (Ini) 76 Table 3.2. miRNAtop14-miRNAtop14* distance and MIRtop14 transcript prediction 78 Figure 3.3. Exon-intron structure predicted for the different genera found harbouring miRNAtop14 79 Figure 3.4. pri-miRNAtop14 secondary structure and schematic representation of the resulting miRNA hairpin 83 Figure 3.5. Detection of miRNAtop14 and pri-miRNAtop14 in different plant species 84 Figure 3.6. Detection of mature miRNAtop14 levels in Solanum lycopersicum root, stem, leaves and leaflets 85 8 Chapter 4 Figure 4.1. AS variants from Arabidopsis MIR842/846 and associated regulation of pri-miRNA and mature miRNA levels upon ABA application 94 Figure 4.2.
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