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Title Page

Contents

Chapter 1. General introduction 13

1.1. Rhizosphere 13

1.2. Plant growth-promoting rhizobacteria (PGPR) 15

1.2.1. Direct plant growth promotion 17

1.2.2. Indirect plant growth promotion 21

1.3. Quorum sensing (QS) 24

1.4. The genus Serratia 28

1.5. Quorum sensing (QS) in Serratia spp. 28

1.6. Objectives of the study 30

Chapter 2. Quorum sensing activity of plant growth-promoting rhizobacterium Serratia glossinae GS2 isolated from the sesame (Sesamum indicum L.) rhizosphere 32

2.1. Introduction 32

2.2. Materials and Methods 35

2.2.1. Isolation and identification of phytohormone-producing bacteria 35

2.2.2. ACC deaminase activity, biofilm formation, and morphological and biochemical characterization 36

2.2.3. IAA analysis by gas chromatography-mass spectrometry (GC-MS) 37

2.2.4. Detection of N-acyl homoserine lactones (AHLs) 38

2.2.5. AHL identification by liquid chromatography-mass spectrometry (LC-MS/MS) 39

2.2.6. In vivo pot trial 40

2.2.7. Statistical analysis 40

2.3. Results 41

2.3.1. Isolation and identification of phytohormone-producing bacteria 41

2.3.2. ACC deaminase activity, biofilm formation, and morphological and biochemical characterization 44

2.3.3. IAA quantification by GC-MS analysis 48

2.3.4. Detection and identification of AHLs 50

2.3.5. In vivo pot trial 52

2.4. Discussion 55

Chapter 3. Complete genome sequence of Serratia glossinae strain GS2, an N-acyl homoserine lactone-producing and plant growth-promoting rhizobacterium 58

3.1. Introduction 58

3.2. Materials and Methods 59

3.2.1. Genomic DNA extraction and bacterial culture conditions 59

3.2.2. Genome sequencing, assembly, and annotation 60

3.2.3. Identification of putative luxI/R-type quorum-sensing (QS) genes 61

3.3. Results 62

3.3.1. Whole genome sequencing and sequence-based gene identification 62

3.3.2. Identification of putative luxI/R-type quorum-sensing (QS) genes 67

3.3.3. Plant growth-promoting related genes 70

3.4. Discussion 73

Chapter 4. Quorum-sensing effects in the plant growth-promoting rhizobacterium Serratia glossinae strain GS2 75

4.1. Introduction 75

4.2. Materials and Methods 77

4.2.1. Mutagenesis of quorum-sensing related genes in Serratia glossinae strain GS2 77

4.2.2. Quorum-sensing regulated phenotypes in Serratia glossinae strain GS2 83

4.2.3. Proteome 90

4.2.4. Transcriptome 93

4.3. Results 95

4.3.1. Mutagenesis of quorum-sensing related genes in Serratia glossinae strain GS2 95

4.3.2. Quorum-sensing regulated phenotypes in Serratia glossinae strain GS2 97

4.3.3. Proteome analysis 116

4.3.4. Transcriptome 119

4.4. Discussion 133

Chapter 5. Bidirectional communication of quorum-sensing signal molecules between rhizobacteria and plants evaluated by root-microbiome and meta-transcriptome analysis 135

5.1. Introduction 135

5.2. Materials and Methods 137

5.2.1. Soil collection and plant growth experiment 137

5.2.2. Root-microbiome analysis 139

5.2.3. Soil meta-transcriptome analysis 141

5.2.4. Statistical analysis 142

5.3. Results 143

5.3.1. Plant growth promotion experiment 143

5.3.2. Root-microbiome analysis 149

5.3.3. Soil meta-transcriptome analysis 160

5.4. Discussion 169

References 171

Abstract 184

초록 186

List of Tables

Table 1.1. Abbreviations of quorum-sensing signal molecules. 26

Table 1.2. Plant-associated bacteria that produce autoinducer signal molecules in... 27

Table 1.3. AHL-dependent quorum-sensing system identified in Serratia spp. 29

Table 1.4. Recent findings of direct AHL impact on different plants. 31

Table 2.1. Plant growth-promoting and N-acyl homoserine lactone activities of bacterial isolates 42

Table 2.2. Morphological and biochemical characteristics of Serratia glossinae strain GS2 45

Table 2.3. Effect of Serratia glossinae strain GS2 on plant growth attributes and chlorophyll content 53

Table 3.1. Genome features of Serratia glossinae strain GS2 63

Table 3.2. Average Nucleotide Identity (ANI) analysis. Genome comparison of... 66

Table 4.1. Strains and plasmids 78

Table 4.2. Primers used in this study 80

Table 4.3. Plant growth-promoting and N-acyl homoserine lactone activities of bacterial isolates 99

Table 4.4. Effect of Serratia glossinae GS2 wild-type and mutant strains on plant growth attributes and chlorophyll content 105

Table 4.5. The production of volatile organic compounds by Serratia glossinae strain GS2 wild-type and mutants as measured... 111

Table 4.6. Results of comparing the △gloI and △gloR mutants with their wild-type... 114

Table 4.7. Identification of the intracellular proteins displayed in quorum-sensing gene mutant strains relative to the wild-... 118

Table 4.9. Ion Proton sequencing summary and number of quorum-sensing-... 124

Table 4.10. Differentially expressed transcripts of plant growth promotion-related gene between wild-type and mutants. 126

Table 4.11. Differentially expressed transcripts of autoinducer type 2-related gene between wild-type and mutants. 127

Table 4.12. Differentially expressed transcripts of biofilm formation-related gene between wild-type and mutants. 128

Table 4.13. Differentially expressed transcripts of motility-related gene between wild-type and mutants. 129

Table 5.1. Effect of N-acyl homoserine lactones on plant growth attributes and chlorophyll content at 1st generation. 146

Table 5.2. Effect of N-acyl homoserine lactones on plant growth attributes and chlorophyll content at 2nd generation. 147

Table 5.3. Effect of N-acyl homoserine lactones on plant growth attributes and chlorophyll content at 3rd generation. 148

Table 5.4. Ion Torrent PGM sequencing data summary. 151

Table 5.5. Richness and diversity estimates of the bacterial community libraries constructed from the rice rhizospheric soil... 152

Table 5.6. Ion Proton sequencing summary. 163

Table. 5.7. Annotation of quorum-sensing-related genes by KEGG classification. 167

List of Figures

Fig. 1.1. Schematic representation of rhizosphere and rhizoplane. 13

Fig. 1.2. Plant root exudates mediate a multitude of rhizospheric interactions... 15

Fig. 1.3. Tryptophan-dependent auxin biosynthetic pathways in PGPR. 18

Fig. 1.4. Proposed model for the regulation of ethylene in the plant by a PGPR that... 20

Fig. 2.1. Phylogenetic tree showing the phylogenetic position of strain GS2 in... 43

Fig. 2.2. Scanning electron micrograph showing the morphological structure and... 47

Fig. 2.3. Gas chromatography (GC)/mass spectrometry analysis of indole-3-acetic... 49

Fig. 2.4. Thin layer chromatography bioassay (A) and LC-MS/MS analysis (B) of... 51

Fig. 2.5. Effect of Serratia glossinae strain GS2 on the growth attributes of rice... 54

Fig. 3.1. Circular map of the chromosome and the two plasmids of Serratia... 64

Fig. 3.2. Circular representation of Serratia glossinae strain GS2. The figure was... 65

Fig. 3.3. Gene map showing organization of gloR (luxR homolog) and gloI (luxI... 68

Fig. 3.4. Phylogenetic tree of GloI. Neighbor-Joining method was used in MEGA6... 69

Fig. 3.5. Phylogenetic tree of GloR. Neighbor-Joining method was used in MEGA6... 69

Fig. 3.6. Metabolic pathways involved in indole-3-acetic acid present in Serratia... 71

Fig. 3.7. Metabolic pathway to acetoin and 2,3-butanediol in Serratia glossinae... 72

Fig. 4.1. Verification of markerless deletion mutants with agarose gel... 96

Fig. 4.2. Plant growth-promoting related phenotype analysis. Growth curves (A)... 100

Fig. 4.3. Gas chromatography (GC)/mass spectrometry analysis of indole-3-acetic... 101

Fig. 4.4. Voges-Proskauer (A) and methyl red (B) reaction of Serratia glossinae... 102

Fig. 4.5. Swimming motility of Serratia glossinae GS2 wild-type, △gloI and △gloR... 103

Fig. 4.6. Effect of Serratia glossinae GS2 wild-type and mutant strains on the growth of rice plants (Waito-c) after 3 weeks... 106

Fig. 4.7. The effect of the volatile compounds of Serratia glossinae strain GS2 wild-... 108

Fig. 4.8. The plant growth modulating effects of volatile compounds from Serratia... 109

Fig. 4.9. Serratia glossinae strain GS2 wild-type and mutants were subjected to... 113

Fig. 4.10. The cluster heatmap showing the average area values of Serratia... 115

Fig. 4.11. Comparative 2-DE of intracellular proteins in Serratia glossinae GS2 wild-type (A), △gloI (8), and △gioR (C)... 117

Fig. 4.12. Agarose gel electrophoresis of RNA extracted from Serratia glossinae... 120

Fig. 4.13. Agarose gel electrophoresis of 16S rRNA gene PCR products using RNA... 121

Fig. 4.14. Agarose gel electrophoresis of double-strand cDNA synthesized by... 122

Fig. 4.15. Volcano plot distribution of the transcriptome data. A, volcano plot... 125

Fig. 4.16. Cluster analysis heat map. The heat map shown in graphical form the... 131

Fig. 4.17. Annotation of the Serratia glossinae GS2 wild-type and mutant strains transcriptome by KEGG classification.... 132

Fig. 5.1. Experimental design of multi-generation plant growth. Sterilized sand was... 138

Fig. 5.2. Effect of N-acyl homoserine lactones on the growth of rice plants. A, 1st... 144

Fig. 5.3. Effect of N-acyl homoserine lactones on plant growth attributes and chlorophyll content. A, shoot length; B, root... 145

Fig. 5.4. Rarefaction curves from the 16S rRNA libraries constructed at each time... 150

Fig. 5.5. Relative abundances of the most abundant phyla in the rice rhizospheric... 155

Fig. 5.6. Relative abundances of the most abundant class in the rice rhizospheric... 156

Fig. 5.7. Cluster analysis heat map drawn by classified predominant genus. The... 157

Fig. 5.8. Number of observed taxonomic units in the 1st, 2nd, and 3rd generation... 158

Fig. 5.9. Principal-coordinate analysis (PCoA) plot of rhizobacterial community... 159

Fig. 5.10. Agarose gel electrophoresis of soil RNA extracted from rhizospheric soil... 161

Fig. 5.11. Agarose gel electrophoresis of double-strand cDNA synthesized by soil... 161

Fig. 5.12. Annotation of the meta-transcriptome by KEGG classification. Total transcript were subjected to KEGG... 164

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