Transcriptomic Studies of the Effect of nod Gene-Inducing Molecules in Rhizobia: Different Weapons, One Purpose
Abstract
:1. Introduction
2. Rhizobial Transcriptomic Studies Related with Symbiosis
2.1. Bacteroid and Microaerobiosis Conditions
2.2. Rhizosphere and Exudates Conditions
3. Gene Expression Changes under nod Gene-Inducing Molecules: The Arsenal of Weapons
3.1. Bradyrhizobium Japonicum USDA 110: Diversification in the Activation Pathways for NF Production, Assembly of the T3SS and the Flagellum
3.1.1. Genes Controlled by NB
3.1.2. Genes Controlled by TB
3.1.3. Genes Not Preceded by a NB or a TB
3.2. Rhizobium Leguminosarum Biovar Viciae 3841: NF Synthesis and Adaptation to the Rhizosphere Environment
3.2.1. Genes Controlled by NB
3.2.2. Genes Not Preceded by a NB
3.3. Rhizobium Tropici CIAT 899: NF Synthesis Also under Stressing Conditions, Production of a Large Variety of NF and Phytohormones
3.3.1. Genes Controlled by NB
3.3.2. Genes Not Preceded by a NB
3.4. Sinorhizobium Meliloti 1021: Only Production and Export of NF?
3.4.1. Genes Controlled by NB via NodD1
3.4.2. Genes Not Preceded by a NB
3.5. Sinorhizobium Fredii HH103: A Hierarchical Regulatory Cascade Controls NF Production and Export, Biosynthesis of Phytohormones, and Assembly of the T3SS
3.5.1. Genes Controlled by NB via NodD1
3.5.2. Genes Controlled by TB via TtsI
3.5.3. Genes Not Preceded by a NB or a TB
4. Conclusions
Supplementary Materials
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Comparison | Bacteria | Method | Strains | Specific Conditions | Results Related with the Symbiotic Process | References |
---|---|---|---|---|---|---|
Free-living cells vs. Bacteroids | Bradyrhizobium japonicum USDA 110 | Microarray (Affymetrix GeneChip) | Wild-type and RNA polymerase σ54 factor (rpoN1-2) double mutant | -Free-living cultures in either aerobic or microaerobic conditions (mid-exponential phase). -Bacteroids in soybean (10, 13, 21 and 31 days post inoculation, dpi). | -Distinction among genes expressed in early and late bacteroids. -1/3 of the genes induced in bacteroids (21 dpi) are also upregulated in microaerobiosis, including fix and nif genes. The other induced genes are regulated by factors other than O2 limitation. -Determination of genes transcribed in bacteroids in a σ54 (rpoN1)-dependent manner (several fix, nif and hup genes included). | [19] |
B. japonicum USDA 110 | Microarray (Operon Biotechnologies) | Wild-type | -Minimal and rich media (mid-exponential phase). -Osmotic stress conditions (mid-exponential phase). -Bacteroids in soybean (28 dpi). | -15% of the genes of the genome were differentially expressed in bacteroids: N2 fixation (nif and fix) and H2 uptake (hup) genes up-regulated. Nodulation (nod) genes also up-regulated. T3SS (hrc) genes are repressed. | [33] | |
Rhizobium leguminosarum biovar viciae 3841 | Microarray (Operon Biotechnologies) | Wild-type | -Several carbon substrates (glucose, pyruvate, succinate, inositol, acetate, and acetoacetate). -Bacteroids in vetch (28 dpi). -Bacteroids in pea (7, 15, 21 and 28 dpi). | -386 genes were differentially expressed in at least one stage of bacteroid development. -The decarboxylating arm of the tricarboxylic acid cycle and the aminobutyrate metabolism were highly induced in early nodule bacteroids (7 dpi). -Changes in the expression of regulators, exported and cell surface molecules, multidrug exporters, and heat and cold shock proteins in bacteroids of early pea nodules (7 dpi). -The fix genes were induced early but continued to increase in mature bacteroids (15 and 21 dpi), while nif genes were induced strongly in older bacteroids of pea nodules (28 dpi). | [34] | |
Mesorhizobium huakuii 7653R | RNA-Seq Microarray (Roche NimbleGen) | Wild-type | -Bacteroids in Astragalus sinicus (32 dpi). | -Mostly, bacteroid up-regulated genes are located on plasmid while downregulated genes are chromosomal. -Free-living cells have a primary role in maintaining basal metabolism, whereas bacteroids in N2 fixation (nif, fix and suf clusters up-regulated). -Up-regulation of rpoN (σ54) and rpoH (RNA polymerase σ32 factor) indicates an essential role of both transcriptional factors in the activation of genes implied in the N2 fixation. | [35] | |
Mesorhizobium loti MAFF303099 | Microarray (Made by Authors) | Wild-type | -Free-living cultures in either aerobic or microaerobic conditions (mid-exponential phase). -Bacteroids in Lotus japonicus (42 dpi). -C-starving conditions. | -Clusters of genes within the symbiotic islands are collectively up-regulated in bacteroids (including nif, fix, fdx, and rpoN genes) through σ54 (rpoN). -Most of the upregulated genes in bacteroids are induced in a NifA-independent manner. -Transcription outside the symbiotic island is strongly repressed in bacteroids (genes implied in cell division, cell wall and flagella synthesis). | [20] | |
Sinorhizobium meliloti 1021 | Macroarrays (Made by authors) | Wild-type and bacA mutant | -Free-living cultures (minimal and rich media) with and without luteolin. -Free-living cultures in either aerobic or microaerobic conditions. -Bacteroids in young (8 dpi) nodules and in mature nitrogen-fixing nodules (18 dpi) in Medicago truncatula. -Bacteroids in Medicago sativa mature nodules (18 dpi). | -15 out of 214 tested genes were induced in young and mature nodules of the two strains (specific of the infection stage), including genes that code for hemolysin calcium-binding proteins, adenylate cyclases and type-IV secretion system proteins. -24 out of 214 tested genes were up-regulated in mature nodules of both plants (specific of symbiosis), including nif, fix and cya genes. -18 out of 214 tested genes were down-regulated in mature nodules of both plants (specific of symbiosis), including genes implied in cell division (ftsZ) and chaperonins. | [36] | |
S. meliloti 1021 | Microarray and Macroarray (Made by authors) | Wild-type | -Free-living cultures in either aerobic or microaerobic conditions. -Bacteroids from M. sativa nodules (18 to 22 dpi). | -982 genes differentially expressed in bacteroids. -Genes downregulated were implied in cell division (ftsZ), DNA, RNA and protein metabolisms (dna and rpo cluster genes), motility and chemotaxis (che genes), phosphorus uptake and utilization (pho genes), nitrogen assimilation (gln genes) and glucolysis and aerobic respiration (nuoACEFHIKLMN operon). -Genes upregulated included mainly those related with symbiosis (several nod and noe genes), nitrogen fixation (nif and fix operons) and transport of peptides and aminoacids. | [18] | |
S. meliloti 1021 | Microarray (Made by authors) | Wild-type and bacA mutant | -Free-living cultures in early and late exponential and stationary phase. -Bacteroids from M. sativa nodules at 5, 8, 14–18 dpi in the wild-type. -Bacteroids from M. sativa nodules at 11 dpi in the mutant. | -36 genes were specifically induced in early stages of the symbiosis (nod genes and genes implied in the synthesis of the cytochrome c). -Bacterial transcriptomic profile changes during nodule development. -The nif and fix cluster genes were up-regulated even in young nodules. | [37] | |
S. meliloti 1021 | Microarray (Affymetrix GeneChip) | Wild-type, triple nodD1 nodD2 nodD3 mutant, rpoN and fixJ mutants, and triple nodD1 nodD2 nodD3 mutant overexpressing either nodD1 or nodD3 | -Minimal and rich media (mid-exponential phase). -Late exponential cultures diluted to 0.15–0.2 OD600 and induced for 4 h with luteolin. -Bacteroids from M. truncatula nodules at 33–35 dpi. | -RpoN controlled genes that are not differentially expressed in free-living bacteria (fdx, nif and fix operons). -Study of gene expression simultaneously in both symbiotic partners indicate that in total more than 5000 genes are differentially expressed in both organisms. -Most of the plant genes upregulated in wild-type nodules were also induced in Fix− nodules (fixJ mutant), indicating that the nitrogen fixing status does not significantly affect plant transcriptomic changes. | [38] | |
S. meliloti 1021 | Microarray (Made by authors) | Wild-type and and fixJ, nifA, fixK, and nifH mutants | -Free-living cultures in either aerobic or microaerobic conditions. -Bacteroids from M. truncatula nodules at 14 dpi. | -122 genes were activated by FixJ via NifA and FixK (97% located in the symbiotic plasmid), including fix and nif genes. -FixJ controls the majority of genes expressed in mature bacteroids. -NifA activated genes implied in nitrogen fixation and exopolysaccharides (EPS) production and FixK up-regulated genes involved in respiration, arginine metabolism, denitrification and stress responses. | [39] | |
S. meliloti 2011 | RNA-seq (Illumina Hiseq 2000) | Wild-type and rpoE2 mutant | -Free-living cultures in mid-exponential or early stationary phase. -Bacteroids from M. truncatula nodules at 10 dpi. | -Authors designed EuGene-P, a tool that enables the automated prediction of coding sequences, untranslated regions, transcription start sites and non-coding RNA genes. -Prediction of 6308 coding sequences, 1876 non-coding RNAs and 4077 transcription start sites using cDNA of all conditions. | [10] | |
S. meliloti 2011 | RNA-seq (Illumina Hiseq 2000) | Wild-type | -Bacteroids from M. truncatula nodules at 10 and 15 dpi. | -Coupling bacterial and plant gene transcriptome determination to laser dissection, authors determined expression changes at the tissue level on indeterminate nodules. | [40] | |
Sinorhizobium fredii NGR234 | RNA-seq (Illumina Hiseq 2000) | Wild-type | -Bacteroids from Vigna unguiculata nodules (21 dpi nodules) -Bacteroids from Leucaena leucocephala (35 dpi nodules). | -3143 genes differentially expressed in bacteroids of V. unguiculata and 2780 in bacteroids of L. leucocephala. -Upregulated genes in bacteroids from both hosts were implied in the synthesis of ATP-binding cassette (ABC) transporters, type 3 secretion system (T3SS), nitrogen metabolism, nitrogen fixation (nif and fix operons), fatty acid metabolism, benzoate degradation and exopolysaccharide biosynthesis (exo cluster genes). -Downregulated genes in bacteroids of both plants were involved in synthesis of DNA, RNA and protein metabolisms and flagellar assembly. | [41] | |
Aerobiosis (Free-living cells) vs. Microaerobiosis | B. japonicum USDA 110 | Microarray (Affymetrix GeneChip) | Wild-type and rpoN1-2 double mutant | -Free-living cultures in either aerobic or microaerobic conditions. -Bacteroids in soybean (10, 13, 21 and 31 dpi). | -Microaerobiosis triggered upregulation of symbiotic relevant genes, including fix and nif clusters, mostly in a σ54-dependent manner. -1/3 of the genes induced in bacteroids (21 dpi) are also upregulated in microaerobic conditions. | [19] |
M. loti MAFF303099 | Microarray (Made by authors) | Wild-type | -Free-living cultures in either aerobic or microaerobic conditions. -Bacteroids in L. japonicus MG20 (42 dpi). -C-starved cells. | -The genome region containing the fixNOPQ genes (outside the symbiosis island) and the fix and nif regions (in the symbiotic island) were upregulated as under both microaerobic and symbiotic conditions. | [20] | |
S. meliloti 021 | Macroarrays (Made by authors) | Wild-type and bacA mutant | -Free-living cultures (minimal and rich media) with and without luteolin. -Free-living cultures in either aerobic or microaerobic conditions. -Bacteroids in young (8 dpi) nodules and in mature nitrogen-fixing nodules (18 dpi) in M. truncatula J6. -Bacteroids in M. sativa mature nodules (18 dpi). | -8 out of 214 tested genes were found to be induced under microoxic and bacteroids conditions, including fix and nif genes. | [36] | |
S. meliloti 1021 | Microarray (Made by authors) | Wild-type and and fixJ, nifA, fixK, and nifH mutants | -Free-living cultures in either aerobic or microaerobic conditions (mid-exponential phase). -Bacteroids from M. truncatula nodules at 14 dpi. | -FixJ controlled 74% of the genes induced in microaerobiosis and the majority of genes expressed in mature bacteroids (including fix and nif genes). | [39] | |
S. meliloti 1021 | Microarray and Macroarray (Made by authors) | Wild-type | -Free-living cultures in either aerobic or microaerobic conditions. -Bacteroids from M. sativa nodules (18 to 22 dpi). | -377 genes regulated by oxygen concentration (266 induced and 111 repressed in microaerobic conditions). -31 genes were induced both under microoxic and bacteroids conditions, including genes implied in N2-fixation (nif and fix operons), proline metabolism and denitrification. | [18] | |
Free-living cells vs. Rhizosphere | R. leguminosarum biovar viciae 3841 | Microarray (Operon Biotechnologies) | Wild-type and mutants in many different genes | -Free-living cells vs. rhizosphere (pea, alfalfa or sugar beet) attached bacteria (7 dpi). -Free-living cultures with and without root exudates (pea). -Free-living cultures with and without the flavonoid hesperetin. | -A common core of 106 genes were rhizosphere-induced genes (70 genes encode for proteins with unknown functions). -The increase of gene expression of the glyoxylate cycle only occurred in the pea rhizosphere. -Many genes on pRL8 (plasmid 8 of R. leguminosarum) were specifically up-regulated in the pea rhizosphere. | [42] |
Non-induced (Free-living cells) vs. root secretions | R. leguminosarum biovar viciae 3841 | Microarray (Operon Biotechnologies) | Wild-type and mutants in many different genes | -Free living cells vs. rhizosphere (pea, alfalfa or sugar beet) attached bacteria (7 dpi).-Free-living cultures with and without root exudates (pea). -Free-living cultures with and without the flavonoid hesperetin. | -21 genes up-regulated including the nodulation (nod) and rhi gene clusters on pRL10 (the symbiotic plasmid). | [42] |
Non-induced (Free-living cells) vs. flavonoids | B. japonicum USDA 110 | Microarray (Affymetrix GeneChip) | Wild-type, nodW mutant and nodW mutant overexpressing nwsB | -Free-living cultures with and without genistein (8 hpi). | -101 genes up-regulated in the presence of genistein, including nod genes, the flagellar cluster and transport genes. -NodW was essencial for induction of most of these genes. -The phenotype and the gene expression levels in the nodW mutant were partially restored by overexpression of nwsB gene. | [43] |
R. leguminosarum biovar viciae 3841 | Microarray (Operon Biotechnologies) | Wild-type and mutants in many different genes | -Free-living cells vs. rhizosphere (pea, alfalfa or sugar beet) attached bacteria (7 dpi). -Free-living cultures with and without root exudates (pea). -Free-living cultures with and without the flavonoid hesperetin. | -27 genes up-regulated in the presence of flavonoids, including the nod and rhi gene clusters on pRL10 (the symbiotic plasmid). -6 genes down-regulated, including flaD. | [42] | |
Rhizobium tropici CIAT 899 | RNA-seq (Illumina Hiseq 2000) | Wild-type, nodD1 mutant and nodD2 mutant | -Free-living cultures with and without the flavonoid apigenin. -Free-living cultures with and without salt. | -13 symbiotic-related genes up-regulated in the presence of apigenin, including nod genes and the IAA synthesis genes. -2 hypothetical-protein genes putatively related with symbiosis were up-regulated via NodD1 and apigenin. -NodD1 activated the expression of the 13 symbiotic-related found genes. | [44,45] | |
S. meliloti 1021 | Macroarrays (Made by authors) | Wild-type and bacA mutant | -Free-living cultures (minimal and rich media) with and without the flavonoid luteolin. -Aerobic and microaerobic conditions. -Bacteroids in young (8 dpi) nodules and in mature nitrogen-fixing nodules (18 dpi) in M. truncatula J6. -Bacteroids in M. sativa mature nodules (18 dpi). | -7 out of the 214 tested genes were induced with luteolin, including the nod genes, traA and three genes related to iron metabolism (also in nodules). | [36] | |
S. meliloti 1021 | Microarray (Made by authors) | Wild-type and wild-type overexpressing nodD1 | -Late exponential cultures diluted to 0.15–0.2 OD600 and induced for 4 and 24 h with luteolin. | -26 and 5 genes after 4 and 24 h, respectively, were affected in the presence of genistein, including those belonging to nod/nol/noe operons. -Other genes encoding for hyphotetical proteins were also identified (varying among replicates). | [46] | |
S. meliloti 1021 | Microarray (Affymetrix GeneChip) | Wild-type, triple nodD1 nodD2 nodD3 mutant, rpoN and fixJ mutants, and triple nodD1 nodD2 nodD3 mutant overexpressing either nodD1 or nodD3 | -Minimal and rich media (mid-exponential phase). -Late exponential cultures diluted to 0.15–0.2 OD600 and induced for 4 h with luteolin.-Bacteroids from M. truncatula nodules at 33–35 dpi. | -Luteolin induced significant expression changes in nod/nol/noe operons (12 genes). -Other 12 genes did not show true flavonoid induction but instead vary in expression depending on replicate. | [38] | |
Sinorhizobium fredii HH103 | RNA-seq (Illumina Hiseq 2000) | Wild-type, nodD1 and ttsI mutants | -Free-living cultures (early stationary phase) with and without the flavonoid genistein. | -100 genes were affected in the presence of genistein: 70 genes induced through nod boxes (nod, nol and noe genes) and tts boxes (T3SS genes) were upregulated. 30 genes not controlled by NB or TB were differentially expressed in the presence of genistein. | [47] | |
Non-induced (Free-living cells) vs. saline stress (nod gene inducing conditions) | R. tropici CIAT 899 | RNA-seq (Illumina Hiseq 2000) | Wild-type, nodD1 mutant and nodD2 mutant | -Free-living cultures with and without the flavonoid apigenin. -Free-living cultures with and without salt. | -17 symbiotic-related genes up-regulated in the presence of salt, including nod genes and the IAA synthesis genes. -All the symbiotic-related genes upregulated in presence of apigenin are upregulated in salt conditions as well. -2 hypothetical-protein genes putatively related with symbiosis were upregulated via NodD2 and salt. -In general, higher nod gene expression was detected with salt than with apigenin. -NodD2 activated the expression of the 17 symbiotic-related found genes. -NodD1 enhanced the expression of nodD2 under salt conditions. | [44,45] |
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Jiménez-Guerrero, I.; Acosta-Jurado, S.; Del Cerro, P.; Navarro-Gómez, P.; López-Baena, F.J.; Ollero, F.J.; Vinardell, J.M.; Pérez-Montaño, F. Transcriptomic Studies of the Effect of nod Gene-Inducing Molecules in Rhizobia: Different Weapons, One Purpose. Genes 2018, 9, 1. https://doi.org/10.3390/genes9010001
Jiménez-Guerrero I, Acosta-Jurado S, Del Cerro P, Navarro-Gómez P, López-Baena FJ, Ollero FJ, Vinardell JM, Pérez-Montaño F. Transcriptomic Studies of the Effect of nod Gene-Inducing Molecules in Rhizobia: Different Weapons, One Purpose. Genes. 2018; 9(1):1. https://doi.org/10.3390/genes9010001
Chicago/Turabian StyleJiménez-Guerrero, Irene, Sebastián Acosta-Jurado, Pablo Del Cerro, Pilar Navarro-Gómez, Francisco Javier López-Baena, Francisco Javier Ollero, José María Vinardell, and Francisco Pérez-Montaño. 2018. "Transcriptomic Studies of the Effect of nod Gene-Inducing Molecules in Rhizobia: Different Weapons, One Purpose" Genes 9, no. 1: 1. https://doi.org/10.3390/genes9010001