Abstract
Key message
Different responses are elicited in tomato plants by Bactericera cockerelli harboring or not the pathogen ‘Candidatus Liberibacter solanacearum’.
Abstract
‘Candidatus Liberibacter solanacearum’ (Lso) has emerged as a major pathogen of crops worldwide. This bacterial pathogen is transmitted by Bactericera cockerelli, the tomato psyllid, to solanaceous crops. In this study, the transcriptome profiles of tomato (Solanum lycopersicum) exposed to B. cockerelli infestation and Lso infection were evaluated at 1, 2 and 4 weeks following colonization and/or infection. The plant transcriptional responses to Lso-negative B. cockerelli were different than plant responses to Lso-positive B. cockerelli. The comparative transcriptome analyses of plant responses to Lso-negative B. cockerelli revealed the up-regulation of genes associated with plant defenses regardless of the time-point. In contrast, the general responses to Lso-positive B. cockerelli and Lso-infection were temporally different. Infected plants down-regulated defense genes at week one while delayed the up-regulation of the defense genes until weeks two and four, time points in which early signs of disease development were also detected in the transcriptional response. For example, infected plants regulated carbohydrate metabolism genes which could be linked to the disruption of sugar distribution usually associated with Lso infection. Also, infected plants down-regulated photosynthesis-related genes potentially resulting in plant chlorosis, another symptom associated with Lso infection. Overall, this study highlights that tomato plants induce different sets of genes in response to different stages of B. cockerelli infestation and Lso infection. This is the first transcriptome study of tomato responses to B. cockerelli and Lso, a first step in the direction of finding plant defense genes to enhance plant resistance.
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Acknowledgements
This material is based upon work supported by the NIFA-AFRI Grant 2012-67013-19431. Ordom Huot is supported by the Texas A&M University Diversity Fellowship and the National Science Foundation Graduate Research Fellowship under Grant No. 1252521. We thank Dr. Azucena Mendoza, Dr. Kyle Harrison, Dr. Elizabeth Pierson and Dr. Punya Nachappa for their assistance.
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OH, JL and CT designed the experiments. OH performed the experiments and analyzed data. OH, JL and CT wrote the manuscript.
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Supplementary Document 1
List of parameters used for the bioinformatics analyses. Supplementary material 1 (PDF 6 KB)
Supplementary Table 1
Primers for genes of interest. Supplementary material 2 (PDF 39 KB)
Supplementary Table 2
Summary of the transcriptomic data. Reads were mapped to the Solanum lycopersicum genome. C: control plants. P: plants infested with Lso-negative B. cockerelli. L: plants infested with Lso-positive B. cockerelli. C and P plants tested negative for Lso. L plants tested positive for Lso. T1, T2, and T3 represent one, two, and four weeks after infestation, respectively. * mark the libraries sequenced with 125PE. Supplementary material 3 (PDF 18 KB)
Supplementary Table 3
List of significantly differentially expressed genes (DEGs) in C vs P comparison. Time represents time point as indicated in methods. q-value indicates the adjusted p-value after the Benjamini-Hochberg correction for multiple comparison. C: control plants and P: plants infested with Lso-negative B. cockerelli. C and P plants tested negative for Lso. Supplementary material 4 (PDF 126 KB)
Supplementary Table 4
List of significantly differentially expressed genes (DEGs) in C vs L comparison. Time represents time point as indicated in the method. q-value indicates the adjusted p-value after the Benjamini-Hochberg correction for multiple comparison. C: control plants and L: plants infested with Lso-positive B. cockerelli. C plants tested negative for Lso. L plants tested positive for Lso. Supplementary material 5 (PDF 216 KB)
Supplementary Table 5
List of significantly differentially expressed genes (DEGs) in P vs L comparison. Time represents time point as indicated in the method. q-value indicates the adjusted p-value after the Benjamini-Hochberg correction for multiple comparison. P: plants infested with Lso-negative B. cockerelli and L: plants infested with Lso-positive B. cockerelli. P plants tested negative for Lso. L plants tested positive for Lso. Supplementary material 6 (PDF 191 KB)
Supplementary Table 6
Significantly enriched gene ontology (GO) terms associated with the up- and down-regulated genes in the C vs P comparative transcriptomes. C: control plants. P: plants infested with Lso-negative B. cockerelli. NA = not applicable. P-value was adjusted for multiple comparisons by the Holm-Bonferroni method. Biological process (BP). Cellular component (CC). Molecular function (MF). Supplementary material 7 (PDF 70 KB)
Supplementary Table 7
Significantly enriched gene ontology (GO) terms associated with the up- and down-regulated genes in the C vs L comparative transcriptomes. C: control plants. L: plants infested with Lso-positive B. cockerelli. NA = not applicable. P-value was adjusted for multiple comparisons by the Holm-Bonferroni method. Biological process (BP). Cellular component (CC). Molecular function (MF). Supplementary material 8 (PDF 55 KB)
Supplementary Table 8
Significantly enriched gene ontology (GO) terms associated with the up- and down-regulated genes in the P vs L comparative transcriptomes. P: plants infested with Lso-negative B. cockerelli. L: plants infested with Lso-positive B. cockerelli. NA = not applicable. P-value was adjusted for multiple comparisons by the Holm-Bonferroni method. Biological process (BP). Cellular component (CC). Molecular function (MF). Supplementary material 9 (PDF 51 KB)
Supplementary Table 9
List of significantly differentially expressed genes (DEGs) involved in plant defense, photosynthesis, and sugar metabolism identified in the comparative transcriptomes. C: control plants. P: plants infested with Lso-negative B. cockerelli. L: plants infested with Lso-positive B. cockerelli. For each DEG the log2(Fold change) is reported. NS: Not significant. Supplementary material 10 (PDF 98 KB)
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Huot, O.B., Levy, J.G. & Tamborindeguy, C. Global gene regulation in tomato plant (Solanum lycopersicum) responding to vector (Bactericera cockerelli) feeding and pathogen (‘Candidatus Liberibacter solanacearum’) infection. Plant Mol Biol 97, 57–72 (2018). https://doi.org/10.1007/s11103-018-0724-y
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DOI: https://doi.org/10.1007/s11103-018-0724-y