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Global gene regulation in tomato plant (Solanum lycopersicum) responding to vector (Bactericera cockerelli) feeding and pathogen (‘Candidatus Liberibacter solanacearum’) infection

ABSTRACT: ‘Candidatus Liberibacter solanacearum’ (Lso) has emerged as a major pathogen of crops worldwide. This bacterial pathogen is transmitted by Bactericera cockerelli, tomato psyllid, to solanaceous crops. In this study, the transcriptome profiles of Solanum lycopersicum exposed to B. cockerelli infestation and to Lso infection were evaluated at one, two and four weeks following colonization and/or infection. Plant transcriptional response to Lso-negative B. cockerelli was different than plant responses to Lso-positive B. cockerelli. The comparative transcriptomes 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 plant 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 to week two and four, time points in which early signs of disease development were also detected in the transcriptional response. For example, infected plants up-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 genes potentially resulting in plant chlorosis, another symptom associated with Lso infection. Overall, this study highlights that S. lycopersicum plants induced 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.

ORGANISM(S): Solanum lycopersicum

PROVIDER: GSE95710 | GEO | 2019/01/04

REPOSITORIES: GEO

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Project description:The tomato psyllid, Bactericera cockerelli Šulc (Hemiptera: Triozidae), is a pest of solanaceous crops such as tomato (Solanum lycopersicum L.) in the U.S. and vectors the disease-causing pathogen ‘Candidatus Liberibacter solanacearum’ (or Lso). Lso disease symptom severity is dependent on Lso haplotype: tomato plants infected with Lso haplotype B experience more severe symptoms and higher mortality compared to plants infected with Lso haplotype A. By characterizing the molecular differences in the tomato plant’s responses to Lso haplotypes, the key components of LsoB virulence can be identified and, thus, targeted for disease mitigation strategies. To characterize the tomato plant genes putatively involved in the differential immune responses to Lso haplotypes A and B, RNA was extracted from tomato ‘Moneymaker’ leaves three weeks after psyllid infestation. Gene expression levels were compared between uninfected tomato plants (i.e., controls and plants infested with Lso-free psyllids) and infected plants (i.e., plants infested with psyllids infected with either Lso haplotype A or Lso haplotype B). Furthermore, expression levels were compared between plants infected with Lso haplotype A and plants infected with Lso haplotype B. A whole transcriptome analysis identified 578 differentially expressed genes (DEGs) between uninfected and infected plants as well as 451 DEGs between LsoA- and LsoB-infected plants. These DEGs were primarily associated with plant defense against abiotic and biotic stressors, growth/development, plant primary metabolism, transport and signaling, and transcription/translation. These gene expression changes suggested that tomato plants traded off plant growth and homeostasis for improved defense against pathogens, especially when infected with LsoB. Consistent with these results, tomato plant growth experiments determined that LsoB-infected plants were significantly stunted and had impaired negative geotropism. However, it appeared that the defense responses mounted by tomatoes were insufficient for overcoming the disease symptoms and mortality caused by LsoB infection, while these defenses could compensate for LsoA infection. The transcriptomic analysis and growth experiments demonstrated that Lso-infected tomato plants underwent gene expression changes related to abiotic and biotic stressors, impaired growth/development, impaired plant primary metabolism, impaired transport and signaling transduction, and impaired transcription/translation. Furthermore, the transcriptomic analysis also showed that LsoB-infected plants, relative to LsoA-infected, experienced more severe stunting, had improved responses to some stressors and impaired responses to others, had poorer transport and signaling transduction, and had impaired carbohydrate synthesis and photosynthesis.

Project description:BACKGROUND: The tomato psyllid, Bactericera cockerelli Šulc (Hemiptera: Triozidae), is a pest of solanaceous crops such as tomato (Solanum lycopersicum L.) in the U.S. and vectors the disease-causing pathogen ‘Candidatus Liberibacter solanacearum’. Currently, the only effective strategies for controlling the diseases associated with this pathogen involve regular pesticide applications to manage psyllid population density. However, such practices are unsustainable and will eventually lead to widespread pesticide resistance in psyllids. Therefore, new control strategies must be developed to increase host-plant resistance to insect vectors. For example, expression of constitutive and inducible plant defenses can be improved through selection. Currently, it is still unknown whether psyllid infestation has any lasting consequences on tomato plant defense or tomato plant gene expression in general. RESULTS: To characterize the genes putatively involved in tomato defense against psyllid infestation, RNA was extracted from psyllid-infested and uninfested tomato leaves (Moneymaker) three weeks post-infestation. Transcriptome analysis identified 362 differentially expressed genes. These differentially expressed genes were primarily associated with defense responses to abiotic/biotic stress, transcription/translation, cellular signaling/transport, and photosynthesis. These gene expression changes suggested that tomato plants underwent a reduction in plant growth/health in exchange for improved defense against stress that was observable three weeks after psyllid infestation. Consistent with these observations, tomato plant growth experiments determined that the plants were shorter three weeks after psyllid infestation. Furthermore, psyllid nymphs had lower survival rates on tomato plants that had been previously psyllid infested. CONCLUSION: These results suggested that psyllid infestation has lasting consequences for tomato gene expression, defense, and growth.

Project description:Purpose: The tomato psyllid, Bactericera cockerelli Šulc (Hemiptera: Triozidae), is a pest of tomato (Solanum lycopersicum) and potato (S. tuberosum) in the U.S. and vectors the disease-causing pathogen ‘Candidatus Liberibacter solanacearum’. Plants undergo physiological, transcriptomic, or epigenetic changes in order to mount a stronger, faster response against secondary challenges by previously perceived threats. This is called defense ‘priming’ and it likely has an impact on vectored disease transmission. Currently, it is still unknown whether or not psyllid infestation has any lasting consequences for tomato gene expression or defense. To characterize the genes potentially involved in tomato priming against psyllids, RNA was extracted from psyllid-primed and uninfested tomato (Moneymaker) leaves three weeks after infestation. Methods: RNA was extracted and sequenced from plants three weeks after psyllid infestation. Plants were either left alone (Control or C) or infested with psyllids (Primed or J1). Libraries were developed using the TruSeq RNA Library Prep Kit v2. Sequencing was performed on the Illumina PE HiSeq 2500 v4 platform. Processed sequences were uploaded to the CyVerse Discovery Environment computational infrastructure where bioinformatic analysis was performed using the Tuxedo Suite 2 workflow. Results: Illumina HiSeq sequencing of tomato cDNA libraries produced 132,428,443 total reads that met FastQC quality control criteria. 94.6% of all reads mapped to vSL3.0 of the S. lycopersicum genome. CuffDiff2 analysis identified 310 differentially expressed genes (DEGs) between control and psyllid-primed plants (q-value <0.01). Conclusions: A week-long infestation by a small number of B. cockerelli had lasting consequences for gene expression in tomato plants. Homologs of the DEGs were associated with 1) defense against abiotic and biotic stress, 2) growth and development, and 3) components of plant biology indirectly involved in plant growth and development such as homeostasis, transcription/translation, and molecular transport.

Project description:Aphid attack induces defense responses in plants activating several signaling cascades that led to the production of toxic, repellent or antinutritive compounds and the consequent reorganization of the plant primary metabolism. Pepper (Capsicum annuum L.) leaf proteomic response against Myzus persicae (Sulzer) has been investigated and analyzed by LC-MS/MS coupled with bioinformatics tools. Infestation with an initially low density (20 aphids/plant) of aphids restricted to a single leaf taking advantage of clip cages resulted in 6 differentially expressed proteins relative to control leaves (3 proteins at 2 days post-infestation and 3 proteins at 4 days post-infestation). Conversely, when plants were infested with a high density of infestation (200 aphids/plant) 140 proteins resulted differentially expressed relative to control leaves (97 proteins at 2 days post-infestation, 112 proteins at 4 days post-infestation and 105 proteins at 7 days post-infestation). The majority of proteins altered by aphid attack were involved in photosynthesis and photorespiration, oxidative stress, translation, protein folding and degradation and amino acid metabolism. Other proteins identified were involved in lipid, carbohydrate and hormone metabolism, transcription, transport, energy production and cell organization. However proteins directly involved in defense were scarce and were mostly downregulated in response to aphids. The unexpectedly very low number of regulated proteins found in the experiment with a low aphid density suggests an active mitigation of plant defensive response by aphids or alternatively an aphid strategy to remain undetected by the plant. Under a high density of aphids, pepper leaf proteome however changed significantly revealing nearly all routes of plant primary metabolism being altered. Photosynthesis was so far the process with the highest number of proteins being regulated by the presence of aphids. In general, at short times of infestation (2 days) most of the altered proteins were upregulated. However, at longer times of infestation (7 days) the protein downregulation prevailed. Proteins involved in plant defense and in hormone signaling were scarce and mostly downregulated.

Project description:Transcriptomic analysis in response to Botrytis cinerea infections under conrasting nitrate regime Nitrogen (N) is one of the main limiting nutrients for plant growth and crop yield. It is well documented that changes in nitrate availability, the main N source found in agricultural soils, influences a myriad of developmental programs and processes including the plant defense response. Indeed, many agronomical reports indicate that the plant N nutritional status influences their ability to respond effectively when challenged by different pathogens. However, the molecular mechanisms involved in N-modulation of plant susceptibility to pathogens are poorly characterized. In this work, we show that Solanum lycopersicum defense response to the necrotrophic fungus Botrytis cinerea is affected by plant N availability, with higher susceptibility in nitrate-limiting conditions. Global gene expression responses of tomato against B. cinerea under contrasting nitrate conditions reveals that plant primary metabolism is affected by the fungal infection regardless of N regimes. This result suggests that differential susceptibility to pathogen attack under contrasting N conditions is not only explained by a metabolic alteration. We used a systems biology approach to identify the transcriptional regulatory network implicated in plant response to the fungus infection under contrasting nitrate conditions. Interestingly, hub genes in this network are known key transcription factors involved in ethylene and jasmonic acid signaling. This result positions these hormones as key integrators of nitrate and defense against B. cinerea in tomato plants. Our results provide insights into potential crosstalk mechanisms between necrotrophic defense response and N status in plants. To better understand the molecular changes underlying the impact of nitrate availability on plant susceptibility to B. cinerea, we performed plant transcriptome profiling assays on mock-treated (3 biological replicates) and infected plants ( 3 biological replicates) grown under three N conditions, using GeneChip Tomato Genome Arrays (Affymetrix).

Dataset Information

Global gene regulation in tomato plant (Solanum lycopersicum) responding to vector (Bactericera cockerelli) feeding and pathogen (‘Candidatus Liberibacter solanacearum’) infection

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