Comparison of Tomato Transcriptomic Profiles Reveals Overlapping Patterns in Abiotic and Biotic Stress Responses.

Until a few years ago, many studies focused on the transcriptomic response to single stresses. However, tomato cultivations are often constrained by a wide range of biotic and abiotic stress that can occur singularly or in combination, and several genes can be involved in the defensive mechanism response. Therefore, we analyzed and compared the transcriptomic responses of resistant and susceptible genotypes to seven biotic stresses (Cladosporium fulvum, Phytophthora infestans, Pseudomonas syringae, Ralstonia solanacearum, Sclerotinia sclerotiorum, Tomato spotted wilt virus (TSWV) and Tuta absoluta) and five abiotic stresses (drought, salinity, low temperatures, and oxidative stress) to identify genes involved in response to multiple stressors. With this approach, we found genes encoding for TFs, phytohormones, or participating in signaling and cell wall metabolic processes, participating in defense against various biotic and abiotic stress. Moreover, a total of 1474 DEGs were commonly found between biotic and abiotic stress. Among these, 67 DEGs were involved in response to at least four different stresses. In particular, we found RLKs, MAPKs, Fasciclin-like arabinogalactans (FLAs), glycosyltransferases, genes involved in the auxin, ET, and JA pathways, MYBs, bZIPs, WRKYs and ERFs genes. Detected genes responsive to multiple stress might be further investigated with biotechnological approaches to effectively improve plant tolerance in the field.

Genomic and metabolic profiling of two tomato contrasting cultivars for tolerance to Tuta absoluta.

MAIN CONCLUSION: Dissimilar patterns of variants affecting genes involved in response to herbivory, including those leading to difference in VOC production, were identified in tomato lines with contrasting response to Tuta absoluta. Tuta absoluta is one of the most destructive insect pest affecting tomato production, causing important yield losses both in open field and greenhouse. The selection of tolerant varieties to T. absoluta is one of the sustainable approaches to control this invasive leafminer. In this study, the genomic diversity of two tomato varieties, one tolerant and the other susceptible to T. absoluta infestation was explored, allowing us to identify chromosome regions with highly dissimilar pattern. Genes affected by potential functional variants were involved in several processes, including response to herbivory and secondary metabolism. A metabolic analysis for volatile organic compounds (VOCs) was also performed, highlighting a difference in several classes of chemicals in the two genotypes. Taken together, these findings can aid tomato breeding programs aiming to develop tolerant plants to T. absoluta.

Multilevel evolution shapes the function of NB-LRR encoding genes in plant innate immunity.

A sophisticated innate immune system based on diverse pathogen receptor genes (PRGs) evolved in the history of plant life. To reconstruct the direction and magnitude of evolutionary trajectories of a given gene family, it is critical to detect the ancestral signatures. The rearrangement of functional domains made up the diversification found in PRG repertoires. Structural rearrangement of ancient domains mediated the NB-LRR evolutionary path from an initial set of modular proteins. Events such as domain acquisition, sequence modification and temporary or stable associations are prominent among rapidly evolving innate immune receptors. Over time PRGs are continuously shaped by different forces to find their optimal arrangement along the genome. The immune system is controlled by a robust regulatory system that works at different scales. It is important to understand how the PRG interaction network can be adjusted to meet specific needs. The high plasticity of the innate immune system is based on a sophisticated functional architecture and multi-level control. Due to the complexity of interacting with diverse pathogens, multiple defense lines have been organized into interconnected groups. Genomic architecture, gene expression regulation and functional arrangement of PRGs allow the deployment of an appropriate innate immunity response.

PRGdb 4.0: an updated database dedicated to genes involved in plant disease resistance process.

The Plant Resistance Genes database (PRGdb; http://prgdb.org/prgdb4/) has been greatly expanded, keeping pace with the increasing amount of available knowledge and data (sequenced proteomes, cloned genes, public analysis data, etc.). The easy-to-use style of the database website has been maintained, while an updated prediction tool, more data and a new section have been added. This new section will contain plant resistance transcriptomic experiments, providing additional easy-to-access experimental information. DRAGO3, the tool for automatic annotation and prediction of plant resistance genes behind PRGdb, has been improved in both accuracy and sensitivity, leading to more reliable predictions. PRGdb offers 199 reference resistance genes and 586.652 putative resistance genes from 182 sequenced proteomes. Compared to the previous release, PRGdb 4.0 has increased the number of reference resistance genes from 153 to 199, the number of putative resistance genes from 177K from 76 proteomes to 586K from 182 sequenced proteomes. A new section has been created that collects plant-pathogen transcriptomic data for five species of agricultural interest. Thereby, with these improvements and data expansions, PRGdb 4.0 aims to serve as a reference to the plant scientific community and breeders worldwide, helping to further study plant resistance mechanisms that contribute to fighting pathogens.

Tomato transcriptomic response to Tuta absoluta infestation.

BACKGROUND: The South America pinworm, Tuta absoluta, is a destructive pest of tomato that causes important losses worldwide. Breeding of resistant/tolerant tomato cultivars could be an effective strategy for T. absoluta management but, despite the economic importance of tomato, very limited information is available about its response to this treat. To elucidate the defense mechanisms to herbivore feeding a comparative analysis was performed between a tolerant and susceptible cultivated tomato at both morphological and transcriptome level to highlight constitutive leaf barriers, molecular and biochemical mechanisms to counter the effect of T. absoluta attack. RESULTS: The tolerant genotype showed an enhanced constitutive barrier possibly as result of the higher density of trichomes and increased inducible reactions upon mild infestation thanks to the activation/repression of key transcription factors regulating genes involved in cuticle formation and cell wall strength as well as of antinutritive enzymes, and genes involved in the production of chemical toxins and bioactive secondary metabolites. CONCLUSIONS: Overall, our findings suggest that tomato resilience to the South America pinworm is achieved by a combined strategy between constitutive and induced defense system. A well-orchestrated modulation of plant transcription regulation could ensure a trade-off between defense needs and fitness costs. Our finding can be further exploited for developing T. absoluta tolerant cultivars, acting as important component of integrated pest management strategy for more sustainable production.

Deciphering the biological processes underlying tomato biomass production and composition.

The huge amounts of biomass residues, remaining in the field after tomato fruits harvesting, can be utilized to produce bioenergy. A multiple level approach aimed to characterize two Solanum pennellii introgression lines (ILs), with contrasting phenotypes for plant architecture and biomass was carried out. The study of gene expression dynamics, microscopy cell traits and qualitative and quantitative cell wall chemical compounds variation enabled the discovery of key genes and cell processes involved biomass accumulation and composition. Enhanced biomass production observed in IL2-6 line is due to a more effective coordination of chloroplasts and mitochondria energy fluxes. Microscopy analysis revealed a higher number of cells and chloroplasts in leaf epidermis in the high biomass line whilst chemical measurements on the two lines pointed out striking differences in the cell wall composition and organization. Taken together, our findings shed light on the mechanisms underlying the tomato biomass production and processability.

Adaptive responses along a depth and a latitudinal gradient in the endemic seagrass Posidonia oceanica.

Seagrass meadows provide important ecosystem services and are critical for the survival of the associated invertebrate community. However, they are threatened worldwide by human-driven environmental change. Understanding the seagrasses' potential for adaptation is critical to assess not only their ability to persist under future global change scenarios, but also to assess the persistence of the associated communities. Here we screened a wild population of Posidonia oceanica, an endemic long-lived seagrass in the Mediterranean Sea, for genes that may be target of environmental selection, using an outlier and a genome-wide transcriptome analysis. We identified loci where polymorphism or differential expression was associated with either a latitudinal or a bathymetric gradient, as well as with both gradients in an effort to identify loci associated with temperature and light. We found the candidate genes underlying growth and immunity to be divergent between populations adapted to different latitudes and/or depths, providing evidence for local adaptation. Furthermore, we found evidence of reduced gene flow among populations including adjacent populations. Reduced gene flow, combined with low sexual recombination, small effective population size, and long generation time of P. oceanica raises concerns for the long-term persistence of this species, especially in the face of rapid environmental change driven by human activities.

Unraveling the complexity of transcriptomic, metabolomic and quality environmental response of tomato fruit.

BACKGROUND: The environment has a profound influence on the organoleptic quality of tomato (Solanum lycopersicum) fruit, the extent of which depends on a well-regulated and dynamic interplay among genes, metabolites and sensorial attributes. We used a systems biology approach to elucidate the complex interacting mechanisms regulating the plasticity of sensorial traits. To investigate environmentally challenged transcriptomic and metabolomic remodeling and evaluate the organoleptic consequences of such variations we grown three tomato varieties, Heinz 1706, whose genome was sequenced as reference and two "local" ones, San Marzano and Vesuviano in two different locations of Campania region (Italy). RESULTS: Responses to environment were more pronounced in the two "local" genotypes, rather than in the Heinz 1706. The overall genetic composition of each genotype, acting in trans, modulated the specific response to environment. Duplicated genes and transcription factors, establishing different number of network connections by gaining or losing links, play a dominant role in shaping organoleptic profile. The fundamental role of cell wall metabolism in tuning all the quality attributes, including the sensorial perception, was also highlighted. CONCLUSIONS: Although similar fruit-related quality processes are activated in the same environment, different tomato genotypes follow distinct transcriptomic, metabolomic and sensorial trajectories depending on their own genetic makeup.

Depth-specific fluctuations of gene expression and protein abundance modulate the photophysiology in the seagrass Posidonia oceanica.

Here we present the results of a multiple organizational level analysis conceived to identify acclimative/adaptive strategies exhibited by the seagrass Posidonia oceanica to the daily fluctuations in the light environment, at contrasting depths. We assessed changes in photophysiological parameters, leaf respiration, pigments, and protein and mRNA expression levels. The results show that the diel oscillations of P. oceanica photophysiological and respiratory responses were related to transcripts and proteins expression of the genes involved in those processes and that there was a response asynchrony between shallow and deep plants probably caused by the strong differences in the light environment. The photochemical pathway of energy use was more effective in shallow plants due to higher light availability, but these plants needed more investment in photoprotection and photorepair, requiring higher translation and protein synthesis than deep plants. The genetic differentiation between deep and shallow stands suggests the existence of locally adapted genotypes to contrasting light environments. The depth-specific diel rhythms of photosynthetic and respiratory processes, from molecular to physiological levels, must be considered in the management and conservation of these key coastal ecosystems.

Fusarium oxysporum f.sp. radicis-lycopersici induces distinct transcriptome reprogramming in resistant and susceptible isogenic tomato lines.

BACKGROUND: Fusarium oxysporum f.sp. radicis-lycopersici (FORL) is one of the most destructive necrotrophic pathogens affecting tomato crops, causing considerable field and greenhouse yield losses. Despite such major economic impact, little is known about the molecular mechanisms regulating Fusarium oxysporum f.sp. radicis-lycopersici resistance in tomato. RESULTS: A transcriptomic experiment was carried out in order to investigate the main mechanisms of FORL response in resistant and susceptible isogenic tomato lines. Microarray analysis at 15 DPI (days post inoculum) revealed a distinct gene expression pattern between the two genotypes in the inoculated vs non-inoculated conditions. A model of plant response both for compatible and incompatible reactions was proposed. In particular, in the incompatible interaction an activation of defense genes related to secondary metabolite production and tryptophan metabolism was observed. Moreover, maintenance of the cell osmotic potential after the FORL challenging was mediated by a dehydration-induced protein. As for the compatible interaction, activation of an oxidative burst mediated by peroxidases and a cytochrome monooxygenase induced cell degeneration and necrosis. CONCLUSIONS: Our work allowed comprehensive understanding of the molecular basis of the tomato-FORL interaction. The result obtained emphasizes a different transcriptional reaction between the resistant and the susceptible genotype to the FORL challenge. Our findings could lead to the improvement in disease control strategies.

Genetic diversity and structure in two protected Posidonia oceanica meadows.

Posidonia oceanica meadows growing along the west Mediterranean coastline are under continuous anthropogenic pressure. The way meadow health correlates with genetic and genotypic diversity in P. oceanica, is still under debate. Here we report a microsatellite analysis of two P. oceanica meadows living in protected areas of the Ligurian (Monterosso al Mare, MPA of "Cinque Terre") and central Tyrrhenian Sea (Santa Marinella, regional Site of Community Importance). Both meadows were recently classified as "disturbed", according to shoot density and other phenological parameters. Between the two meadows, Santa Marinella showed higher genetic diversity, while clear genetic substructure was present in both sites, reflecting high spatial heterogeneity. The present study suggests that genetic diversity does not match unequivocally with shoot density and leaf morphology and that small scale intra-meadow heterogeneity is an important factor to consider for establishing the relation between genetic/genotypic variability and health of natural seagrass meadows.