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In tomato, sugar content is highly correlated with consumer preferences, with most consumers preferring sweeter fruit 1 – 4 . However, the sugar content of commercial varieties is generally low, as it is inversely correlated with fruit size, and growers prioritize yield over flavour quality 5 – 7 . Here we identified two genes, tomato ( Solanum lycopersicum ) calcium-dependent protein kinase 27 (Sl CDPK27 ; also known as Sl CPK2 7) and its paralogue Sl CDPK26 , that control fruit sugar content. They act as sugar brakes by phosphorylating a sucrose synthase, which promotes degradation of the sucrose synthase. Gene-edited Sl CDPK27 and Sl CDPK26 knockouts increased glucose and fructose contents by up to 30%, enhancing perceived sweetness without fruit weight or yield penalty. Although there are fewer, lighter seeds in the mutants, they exhibit normal germination. Together, these findings provide insight into the regulatory mechanisms controlling fruit sugar accumulation in tomato and offer opportunities to increase sugar content in large-fruited cultivars without sacrificing size and yield. A study identifies two genes that act as brakes controlling the sugar content of tomatoes and demonstrates their manipulation to generate sweeter tomatoes without affecting the fruit size and yield.

Survival biomass production and crop yield are heavily constrained by a wide range of environmental stresses. Several phytohormones among which abscisic acid (ABA), ethylene and salicylic acid (SA) are known to mediate plant responses to these stresses. By contrast, the role of the plant hormone auxin in stress responses remains so far poorly studied. Auxin controls many aspects of plant growth and development, and Auxin Response Factors play a key role in the transcriptional activation or repression of auxin-responsive genes through direct binding to their promoters. As a mean to gain more insight on auxin involvement in a set of biotic and abiotic stress responses in tomato, the present study uncovers the expression pattern of SlARF genes in tomato plants subjected to biotic and abiotic stresses. In silico mining of the RNAseq data available through the public TomExpress web platform, identified several SlARFs as responsive to various pathogen infections induced by bacteria and viruses. Accordingly, sequence analysis revealed that 5' regulatory regions of these SlARFs are enriched in biotic and abiotic stress-responsive cis-elements. Moreover, quantitative qPCR expression analysis revealed that many SlARFs were differentially expressed in tomato leaves and roots under salt, drought and flooding stress conditions. Further pointing to the putative role of SlARFs in stress responses, quantitative qPCR expression studies identified some miRNA precursors as potentially involved in the regulation of their SlARF target genes in roots exposed to salt and drought stresses. These data suggest an active regulation of SlARFs at the post-transcriptional level under stress conditions. Based on the substantial change in the transcript accumulation of several SlARF genes, the data presented in this work strongly support the involvement of auxin in stress responses thus enabling to identify a set of candidate SlARFs as potential mediators of biotic and abiotic stress responses.

Tomato is one of the major vegetable crops consumed worldwide. Tomato yellow leaf curl virus (TYLCV) and fungal Oidium sp. are devastating pathogens causing yellow leaf curl disease and powdery mildew. Such viral and fungal pathogens reduce tomato crop yields and cause substantial economic losses every year. Several commercial tomato varieties include Ty-5 (SlPelo) and Mildew resistance locus o 1 (SlMlo1) locus that carries the susceptibility (S-gene) factors for TYLCV and powdery mildew, respectively. The clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein (Cas) is a valuable genome editing tool to develop disease-resistant crop varieties. In this regard, targeting susceptibility factors encoded by the host plant genome instead of the viral genome is a promising approach to achieve pathogen resistance without the need for stable inheritance of CRISPR components. In this study, the CRISPR/Cas9 system was employed to target the SlPelo and SlMlo1 for trait introgression in elite tomato cultivar BN-86 to confer host-mediated immunity against pathogens. SlPelo-knockout lines were successfully generated, carrying the biallelic indel mutations. The pathogen resistance assays in SlPelo mutant lines confirmed the suppressed accumulation of TYLCV and restricted the spread to non-inoculated plant parts. Generated knockout lines for the SlMlo1 showed complete resistance to powdery mildew fungus. Overall, our results demonstrate the efficiency of the CRISPR/Cas9 system to introduce targeted mutagenesis for the rapid development of pathogen-resistant varieties in tomato.

Nucleotide-binding leucine-rich repeat (NLR) proteins play a pivotal role in plant immunity by recognizing pathogen effectors 1 , 2 . Maintaining a balanced immune response is crucial, as excessive NLR expression can lead to unintended autoimmunity 3 , 4 . Unlike most NLRs, the plant NLR required for cell death 2 (NRC2) belongs to a small NLR group characterized by constitutively high expression without self-activation 5 . The mechanisms underlying NRC2 autoinhibition and activation are not yet understood. Here we show that Solanum lycopersicum (tomato) NRC2 ( Sl NRC2) forms dimers and tetramers and higher-order oligomers at elevated concentrations. Cryo-electron microscopy shows an inactive conformation of Sl NRC2 in these oligomers. Dimerization and oligomerization not only stabilize the inactive state but also sequester Sl NRC2 from assembling into an active form. Mutations at the dimeric or interdimeric interfaces enhance pathogen-induced cell death and immunity in Nicotiana benthamiana . The cryo-electron microscopy structures unexpectedly show inositol hexakisphosphate (IP 6 ) or pentakisphosphate (IP 5 ) bound to the inner surface of the C-terminal leucine-rich repeat domain of Sl NRC2, as confirmed by mass spectrometry. Mutations at the inositol phosphate-binding site impair inositol phosphate binding of Sl NRC2 and pathogen-induced Sl NRC2-mediated cell death in N. benthamiana . Our study indicates a negative regulatory mechanism of NLR activation and suggests inositol phosphates as cofactors of NRCs. Cryo-electron microscopy reveals that the tomato immune receptor NRC2 forms oligomers to stabilize its inactive state and sequester it from activation, with inositol phosphates acting as immunoregulatory cofactors.

Roots have important roles for plants to withstand adverse environmental conditions, including salt stress. Biostimulant application was shown to enhance plant resilience towards abiotic stresses. Here, we studied the effect of a tannin-based biostimulant on tomato ( Solanum lycopersicum L.) grown under salt stress conditions. We investigated the related changes at both root architecture (via imaging and biometric analysis) and gene expression (RNA-Seq/qPCR) levels. Moreover, in order to identify the main compounds potentially involved in the observed effects, the chemical composition of the biostimulant was evaluated by UV/Vis and HPLC-ESI-Orbitrap analysis. Sixteen compounds, known to be involved in root development and having a potential antioxidant properties were identified. Significant increase of root weight (+ 24%) and length (+ 23%) was observed when the plants were grown under salt stress and treated with the biostimulant. Moreover, transcriptome analysis revealed that the application of the biostimulant upregulated 285 genes, most of which correlated to root development and salt stress tolerance. The 171 downregulated genes were mainly involved in nutrient uptake. These data demonstrated that the biostimulant is able not only to restore root growth in salty soils, but also to provide the adequate plant nourishment by regulating the expression of essential transcription factors and stress responsive genes.

Beneficial root endophytes such as Trichoderma spp. can reduce infections by parasitic nematodes through triggering host defences. Little is currently known about the complex hormone signalling underlying the induction of resistance. In this study, we investigated whether Trichoderma modulates the hormone signalling network in the host to induce resistance to nematodes. We investigated the role and the timing of the jasmonic acid (JA)- and salicylic acid (SA)-regulated defensive pathways in Trichoderma-induced resistance to the root knot nematode Meloidogyne incognita. A split-root system of tomato (Solanum lycopersicum) was used to study local and systemic induced defences by analysing nematode performance, defence gene expression, responsiveness to exogenous hormone application, and dependence on SA and JA signalling of Trichoderma-induced resistance. Root colonization by Trichoderma impeded nematode performance both locally and systemically at multiple stages of the parasitism, that is, invasion, galling and reproduction. First, Trichoderma primed SA-regulated defences, which limited nematode root invasion. Then, Trichoderma enhanced JA-regulated defences, thereby antagonizing the deregulation of JA-dependent immunity by the nematodes, which compromised galling and fecundity. Our results show that Trichoderma primes SA- and JA-dependent defences in roots, and that the priming of responsiveness to these hormones upon nematode attack is plastic and adaptive to the parasitism stage.

The maturation and ripening of fleshy fruits is a developmental program that synchronizes seed maturation with metabolism, rendering fruit tissues desirable to seed dispersing organisms. Through RNA interference repression, we show that Tomato AGAMOUS-LIKE1 (TAGL1), the tomato (Solanum lycopersicum) ortholog of the duplicated SHATTERPROOF (SHP) MADS box genes of Arabidopsis thaliana, is necessary for fruit ripening. Tomato plants with reduced TAGL1 mRNA produced yellow-orange fruit with reduced carotenoids and thin pericarps. These fruit are also decreased in ethylene, indicating a comprehensive inhibition of maturation mediated through reduced ACC Synthase 2 expression. Furthermore, ectopic expression of TAGL1 in tomato resulted in expansion of sepals and accumulation of lycopene, supporting the role of TAGL1 in ripening. In Arabidopsis, the duplicate SHP1 and SHP2 MADS box genes regulate the development of separation layers essential for pod shatter. Expression of TAGL1 in Arabidopsis failed to completely rescue the shp1 shp2 mutant phenotypes, indicating that TAGL1 has evolved distinct molecular functions compared with its Arabidopsis counterparts. These analyses demonstrate that TAGL1 plays an important role in regulating both fleshy fruit expansion and the ripening process that together are necessary to promote seed dispersal of fleshy fruit. From this broad perspective, SHP1/2 and TAGL1, while distinct in molecular function, regulate similar activities via their necessity for seed dispersal in Arabidopsis and tomato, respectively.

As a primary source of lycopene in the human diet, fleshy fruits synthesize this compound both de novo and via chlorophyll metabolism during ripening. SlSGR1 encodes a STAY-GREEN protein that plays a critical role in the regulation of chlorophyll degradation in tomato leaves and fruits. We report that SlSGR1 can regulate tomato (Solanum lycopersicum) lycopene accumulation through direct interaction with a key carotenoid synthetic enzyme SlPSY1, and can inhibit its activity. This interaction with SlSGR1 mediates lycopene accumulation during tomato fruit maturation. We confirmed this inhibitory activity in bacteria engineered to produce lycopene, where the introduction of SlSGR1 reduced dramatically lycopene biosynthesis. The repression of SlSGR1 in transgenic tomato fruits resulted in altered accumulation patterns of phytoene and lycopene, whilst simultaneously elevating SlPSY1 mRNA accumulation and plastid conversion at the early stages of fruit ripening, resulting in increased lycopene and β-carotene (four- and nine-fold, respectively) in red ripe fruits. SlSGR1 influences ethylene signal transduction via the altered expression of ethylene receptor genes and ethylene-induced genes. Fruit shelf-life is extended significantly in SlSGR1-repressed tomatoes. Our results indicate that SlSGR1 plays a pivotal regulatory role in color formation and fruit ripening regulation in tomato, and further suggest that SlSGR1 activity is mediated through direct interaction with PSY1.

Tomato mosaic virus (ToMV) is one of the economically damageable Tobamovirus infecting the tomato in Egypt that has caused significant losses. It is therefore of great interest to trigger systemic resistance to ToMV. In this endeavor, we aimed to explore the capacity of ZnO-NPs (zinc oxide nanoparticles) to trigger tomato plant resistance against ToMV. Effects of ZnO-NPs on tomato (Solanum lycopersicum L.) growth indices and antioxidant defense system activity under ToMV stress were investigated. Noticeably that treatment with ZnO-NPs showed remarkably increased growth indices, photosynthetic attributes, and enzymatic and non-enzymatic antioxidants compared to the challenge control. Interestingly, oxidative damage caused by ToMV was reduced by reducing malondialdehyde, H2O2, and O2 levels. Overall, ZnO-NPs offer a safe and economic antiviral agent against ToMV.

Carotenoids play important roles in many biological processes, such as light harvesting, photoprotection and visual attraction in plants. However, the regulation of carotenoid biosynthesis is still not fully understood. Here, we demonstrate that SlBBX20, a B-box (BBX) zinc-finger transcription factor, is a positive regulator of carotenoid accumulation in tomato (Solanum lycopersicum). Overexpression of SlBBX20 leads to dark green fruits and leaves and higher levels of carotenoids relative to the wild-type. Interactions between SlBBX20 and DE-ETIOLATED 1 (Sl DET1) lead to the ubiquitination and 26S proteasome-mediated degradation of SlBBX20. Moreover, deficiencies in the components of the CUL4-DDB1-DET1 complex enhanced the stability of the SlBBX20 protein. Thus, we conclude that SlBBX20 is a substrate of the CUL4-DDB1-DET1 E3 ligase. SlBBX20 can activate the expression of PHYTOENE SYNTHASE 1, encoding a key enzyme in carotenoid biosynthesis, by directly binding to a G-box motif in its promoter, which results in the elevated levels of carotenoids in SlBBX20 overexpression lines. We identified a key regulator of carotenoid biosynthesis and demonstrated that the stability of SlBBX20 is regulated by ubiquitination. These findings provide us a new target for the genetic improvement of the nutritional quality of tomato fruit.