Phenolic compound profile and gastrointestinal action of Solanaceae fruits: Species-specific differences.

In this study, the presence of phenolic compounds derived from four Solanaceae fruits (tomato, pepino, tamarillo, and goldenberry) during gastrointestinal digestion and the effect of these compounds on human gut microbiota was investigated. The results indicated that the total phenolic content of all Solanaceae fruits were increased during digestion. Furthermore, the targeted metabolic analysis identified 296 compounds, of which 71 were changed after gastrointestinal digestion in all Solanaceae fruits. Among these changed phenolic compounds, 51.3% phenolic acids and 91% flavonoids presented higher bioaccessibility in pepino and tamarillo, respectively. Moreover, higher levels of glycoside-formed phenolic acids, including dihydroferulic acid glucoside and coumaric acid glucoside, were found in tomato fruits. In addition, tachioside showed the highest bioaccessibility in goldenberry fruits. The intake of Solanaceae fruits during the in vitro fermentation decreased the Firmicutes/Bacteroidetes ratio (F/B) compared with the control (∼15-fold change on average), and goldenberry fruits showed the best effect (F/B = 2.1). Furthermore, tamarillo significantly promoted the growth of Bifidobacterium and short-chain fatty acids production. Overall, this study revealed that Solanaceae fruits had different phenolic compound profiles and health-promoting effects on the gut microbiota. It also provided relevant information to improve the consumption of Solanaceae fruits, mainly tamarillo and goldenberry fruits, due to their gut health-promoting properties, as functional foods.

SlIAA23-SlARF6 module controls arbuscular mycorrhizal symbiosis by regulating strigolactone biosynthesis in tomato.

Auxins are a class of phytohormones with roles involved in the establishment and maintenance of the arbuscular mycorrhizal symbiosis (AMS). Auxin response factors (ARFs) and Auxin/Indole-acetic acids (AUX/IAAs), as two transcription factors of the auxin signaling pathway, coregulate the transcription of auxin response genes. However, the interrelation and regulatory mechanism of ARFs and AUX/IAAs in regulating AMS are still unclear. In this study, we found that the content of auxin in tomato roots increased sharply and revealed the importance of the auxin signaling pathway in the early stage of AMS. Notably, SlARF6 was found to play a negative role in AMF colonization. Silencing SlARF6 significantly increased the expression of AM-marker genes, as well as AMF-induced phosphorus uptake. SlIAA23 could interact with SlARF6 in vivo and in vitro, and promoted the AMS and phosphorus uptake. Interestingly, SlARF6 and SlIAA23 played a contrary role in strigolactone (SL) synthesis and accumulation in AMF-colonized roots of tomato plants. SlARF6 could directly bind to the AuxRE motif of the SlCCD8 promoter and inhibited its transcription, however, this effect was attenuated by SlIAA23 through interaction with SlARF6. Our results suggest that SlIAA23-SlARF6 coregulated tomato-AMS via an SL-dependent pathway, thus affecting phosphorus uptake in tomato plants.

Chromosome-level genome assembly of bunching onion illuminates genome evolution and flavor formation in Allium crops.

The Allium genus is cultivated globally as vegetables, condiments, or medicinal plants and is characterized by large genomes and strong pungency. However, the genome evolution and genomic basis underlying their unique flavor formation remain poorly understood. Herein, we report an 11.27-Gb chromosome-scale genome assembly for bunching onion (A. fistulosum). The uneven bursts of long-terminal repeats contribute to diversity in genome constituents, and dispersed duplication events largely account for gene expansion in Allium genomes. The extensive duplication and differentiation of alliinase and lachrymatory factor synthase manifest as important evolutionary events during flavor formation in Allium crops. Furthermore, differential selective preference for flavor-related genes likely lead to the variations in isoalliin content in bunching onions. Moreover, we reveal that China is the origin and domestication center for bunching onions. Our findings provide insights into Allium genome evolution, flavor formation and domestication history and enable future genome-assisted breeding of important traits in these crops.

A single-nucleotide polymorphism in WRKY33 promoter is associated with the cold sensitivity in cultivated tomato.

Natural variations in cis-regulatory regions often affect crop phenotypes by altering gene expression. However, the mechanism of how promoter mutations affect gene expression and crop stress tolerance is still poorly understood. In this study, by analyzing RNA-sequencing (RNA-Seq) data and reverse transcription quantitative real-time PCR validation in the cultivated tomato and its wild relatives, we reveal that the transcripts of WRKY33 are almost unchanged in cold-sensitive cultivated tomato Solanum lycopersicum L. 'Ailsa Craig' but are significantly induced in cold-tolerant wild tomato relatives Solanum habrochaites LA1777 and Solanum pennellii LA0716 under cold stress. Overexpression of SlWRKY33 or ShWRKY33 positively regulates cold tolerance in tomato. Variant of the critical W-box in SlWRKY33 promoter results in the loss of self-transcription function of SlWRKY33 under cold stress. Analysis integrating RNA-Seq and chromatin immunoprecipitation sequencing data reveals that SlWRKY33 directly targets and induces multiple kinases, transcription factors, and molecular chaperone genes, such as CDPK11, MYBS3, and BAG6, thus enhancing cold tolerance. In addition, heat- and Botrytis-induced WRKY33s expression in both wild and cultivated tomatoes are independent of the critical W-box variation. Our findings suggest nucleotide polymorphism in cis-regulatory regions is crucial for different cold sensitivity between cultivated and wild tomato plants.

Light-dependent activation of HY5 promotes mycorrhizal symbiosis in tomato by systemically regulating strigolactone biosynthesis.

Light quality affects mutualisms between plant roots and arbuscular mycorrhizal fungi (AMFs), which modify nutrient acquisition in plants. However, the mechanisms by which light systemically modulates root colonization by AMFs and phosphate uptake in roots remain unclear. We used a range of approaches, including grafting techniques, protein immunoblot analysis, electrophoretic mobility shift assay, chromatin immunoprecipitation, and dual-luciferase assays, to unveil the molecular basis of light signal transmission from shoot to root that mediates arbuscule development and phosphate uptake in tomato. The results show that shoot phytochrome B (phyB) triggers shoot-derived mobile ELONGATED HYPOCOTYL5 (HY5) protein accumulation in roots, and HY5 further positively regulates transcription of strigolactone (SL) synthetic genes, thus forming a shoot phyB-dependent systemic signaling pathway that regulates the synthesis and accumulation of SLs in roots. Further experiments with carotenoid cleavage dioxygenase 7 mutants and supplementary red light confirm that SLs are indispensable in the red-light-regulated mycorrhizal symbiosis in roots. Our results reveal a phyB-HY5-SLs systemic signaling cascade that facilitates mycorrhizal symbiosis and phosphate utilization in plants. The findings provide new prospects for the potential application of AMFs and light manipulation to effectively improve nutrient utilization and minimize the use of chemical fertilizers and associated pollution.

Brassinosteroid-mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato.

Phytohormone brassinosteroids (BRs) are essential for plant growth and development, but the mechanisms of BR-mediated pollen development remain largely unknown. In this study, we show that pollen viability, pollen germination and seed number decreased in the BR-deficient mutant d^im , which has a lesion in the BR biosynthetic gene DWARF (DWF), and in the bzr1 mutant, which is deficient in BR signaling regulator BRASSINAZOLE RESISTANT 1 (BZR1), compared with those in wild-type plants, whereas plants overexpressing DWF or BZR1 exhibited the opposite effects. Loss or gain of function in the DWF or BZR1 genes altered the timing of reactive oxygen species (ROS) production and programmed cell death (PCD) in tapetal cells, resulting in delayed or premature tapetal degeneration, respectively. Further analysis revealed that BZR1 could directly bind to the promoter of RESPIRATORY BURST OXIDASE HOMOLOG 1 (RBOH1), and that RBOH1-mediated ROS promote pollen and seed development by triggering PCD and tapetal cell degradation. In contrast, the suppression of RBOH1 compromised BR signaling-mediated ROS production and pollen development. These findings provide strong evidence that BZR1-dependent ROS production plays a critical role in the BR-mediated regulation of tapetal cell degeneration and pollen development in Solanum lycopersicum (tomato) plants.

A novel CO2 -responsive systemic signaling pathway controlling plant mycorrhizal symbiosis.

Elevated atmospheric carbon dioxide (eCO2 ) concentrations promote symbiosis between roots and arbuscular mycorrhizal fungi (AMF), modifying plant nutrient acquisition and cycling of carbon, nitrogen and phosphate. However, the biological mechanisms by which plants transmit aerial eCO2 cues to roots, to alter the symbiotic associations remain unknown. We used a range of interdisciplinary approaches, including gene silencing, grafting, transmission electron microscopy, liquid chromatography tandem mass spectrometry (LC-MS/MS), biochemical methodologies and gene transcript analysis to explore the complexities of environmental signal transmission from the point of perception in the leaves at the apex to the roots. Here we show that eCO2 triggers apoplastic hydrogen peroxide (H2 O2 )-dependent auxin production in tomato shoots followed by systemic signaling that results in strigolactone biosynthesis in the roots. This redox-auxin-strigolactone systemic signaling cascade facilitates eCO2 -induced AMF symbiosis and phosphate utilization. Our results challenge the current paradigm of eCO2 effects on AMF and provide new insights into potential targets for manipulation of AMF symbiosis for high nutrient utilization under future climate change scenarios.

Brassinosteroid Ameliorates Zinc Oxide Nanoparticles-Induced Oxidative Stress by Improving Antioxidant Potential and Redox Homeostasis in Tomato Seedling.

In the last few decades use of metal-based nanoparticles (MNPs) has been increased significantly that eventually contaminating agricultural land and limiting crop production worldwide. Moreover, contamination of food chain with MNPs has appeared as a matter of public concern due to risk of potential health hazard. Brassinosteroid has been shown to play a critical role in alleviating heavy metal stress; however, its function in relieving zinc oxide nanoparticles (ZnO NPs)-induced phytotoxicity remains unknown. In this study, we investigated the potential role of 24-epibrassinolide (BR) in mitigating ZnO NPs-induced toxicity in tomato seedlings. Seedling growth, biomass production, and root activity gradually decreased, but Zn accumulation increased with increasing ZnO NPs concentration (10-100 mg/L) in growth media (½ MS). The augmentation of BR (5 nM) in media significantly ameliorated 50 mg/L ZnO NPs-induced growth inhibition. Visualization of hydrogen peroxide (H2O2), and quantification of H2O2 and malondialdehyde (MDA) in tomato roots confirmed that ZnO NPs induced an oxidative stress. However, combined treatment with BR and ZnO NPs remarkably reduced concentration of H2O2 and MDA as compared with ZnO NPs only treatment, indicating that BR supplementation substantially reduced oxidative stress. Furthermore, the activities of key antioxidant enzymes such as superoxide dismutase (SOD), catalase, ascorbate peroxidase and glutathione reductase were increased by combined treatment of BR and ZnO NPs compared with ZnO NPs only treatment. BR also increased reduced glutathione (GSH), but decreased oxidized glutathione (GSSG)] and thus improved cellular redox homeostasis by increasing GSH:GSSG ratio. The changes in relative transcript abundance of corresponding antioxidant genes such as Cu/Zn SOD, CAT1, GSH1, and GR1 were in accordance with the changes in those antioxidants under different treatments. More importantly, combined application of BR and ZnO NPs significantly decreased Zn content in both shoot and root of tomato seedlings as compared with ZnO NPs alone. Taken together, this study, for the first time, showed that BR could not only improve plant tolerance to ZnO NPs but also reduce the excess zinc content in tomato seedlings. Such a finding may have potential implication in safe vegetable production in the MNPs-polluted areas.

Melatonin mediates selenium-induced tolerance to cadmium stress in tomato plants.

Both selenium (Se) and melatonin reduce cadmium (Cd) uptake and mitigate Cd toxicity in plants. However, the relationship between Se and melatonin in Cd detoxification remains unclear. In this study, we investigated the influence of three forms of Se (selenocysteine, sodium selenite, and sodium selenate) on the biosynthesis of melatonin and the tolerance against Cd in tomato plants. Pretreatment with different forms of Se significantly induced the biosynthesis of melatonin and its precursors (tryptophan, tryptamine, and serotonin); selenocysteine had the most marked effect on melatonin biosynthesis. Furthermore, Se and melatonin supplements significantly increased plant Cd tolerance as evidenced by decreased growth inhibition, photoinhibition, and electrolyte leakage (EL). Se-induced Cd tolerance was compromised in melatonin-deficient plants following tryptophan decarboxylase (TDC) gene silencing. Se treatment increased the levels of glutathione (GSH) and phytochelatins (PCs), as well as the expression of GSH and PC biosynthetic genes in nonsilenced plants, but the effects of Se were compromised in TDC-silenced plants under Cd stress. In addition, Se and melatonin supplements reduced Cd content in leaves of nonsilenced plants, but Se-induced reduction in Cd content was compromised in leaves of TDC-silenced plants. Taken together, our results indicate that melatonin is involved in Se-induced Cd tolerance via the regulation of Cd detoxification.

Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L.

Melatonin is a ubiquitous signal molecule, playing crucial roles in plant growth and stress tolerance. Recently, toxic metal cadmium (Cd) has been reported to regulate melatonin content in rice; however, the function of melatonin under Cd stress, particularly in higher plants, still remains elusive. Here, we show that optimal dose of melatonin could effectively ameliorate Cd-induced phytotoxicity in tomato. The contents of Cd and melatonin were gradually increased over time under Cd stress. However, such increase in endogenous melatonin was incapable to reverse detrimental effects of Cd. Meanwhile, supplementation with melatonin conferred Cd tolerance as evident by plant biomass and photosynthesis. In addition to notable increase in antioxidant enzymes activity, melatonin-induced Cd stress mitigation was closely associated with enhanced H(+)-ATPase activity and the contents of glutathione and phytochelatins. Although exogenous melatonin had no effect on root Cd content, it significantly reduced leaf Cd content, indicating its role in Cd transport. Analysis of Cd in different subcellular compartments revealed that melatonin increased cell wall and vacuolar fractions of Cd. Our results suggest that melatonin-induced enhancements in antioxidant potential, phytochelatins biosynthesis and subsequent Cd sequestration might play a critical role in plant tolerance to Cd. Such a mechanism may have potential implication in safe food production.

Phosphorus and magnesium interactively modulate the elongation and directional growth of primary roots in Arabidopsis thaliana (L.) Heynh.

A balanced supply of essential nutrients is an important factor influencing root architecture in many plants, yet data related to the interactive effects of two nutrients on root growth are limited. Here, we investigated the interactive effect between phosphorus (P) and magnesium (Mg) on root growth of Arabidopsis grown in pH-buffered agar medium at different P and Mg levels. The results showed that elongation and deviation of primary roots were directly correlated with the amount of P added to the medium but could be modified by the Mg level, which was related to the root meristem activity and stem-cell division. High P enhanced while low P decreased the tip-focused fluorescence signal of auxin biosynthesis, transport, and redistribution during elongation of primary roots; these effects were greater under low Mg than under high Mg. The altered root growth in response to P and Mg supply was correlated with AUX1, PIN2, and PIN3 mRNA abundance and expression and the accumulation of the protein. Application of either auxin influx inhibitor or efflux inhibitor inhibited the elongation and increased the deviation angle of primary roots, and decreased auxin level in root tips. Furthermore, the auxin-transport mutants aux1-22 and eir1-1 displayed reduced root growth and increased the deviation angle. Our data suggest a profound effect of the combined supply of P and Mg on the development of root morphology in Arabidopsis through auxin signals that modulate the elongation and directional growth of primary root and the expression of root differentiation and development genes.

Relationship between cytoplasmic male sterility and SPL-like gene expression in stem mustard.

We studied how mitochondria-nuclear interactions may give rise to cytoplasmic male sterility (CMS) in stem mustard exhibiting abnormal microsporogenesis. In this system, expression of SPL-like, the counterpart of the Arabidopsis nuclear gene SPOROCYTELESS, is specifically lost in buds of CMS plants. When mitochondrial-specific inhibitors were applied to wild-type fertile stem mustard plants, expression of SPL-like was repressed to some extent. As a consequence, the shape and vigor of pollen grains were severely affected, whereas the fertility of pistils remained unaltered. Thereby, we suggest that a probable pathway responsible for CMS in stem mustard involves mitochondrial retrograde regulation, with SPL-like as a target nuclear gene for a mitochondrial signal.

Expression of CycD3 is transiently increased by pollination and N-(2-chloro-4-pyridyl)-N'-phenylurea in ovaries of Lagenaria leucantha.

Lagenaria leucantha is an important vegetable crop and a potential model for the study of fruit development. To study the function of D cyclins in fruit development, full-length cDNA clones for two D cyclin genes were isolated from young ovaries of Lagenaria leucantha. They were classified as D3 cyclins by sequence similarities and phylogenetic analysis, and nominated LlCycD3;1 and LlCycD3;2, respectively. The deduced amino acid sequence of both LlCycD3 genes contained a retinoblastoma-binding motif and a PEST-destruction motif. Unpollinated ovaries failed to develop and eventually aborted. N-(2-chloro-4-pyridyl)-N'-phenylurea (CPPU) induced parthenocarpic fruit significantly larger than pollinated ones. In unpollinated ovaries, the expression of both LlCycD3 genes was abundant at anthesis and then suddenly decreased, concomitant with the cessation of cell division. Pollination/fertilization induced an activation of the cell cycle accompanied by a large increase in the transcript levels of LlCycD3;1 and LlCycD3;2 in young fruits. Treating ovaries with CPPU also reactivated cell division and transcription of CycD3 genes and the effect was more rapid and pronounced than after pollination/fertilization.