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Phosphorus (P) is a vital nutrient for plant growth. P availability is generally low in soils, and plant responses to low P availability need to be better understood. In a previous study, we studied the growth and physiological responses of 24 species to low P availability in the soil and verified of eucalypts, five (Eucalyptus acmenoides, E. grandis, E. globulus, E. tereticornis, and Corymbia maculata) contrasted regarding their efficiency and responsiveness to soil P availability. Here, we obtained the metabolomic and lipidomic profile of leaves, stems, and roots from these species growing under low (4.5 mg dm-3) and sufficient (10.8 mg dm-3) P in the soil. Disregarding the level of P in the soils, P allocation was always higher in the stems. However, when grown in the P-sufficient soil, the stems steadily were the largest compartment of the total plant P. Under low P, the relative contents of primary metabolites, such as amino acids, TCA cycle intermediates, organic acids and carbohydrates, changed differently depending on the species. Additionally, phosphorylated metabolites showed enhanced turnover or reductions. While photosynthetic efficiencies were not related to higher biomass production, A/Ci curves showed that reduced P availability increased the eucalypt species' Vcmax, Jmax and photosynthetic P-use efficiency. Plants of E. acmenoides increased galactolipids and sulfolipids in leaves more than other eucalypt species, suggesting that lipid remodelling can be a strategy to cope with the P shortage in this species. Our findings offer insights to understand genotypic efficiency among eucalypt species to accommodate primary metabolism under low soil P availability and eventually be used as biochemical markers for breeding programs.

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Witches' broom disease of cacao is caused by the pathogenic fungus Moniliophthora perniciosa. By using tomato (Solanum lycopersicum) cultivar Micro-Tom (MT) as a model system, we investigated the physiological and metabolic consequences of M. perniciosa infection to determine whether symptoms result from sink establishment during infection. Infection of MT by M. perniciosa caused reductions in root biomass and fruit yield, a decrease in leaf gas exchange, and down-regulation of photosynthesis-related genes. The total leaf area and water potential decreased, while ABA levels, water conductance/conductivity, and ABA-related gene expression increased. Genes related to sugar metabolism and those involved in secondary cell wall deposition were up-regulated upon infection, and the concentrations of sugars, fumarate, and amino acids increased. 14C-glucose was mobilized towards infected MT stems, but not in inoculated stems of the MT line overexpressing CYTOKININ OXIDASE-2 (35S::AtCKX2), suggesting a role for cytokinin in establishing a sugar sink. The up-regulation of genes involved in cell wall deposition and phenylpropanoid metabolism in infected MT, but not in 35S::AtCKX2 plants, suggests establishment of a cytokinin-mediated sink that promotes tissue overgrowth with an increase in lignin. Possibly, M. perniciosa could benefit from the accumulation of secondary cell walls during its saprotrophic phase of infection.

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Most research in plant chronobiology has been done in laboratory conditions. However, laboratories usually fail to mimic natural conditions and their slight fluctuations, highlighting or obfuscating rhythmicity. High-density crops, such as sugarcane (Saccharum hybrid), generate field microenvironments with specific light and temperature regimes resulting from mutual shading. We measured the metabolic and transcriptional rhythms in the leaves of 4-month-old (4 mo) and 9 mo field-grown sugarcane. Most of the assayed rhythms in 9 mo sugarcane peaked >1 h later than in 4 mo sugarcane, including rhythms of the circadian clock gene, LATE ELONGATED HYPOCOTYL (LHY). We hypothesized that older sugarcane perceives dawn later than younger sugarcane as a consequence of self-shading. As a test, we measured LHY rhythms in plants on the east and the west sides of a field. We also tested if a wooden wall built between lines of sugarcane plants changed their rhythms. The LHY peak was delayed in the plants in the west of the field or beyond the wall; both shaded at dawn. We conclude that plants in the same field may have different phases resulting from field microenvironments, impacting important agronomical traits, such as flowering time, stalk weight and number.

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N-Acetylcysteine (NAC) is an antioxidant, anti-adhesive, and antimicrobial compound. Even though there is much information regarding the role of NAC as an antioxidant and anti-adhesive agent, little is known about its antimicrobial activity. In order to assess its mode of action in bacterial cells, we investigated the metabolic responses triggered by NAC at neutral pH. As a model organism, we chose the Gram-negative plant pathogen Xanthomonas citri subsp. citri (X. citri), the causal agent of citrus canker disease, due to the potential use of NAC as a sustainable molecule against phytopathogens dissemination in citrus cultivated areas. In presence of NAC, cell proliferation was affected after 4 h, but damages to the cell membrane were observed only after 24 h. Targeted metabolite profiling analysis using GC-MS/TOF unravelled that NAC seems to be metabolized by the cells affecting cysteine metabolism. Intriguingly, glutamine, a marker for nitrogen status, was not detected among the cells treated with NAC. The absence of glutamine was followed by a decrease in the levels of the majority of the proteinogenic amino acids, suggesting that the reduced availability of amino acids affect protein synthesis and consequently cell proliferation.

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Oral squamous cell carcinoma (OSCC) has high mortality rates that are largely associated with lymph node metastasis. However, the molecular mechanisms that drive OSCC metastasis are unknown. Extracellular vesicles (EVs) are membrane-bound particles that play a role in intercellular communication and impact cancer development and progression. Thus, profiling EVs would be of great significance to decipher their role in OSCC metastasis. For that purpose, we used a reductionist approach to map the proteomic, miRNA, metabolomic, and lipidomic profiles of EVs derived from human primary tumor (SCC-9) cells and matched lymph node metastatic (LN1) cells. Distinct omics profiles were associated with the metastatic phenotype, including 670 proteins, 217 miRNAs, 26 metabolites, and 63 lipids differentially abundant between LN1 cell- and SCC-9 cell-derived EVs. A multi-omics integration identified 11 'hub proteins' significantly decreased at the metastatic site compared with primary tumor-derived EVs. We confirmed the validity of these findings with analysis of data from multiple public databases and found that low abundance of seven 'hub proteins' in EVs from metastatic lymph nodes (ALDH7A1, CAD, CANT1, GOT1, MTHFD1, PYGB, and SARS) is correlated with reduced survival and tumor aggressiveness in patients with cancer. In summary, this multi-omics approach identified proteins transported by EVs that are associated with metastasis and which may potentially serve as prognostic markers in OSCC.

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Adjustment to energy starvation is crucial to ensure growth and survival. In Arabidopsis thaliana (Arabidopsis), this process relies in part on the phosphorylation of the circadian clock regulator bZIP63 by SUCROSE non-fermenting RELATED KINASE1 (SnRK1), a key mediator of responses to low energy. We investigated the effects of mutations in bZIP63 on plant carbon (C) metabolism and growth. Results from phenotypic, transcriptomic and metabolomic analysis of bZIP63 mutants prompted us to investigate the starch accumulation pattern and the expression of genes involved in starch degradation and in the circadian oscillator. bZIP63 mutation impairs growth under light-dark cycles, but not under constant light. The reduced growth likely results from the accentuated C depletion towards the end of the night, which is caused by the accelerated starch degradation of bZIP63 mutants. The diel expression pattern of bZIP63 is dictated by both the circadian clock and energy levels, which could determine the changes in the circadian expression of clock and starch metabolic genes observed in bZIP63 mutants. We conclude that bZIP63 composes a regulatory interface between the metabolic and circadian control of starch breakdown to optimize C usage and plant growth.

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The Target of Rapamycin (TOR) kinase pathway integrates energy and nutrient availability into metabolism promoting growth in eukaryotes. The overall higher efficiency on nutrient use translated into faster growth rates in C4 grass plants led to the investigation of differential transcriptional and metabolic responses to short-term chemical TOR complex (TORC) suppression in the model Setaria viridis. In addition to previously described responses to TORC inhibition (i.e., general growth arrest, translational repression, and primary metabolism reprogramming) in Arabidopsis thaliana (C3), the magnitude of changes was smaller in S. viridis, particularly regarding nutrient use efficiency and C allocation and partitioning that promote biosynthetic growth. Besides photosynthetic differences, S. viridis and A. thaliana present several specificities that classify them into distinct lineages, which also contribute to the observed alterations mediated by TOR. Indeed, cell wall metabolism seems to be distinctly regulated according to each cell wall type, as synthesis of non-pectic polysaccharides were affected in S. viridis, whilst assembly and structure in A. thaliana. Our results indicate that the metabolic network needed to achieve faster growth seems to be less stringently controlled by TORC in S. viridis.

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KEY MESSAGE: The tomato mutant Never ripe (Nr), a loss-of-function for the ethylene receptor SlETR3, shows enhanced growth, associated with increased carbon assimilation and a rewiring of the central metabolism. Compelling evidence has demonstrated the importance of ethylene during tomato fruit development, yet its role on leaf central metabolism and plant growth remains elusive. Here, we performed a detailed characterization of Never ripe (Nr) tomato, a loss-of-function mutant for the ethylene receptor SlETR3, known for its fruits which never ripe. However, besides fruits, the Nr gene is also constitutively expressed in vegetative tissues. Nr mutant showed a growth enhancement during both the vegetative and reproductive stage, without an earlier onset of leaf senescence, with Nr plants exhibiting a higher number of leaves and an increased dry weight of leaves, stems, roots, and fruits. At metabolic level, Nr also plays a significant role with the mutant showing changes in carbon assimilation, carbohydrates turnover, and an exquisite reprogramming of a large number of metabolite levels. Notably, the expression of genes related to ethylene signaling and biosynthesis are not altered in Nr. We assess our results in the context of those previously published for tomato fruits and of current models of ethylene signal transduction, and conclude that ethylene insensitivity mediated by Nr impacts the whole central metabolism at vegetative stage, leading to increased growth rates.

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Metabolomics is a valuable approach used to acquire comprehensive information about the set of metabolites in a cell or tissue, enabling a functional screen of the cellular activities in biological systems. Although metabolomics provides a more immediate and dynamic picture of phenotypes in comparison to the other omics, it is also the most complicated to measure because no single analytical technology can capture the extraordinary complexity of metabolite diversity in terms of structure and physical properties. Metabolomics has been extensively employed for a wide range of applications in plant science, which will be described in detail in this chapter. Among them, metabolomics is used for discriminating patterns of plant responses to genetic and environmental perturbations, as diagnostics and prediction tool to elucidate the function of genes for important and complex agronomic traits in crop species, and flux measurements are used to dissect the structure and regulatory properties of metabolic networks.

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