Elevated carbon assimilation and metabolic reprogramming in tomato high pigment mutants support the increased production of pigments.

KEY MESSAGE: High pigment mutants in tomato (Solanum lycopersicum L.), a loss of function in the control of photomorphogenesis, with greater pigment production, show altered growth, greater photosynthesis, and a metabolic reprogramming. High pigment mutations cause plants to be extremely responsive to light and produce excessive pigmentation as well as fruits with high levels of health-beneficial nutrients. However, the association of these traits with changes in the physiology and metabolism of leaves remains poorly understood. Here, we performed a detailed morphophysiological and metabolic characterization of high pigment 1 (hp1) and high pigment 2 (hp2) mutants in tomato (Solanum lycopersicum L. 'Micro-Tom') plants under different sunlight conditions (natural light, 50% shading, and 80% shading). These mutants occur in the DDB1 (hp1) and DET1 (hp2) genes, which are related to the regulation of photomorphogenesis and chloroplast development. Our results demonstrate that these mutations delay plant growth and height, by affecting physiological and metabolic parameters at all stages of plant development. Although the mutants were characterized by higher net CO2 assimilation, lower stomatal limitation, and higher carboxylation rates, with anatomical changes that favour photosynthesis, we found that carbohydrate levels did not increase, indicating a change in the energy flow. Shading minimized the differences between mutants and the wild type or fully reversed them in the phenotype at the metabolic level. Our results indicate that the high levels of pigments in hp1 and hp2 mutants represent an additional energy cost for these plants and that extensive physiological and metabolic reprogramming occurs to support increased pigment biosynthesis.

Growth inhibition by selenium is associated with changes in primary metabolism and nutrient levels in Arabidopsis thaliana.

Although Selenium (Se) stress is relatively well known for causing growth inhibition, its effects on primary metabolism remain rather unclear. Here, we characterized both the modulation of the expression of specific genes and the metabolic adjustments in Arabidopsis thaliana in response to changes in Se level in the soil. Se treatment culminated with strong inhibition of both shoot and root growth. Notably, growth inhibition in Se-treated plants was associated with an incomplete mobilization of starch during the night. Minor changes in amino acids levels were observed in shoots and roots of plants treated with Se whereas the pool size of tricarboxylic acid (TCA) cycle intermediates in root was not altered in response to Se. By contrast, decreased levels of organic acids involved in the first part of the TCA cycle were observed in shoots of Se-treated plants. Furthermore, decreased expression levels of expansins and endotransglucosylases/endohydrolases (XHTs) genes were observed after Se treatment, coupled with a significant decrease in the levels of essential elements. Collectively, our results revealed an exquisite interaction between energy metabolism and Se-mediated control of growth in Arabidopsis thaliana to coordinate cell wall extension, starch turnover and the levels of a few essential nutrients.

Differential content of leaf and fruit pigment in tomatoes culminate in a complex metabolic reprogramming without growth impacts.

Although significant efforts to produce carotenoid-enriched foods either by biotechnology or traditional breeding strategies have been carried out, our understanding of how changes in the carotenoid biosynthesis might affect overall plant performance remains limited. Here, we investigate how the metabolic machinery of well characterized tomato carotenoid mutant plants [namely crimson (old gold-og), Delta carotene (Del) and tangerine (t)] adjusts itself to varying carotenoid biosynthesis and whether these adjustments are supported by a reprogramming of photosynthetic and central metabolism in the source organs (leaves). We observed that mutations og, Del and t did not greatly affect vegetative growth, leaf anatomy and gas exchange parameters. However, an exquisite metabolic reprogramming was recorded on the leaves, with an increase in levels of amino acids and reduction of organic acids. Taken together, our results show that despite minor impacts on growth and gas exchange, carbon flux is extensively affected, leading to adjustments in tomato leaves metabolism to support changes in carotenoid biosynthesis on fruits (sinks). We discuss these data in the context of our current understanding of metabolic adjustments and carotenoid biosynthesis as well as regarding to improving human nutrition.

Dynamic shifts in primary metabolism across fruit development stages in Capsicum chinense (cv. Habanero).

The development of fleshy fruits involves changes in size and mass, followed by cell differentiation, which is associated with anatomical and histological changes. Parallel to these changes, metabolic alterations lead to the production of osmolytes and energy that modify cell turgor pressure, thereby promoting cell expansion and fruit growth. Detailed information is known about these processes in climacteric fruits (e.g. tomato); however, the regulation of metabolism and its association with anatomical changes in non-climacteric fruit development are poorly understood. In this study, we used detailed anatomical and histological analyses to define three developmental phases of chili pepper (Capsicum chinense cv. Habanero): cell division, cell expansion, and ripening. We showed that each was marked by distinct metabolic profiles, underpinning the switches in energy metabolism to support cellular processes. Interestingly, mitochondrial activity was high in the early stages of development and declined over time, with a modest increase in O2 consumption by pericarp tissues at the beginning of the ripening stage. This respiratory-like burst was associated with the degradation of starch and malate, which are the sources of energy and carbon required for other processes associated with fruit maturation.

Physiological, metabolic, and stomatal adjustments in response to salt stress in Jatropha curcas.

Salinity is a major issue affecting photosynthesis and crop production worldwide. High salinity induces both osmotic and ionic stress in plant tissues as a result of complex interactions among morphological, physiological, and biochemical processes. Salinity, in turn, can provoke inactivation of some enzymes in the Calvin-Benson cycle and therefore affect the fine adjustment of electron transport in photosystem I and carbon related reactions. Here, we used three contrasting Jatropha curcas genotypes namely CNPAE183 (considered tolerant to salinity), CNPAE218 (sensible), and JCAL171 (intermediate) to understand salinity responses. By performing a long-term (12 months) experiment in land conditions, we investigated distinct mechanisms used by J. curcas to cope with threatening salinity effects by analyzing gas exchange, mineral nutrition and metabolic responses. First, our results highlighted the plasticity of stomatal development and density in J. curcas under salt stress. It also demonstrated that the CNPAE183 presented higher salt-tolerance whereas CNPAE218 displayed a more sensitive salt-tolerance response. Our results also revealed that both tolerance and sensitivity to salinity were connected with an extensive metabolite reprogramming in the Calvin-Benson cycle and Tricarboxylic Acid cycle intermediates with significant changes in amino acids and organic acids. Collectively, these results indicate that the CNPAE183 and CNPAE218 genotypes demonstrated certain characteristics of salt-tolerant-like and salt-sensitive-like genotypes, respectively. Overall, our results highlight the significance of metabolites associated with salt responses and further provide a useful selection criterion in during screening for salt tolerance in J. curcas in breeding programmes.

2-Oxoglutarate: linking TCA cycle function with amino acid, glucosinolate, flavonoid, alkaloid, and gibberellin biosynthesis.

The tricarboxylic acid (TCA) cycle intermediate 2-oxoglutarate (2-OG) is used as an obligatory substrate in a range of oxidative reactions catalyzed by 2-OG-dependent dioxygenases. These enzymes are widespread in nature being involved in several important biochemical processes. We have recently demonstrated that tomato plants in which the TCA cycle enzyme 2-OG dehydrogenase (2-ODD) was antisense inhibited were characterized by early senescence and modified fruit ripening associated with differences in the levels of bioactive gibberellin (GA). Accordingly, there is now compelling evidence that the TCA cycle plays an important role in modulating the rate of flux from 2-OG to amino acid metabolism. Here we discuss recent advances in the biochemistry and molecular biology of 2-OG metabolism occurring in different biological systems indicating the importance of 2-OG and 2-OG dependent dioxygenases not only in glucosinolate, flavonoid and alkaloid metabolism but also in GA and amino acid metabolism. We additionally summarize recent findings regarding the impact of modification of 2-OG metabolism on biosynthetic pathways involving 2-ODDs.