The pressing global issue of food insecurity due to population growth, diminishing land and variable climate can only be addressed in agriculture by improving both maximum crop yield potential and resilience. Genetic modification is one potential solution, but has yet to achieve worldwide acceptance, particularly for crops such as wheat. Trehalose-6-phosphate (T6P), a central sugar signal in plants, regulates sucrose use and allocation, underpinning crop growth and development. Here we show that application of a chemical intervention strategy directly modulates T6P levels in planta. Plant-permeable analogues of T6P were designed and constructed based on a 'signalling-precursor' concept for permeability, ready uptake and sunlight-triggered release of T6P in planta. We show that chemical intervention in a potent sugar signal increases grain yield, whereas application to vegetative tissue improves recovery and resurrection from drought. This technology offers a means to combine increases in yield with crop stress resilience. Given the generality of the T6P pathway in plants and other small-molecule signals in biology, these studies suggest that suitable synthetic exogenous small-molecule signal precursors can be used to directly enhance plant performance and perhaps other organism function.
One sentence summary: T6P can be targeted through genetic and chemical methods for crop yield 10 improvements in different environments through the effect of T6P on carbon allocation and 11 biosynthetic pathways 12Significant increases in global food security require improving crop yields in favourable and 13 poor conditions alike. However, it is challenging to increase both the crop yield potential and yield 14 resilience simultaneously, since the mechanisms that determine productivity and stress tolerance are 15 typically inversely related. Carbon allocation and use may be amenable to improving yields in a range 16 of conditions. The interaction between trehalose 6-phosphate (T6P) and SnRK1 (SNF1-related/AMPK 17 protein kinases) significantly affects the regulation of carbon allocation and utilisation in plants. 18Targeting T6P appropriately to certain cell types, tissue types, and developmental stages results in an 31 SUCROSE AND TREHALOSE: THE YIN AND YANG OF CROP IMPROVEMENT 32Plants are the only organisms that synthesise both non-reducing disaccharides, trehalose and 33 sucrose. The ubiquity of both pathways in plants has been known for less than 20 years and was a 34 major revelation for those working on carbon metabolism, as well as plant scientists in general, given 35 the range of processes affected by the trehalose pathway. Plant metabolism is highly regulated. Part 36 of this regulation is through trehalose 6-phosphate (T6P) signalling that regulates metabolism in the 37 light of carbon availability and reprograms metabolism between anabolic or catabolic pathways 38 depending on the carbohydrate status of the plant. This discovery is also significant for understanding 39 the regulation of growth and development by carbon supply. Furthermore, the trehalose pathway may 40 widely impact crop improvement. Crops are not yet optimised to maximize their biosynthetic pathways 41 for yield in sinks and growth recovery that are promoted by high T6P, and for mobilisation of reserves 42 and sugar transport which can enable resilience that are promoted by low T6P. 43Both the trehalose and sucrose biosynthesis pathways draw from a pool of core metabolites, 44 from which the carbon skeletons for all cellular components are also made (Paul et al. 2008 procedures to measure the abundance of T6P and trehalose (Lunn et al. 2006; Carillo et al. 2013; 51 Delatte et al. 2009;Mata et al. 2016). The capacity to synthesise trehalose in 52 plants began to become apparent as the associated plant genes were identified (Blazquez et al. 1998; 53 Vogel et al. 1998). Subsequent publication of the Arabidopsis genome showed an abundance of both 54 trehalose phosphate synthase (TPS) and trehalose phosphate phosphatase (TPP) gene families with 55 11 and 10 members respectively (Leyman et al. 2001). 56It is likely that T6P is a specific signal indicating sucrose abundance (Lunn et al. 2006; Nunes 57 et al. 2013a). T6P and sucrose levels are correlated in many tissues e.g. Arabidopsis and wheat 72TPSs have yet to be resolve...
ABSTRACT. We compare the relative contributions of phototrophy (translocation of photosynthates from zooxanthellae) and heterotrophy (filtered particles) towards the carbon requirements for tissue and shell growth, and metabolism in 4 species of giant clam from the Great Barrier Reef. The primary aims were to determine whether the differences in growth rates of various clam species could be due to nutrition, and to quantify the relative roles of phototrophy and heterotrophy in the nutrition of tridacnids. The species examined were distinguishable by both absolute C flux and relative proportions of components of the C budget. For example, Trjdacna gigas was photosynthetically the most efficient, gaining twice as much nutrition as 7. crocea, and an order of magnitude more than Hippopus hippopus. In the case of the smallest clams tested (0.1 g tissue wt), intake of C via filter feeding was also highest in T. gigas, being 10 times that of the other species. These interspecific differences declined with clam size. Tridacna gigas, T. crocea, and T squamosa were able to satisfy all their growth and metabolic requirements from the intake of photosynthate and particulate food, in some cases with considerable energy to spare. In contrast, small H. tuppopus gained 80% of total C needs from these sources. We confirm that phototrophy is the most significant source of energy to clams. In all but the smallest H. hlppopus, this source provides sufficient C for growth and metabolic requirements. Filterfeeding decreases in importance with increasing size of clam. Ingested C provides 61 to 113% of total needs in 40 to 80 mm T. gigas and 36 to 44 % in H. hippopus, but was less significant to the other species (10 to 20%). H. hippopus allocated the highest proportion of C expenditure to growth (30 to 90 %), up to half of which went into shell. T. gigas and T. squamosa both put 20 to 40% of C into growth, compared with only 10 to 20% in T. crocea. There was no simple nutritional basis to the differences in growth of the 4 species. T. gigas has the greatest excess of energy available for growth, and the highest growth rate in terms of shell length. However, the connection between available energy and growth rate was not consistent across species. Actual growth in units of C was similar in T gigas and H. hippopus, yet small individuals of the latter species appear limited by availability of C. Despite a relatively high calculated 'scope' for growth, 7. crocea exhibited the lowest growth rate possibly because its growth is limited by physical constraints of its burrowing habit.
Little is known about how salt impacts primary metabolic pathways of C 4 plants, particularly related to kernel development and seed set. Osmotic stress was applied to maize (Zea mays) B73 by irrigation with increasing concentrations of NaCl from the initiation of floral organs until 3 d after pollination. At silking, photosynthesis was reduced to only 2% of control plants. Salt treatment was found to reduce spikelet growth, silk growth, and kernel set. Osmotic stress resulted in higher concentrations of sucrose (Suc) and hexose sugars in leaf, cob, and kernels at silking, pollination, and 3 d after pollination. Citric acid cycle intermediates were lower in salt-treated tissues, indicating that these sugars were unavailable for use in respiration. The sugar-signaling metabolite trehalose-6-phosphate was elevated in leaf, cob, and kernels at silking as a consequence of salt treatment but decreased thereafter even as Suc levels continued to rise. Interestingly, the transcripts of trehalose pathway genes were most affected by salt treatment in leaf tissue. On the other hand, transcripts of the SUCROSE NONFERMENTING-RELATED KINASE1 (SnRK1) marker genes were most affected in reproductive tissue. Overall, both source and sink strength are reduced by salt, and the data indicate that trehalose-6-phosphate and SnRK1 may have different roles in source and sink tissues. Kernel abortion resulting from osmotic stress is not from a lack of carbohydrate reserves but from the inability to utilize these energy reserves.
Metabolite transport between organelles, cells and source and sink tissues not only enables pathway co-ordination but it also facilitates whole plant communication, particularly in the transmission of information concerning resource availability. Carbon assimilation is co-ordinated with nitrogen assimilation to ensure that the building blocks of biomass production, amino acids and carbon skeletons, are available at the required amounts and stoichiometry, with associated transport processes making certain that these essential resources are transported from their sites of synthesis to those of utilisation. Of the many possible posttranslational mechanisms that might participate in efficient co-ordination of metabolism and transport only reversible thiol-disulphide exchange mechanisms have been described in detail. Sucrose and trehalose metabolism are intertwined in the signalling hub that ensures appropriate resource allocation to drive growth and development under optimal and stress conditions, with trehalose-6-phosphate acting as an important signal for sucrose availability. The formidable suite of plant metabolite transporters provides enormous flexibility and adaptability in inter-pathway coordination and source-sink interactions. Focussing on the carbon metabolism network, we highlight the functions of different transporter families, and the important of thioredoxins in the metabolic dialogue between source and sink tissues. In addition, we address how these systems can be tailored for crop improvement.
Research into extreme drought tolerance in resurrection plants using species such as Craterostigma plantagineum, C. wilmsii, Xerophyta humilis, Tortula ruralis, and Sporobolus stapfianus has provided some insight into the desiccation tolerance mechanisms utilized by these plants to allow them to persist under extremely adverse environmental conditions. Some of the mechanisms used to ensure cellular preservation during severe dehydration appear to be peculiar to resurrection plants. Apart from the ability to preserve vital cellular components during drying and rehydration, such mechanisms include the ability to down-regulate growth-related metabolism rapidly in response to changes in water availability, and the ability to inhibit dehydration-induced senescence programs enabling reconstitution of photosynthetic capacity quickly following a rainfall event. Extensive research on the molecular mechanism of leaf senescence in non-resurrection plants has revealed a multi-layered regulatory network operates to control programed cell death pathways. However, very little is known about the molecular mechanisms that resurrection plants employ to avoid undergoing drought-related senescence during the desiccation process. To survive desiccation, dehydration in the perennial resurrection grass S. stapfianus must proceed slowly over a period of 7 days or more. Leaves detached from the plant before 60% relative water content (RWC) is attained are desiccation-sensitive indicating that desiccation tolerance is conferred in vegetative tissue of S. stapfianus when the leaf RWC has declined to 60%. Whilst some older leaves remaining attached to the plant during dehydration will senesce, suggesting dehydration-induced senescence may be influenced by leaf age or the rate of dehydration in individual leaves, the majority of leaves do not senesce. Rather these leaves dehydrate to air-dryness and revive fully following rehydration. Hence it seems likely that there are genes expressed in younger leaf tissues of resurrection plants that enable suppression of drought-related senescence pathways. As very few studies have directly addressed this phenomenon, this review aims to discuss current literature surrounding the activation and suppression of senescence pathways and how these pathways may differ in resurrection plants.
BackgroundDrought stress during flowering is a major contributor to yield loss in maize. Genetic and biotechnological improvement in yield sustainability requires an understanding of the mechanisms underpinning yield loss. Sucrose starvation has been proposed as the cause for kernel abortion; however, potential targets for genetic improvement have not been identified. Field and greenhouse drought studies with maize are expensive and it can be difficult to reproduce results; therefore, an in vitro kernel culture method is presented as a proxy for drought stress occurring at the time of flowering in maize (3 days after pollination). This method is used to focus on the effects of drought on kernel metabolism, and the role of trehalose 6-phosphate (Tre6P) and the sucrose non-fermenting-1-related kinase (SnRK1) as potential regulators of this response.ResultsA precipitous drop in Tre6P is observed during the first two hours after removing the kernels from the plant, and the resulting changes in transcript abundance are indicative of an activation of SnRK1, and an immediate shift from anabolism to catabolism. Once Tre6P levels are depleted to below 1 nmol∙g−1 FW in the kernel, SnRK1 remained active throughout the 96 h experiment, regardless of the presence or absence of sucrose in the medium. Recovery on sucrose enriched medium results in the restoration of sucrose synthesis and glycolysis. Biosynthetic processes including the citric acid cycle and protein and starch synthesis are inhibited by excision, and do not recover even after the re-addition of sucrose. It is also observed that excision induces the transcription of the sugar transporters SUT1 and SWEET1, the sucrose hydrolyzing enzymes CELL WALL INVERTASE 2 (INCW2) and SUCROSE SYNTHASE 1 (SUSY1), the class II TREHALOSE PHOSPHATE SYNTHASES (TPS), TREHALASE (TRE), and TREHALOSE PHOSPHATE PHOSPHATASE (ZmTPPA.3), previously shown to enhance drought tolerance (Nuccio et al., Nat Biotechnol (October 2014):1–13, 2015).ConclusionsThe impact of kernel excision from the ear triggers a cascade of events starting with the precipitous drop in Tre6P levels. It is proposed that the removal of Tre6P suppression of SnRK1 activity results in transcription of putative SnRK1 target genes, and the metabolic transition from biosynthesis to catabolism. This highlights the importance of Tre6P in the metabolic response to starvation. We also present evidence that sugars can mediate the activation of SnRK1. The precipitous drop in Tre6P corresponds to a large increase in transcription of ZmTPPA.3, indicating that this specific enzyme may be responsible for the de-phosphorylation of Tre6P. The high levels of Tre6P in the immature embryo are likely important for preventing kernel abortion.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-017-1018-2) contains supplementary material, which is available to authorized users.
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