Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement

Schauer, Nicolas; Semel, Yaniv; Roessner, Ute; Gur, Amit; Balbo, Ilse; Carrari, Fernando; Pleban, Tzili; Perez-Melis, Alicia; Bruedigam, Claudia; Kopka, Joachim; Willmitzer, Lothar; Zamir, Dani; Fernie, Alisdair R.

doi:10.1038/nbt1192

Cited by 685 publications

(655 citation statements)

References 44 publications

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“…Consistent with this idea, cells in developing fruit were shown to contain photosynthetically active chloroplasts (Piechulla et al, 1987), suggesting that photosynthesis may provide a significant contribution to both metabolism and growth of the fruit organ. This hypothesis is further supported by global transcriptomic profiling of transgenic lines altered in auxin response owing to down-regulation of SlIAA9, an Aux/IAA gene, which revealed that the activation of photosynthesis-related genes is a major phenomenon in developing tomato fruit (Schauer et al, 2006;Wang et al, Figure 6. Expression profile of SlAGPase genes in wild-type and ASL1 tomato fruits.…”

Section: Discussionmentioning

confidence: 58%

SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development

et al. 2013

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Successful completion of fruit developmental programs depends on the interplay between multiple phytohormones. However, besides ethylene, the impact of other hormones on fruit quality traits remains elusive. A previous study has shown that downregulation of SlARF4, a member of the tomato (Solanum lycopersicum) auxin response factor (ARF) gene family, results in a darkgreen fruit phenotype with increased chloroplasts (Jones et al., 2002). This study further examines the role of this auxin transcriptional regulator during tomato fruit development at the level of transcripts, enzyme activities, and metabolites. It is noteworthy that the dark-green phenotype of antisense SlARF4-suppressed lines is restricted to fruit, suggesting that SlARF4 controls chlorophyll accumulation specifically in this organ. The SlARF4 underexpressing lines accumulate more starch at early stages of fruit development and display enhanced chlorophyll content and photochemical efficiency, which is consistent with the idea that fruit photosynthetic activity accounts for the elevated starch levels. SlARF4 expression is high in pericarp tissues of immature fruit and then undergoes a dramatic decline at the onset of ripening concomitant with the increase in sugar content. The higher starch content in developing fruits of SlARF4 down-regulated lines correlates with the up-regulation of genes and enzyme activities involved in starch biosynthesis, suggesting their negative regulation by SlARF4. Altogether, the data uncover the involvement of ARFs in the control of sugar content, an essential feature of fruit quality, and provide insight into the link between auxin signaling, chloroplastic activity, and sugar metabolism in developing fruit.

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Section: Discussionmentioning

confidence: 58%

SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development

et al. 2013

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“…Although only a fraction of the metabolic phenotype can be measured, due to the high connectivity in metabolic networks 34 , the profiles carry information about other unmeasured traits 41 . Regression-based analyses have shown that metabolite and enzyme activity profiles provide an integrative metabolic phenotype that is predictive of biomass 33,34,42,43 , heterosis 44 , and, to a lesser extent, abiotic stress tolerance in plants 45 .…”

Section: Resultsmentioning

confidence: 99%

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

et al. 2014

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Growth often involves a trade-off between the performance of contending tasks; metabolic plasticity can play an important role. Here we grow 97 Arabidopsis thaliana accessions in three conditions with a differing supply of carbon and nitrogen and identify a trade-off between two tasks required for rosette growth: increasing the physical size and increasing the protein concentration. We employ the Pareto performance frontier concept to rank accessions based on their multitask performance; only a few accessions achieve a good trade-off under all three growth conditions. We determine metabolic efficiency in each accession and condition by using metabolite levels and activities of enzymes involved in growth and protein synthesis. We demonstrate that accessions with high metabolic efficiency lie closer to the performance frontier and show increased metabolic plasticity. We illustrate how public domain data can be used to search for additional contending tasks, which may underlie the sub-optimality in some accessions. L iving organisms perform many different and sometimes contending tasks, leading to trade-offs in which optimal performance of one task comes at the cost of a sub-optimal performance of another task. Trade-offs are influenced by the environment and their resolution depends on metabolic resources and plasticity 1,2 . One important environmental variable affecting plant growth is resource availability 3-6 . We first ask whether there is a trade-off between two tasks during vegetative growth of Arabidopsis thaliana: the maximization of physical size and the maximization of protein concentration. We then apply two methods to rank accessions: the first based solely on the performance of tasks, and the second based on the efficiency with which metabolic resources are deployed to perform tasks. In addition, we investigate whether the trade-off and the ranking of accessions are affected by the availability of carbon (C) and nitrogen (N) and the way in which it shapes the accession-specific metabolic profiles.Plants use light energy to transform CO 2 and inorganic nutrients into a plethora of metabolic precursors that are used to drive growth. As plants are sessile, resource acquisition is constrained by their physical size. In land plants, the majority of a mature cell is occupied by the vacuole, allowing the generation of a much larger physical size per unit protein than is usually obtained by microbes or animals 7 . For simplification, we do not consider the impact of shape and phenology on the relation between physical size and resource acquisition. On the other hand, proteins are required to catalyse the transformation of resources into biomass. In particular, the majority of the protein in a plant leaf is involved in photosynthesis [8][9][10] . We hypothesize that there is a trade-off between physical size and protein concentration. While production of leaves with a higher protein concentration will allow higher rates of photosynthesis and metabolism per unit biomass, it also increases the costs of growth a...

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“…Association mapping by GWAS is suitable for screening a large number of accessions for common variants within the population at relative high resolution (Huang et al, 2010;Huang and Han, 2012), while linkage mapping using artificial populations such as RILs and ILs is likely to be more powerful in identifying alleles with low frequency or small effects in the population (Fridman et al, 2004;Keurentjes et al, 2006;Schauer et al, 2006;Matsuda et al, 2012). Joint linkage and association mapping as illustrated in the study proved to be useful not just in cross-validating results from one another, but also complimenting each other in identifying new candidate loci (Luo, 2015).…”

Section: Discussionmentioning

confidence: 99%

Evolutionarily Distinct BAHD N-acyltransferases are Responsible for Natural Variation of Aromatic Amine Conjugates in Rice

et al. 2016

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Phenolamides (PAs) are specialized (secondary) metabolites mainly synthesized by BAHD N-acyltransferases. Here, we report metabolic profiling coupled with association and linkage mapping of 11 PAs in rice (Oryza sativa). We identified 22 loci affecting PAs in leaves and 16 loci affecting PAs in seeds. We identified eight BAHD N-acyltransferases located on five chromosomes with diverse specificities, including four aromatic amine N-acyltransferases. We show that genetic variation in PAs is determined, at least in part, by allelic variation in the tissue specificity of expression of the BAHD genes responsible for their biosynthesis. Tryptamine hydroxycinnamoyl transferase 1/2 (Os-THT1/2) and tryptamine benzoyl transferase 1/2 (Os-TBT1/2) were found to be bifunctional tryptamine/tyramine N-acyltransferases. The specificity of Os-THT1 and Os-TBT1 for agmatine involved four tandem arginine residues, which have not been identified as specificity determinants for other plant BAHD transferases, illustrating the versatility of plant BAHD transferases in acquiring new acyl acceptor specificities. With phylogenetic analysis, we identified both divergent and convergent evolution of N-acyltransferases in plants, and we suggest that the BAHD family of tryptamine/tyramine N-acyltransferases evolved conservatively in monocots, especially in Gramineae. Our work demonstrates that omics-assisted gene-to-metabolite analysis provides a useful tool for bulk gene identification and crop genetic improvement.

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Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement

Cited by 685 publications

References 44 publications

SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development

SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development

Metabolic efficiency underpins performance trade-offs in growth of Arabidopsis thaliana

Evolutionarily Distinct BAHD N-acyltransferases are Responsible for Natural Variation of Aromatic Amine Conjugates in Rice

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