TY - JOUR A1 - Córdoba, Sandra Correa A1 - Tong, Hao A1 - Burgos, Asdrubal A1 - Zhu, Feng A1 - Alseekh, Saleh A1 - Fernie, Alisdair R. A1 - Nikoloski, Zoran T1 - Identification of gene function based on models capturing natural variability of Arabidopsis thaliana lipid metabolism JF - Nature Communications N2 - The use of automated tools to reconstruct lipid metabolic pathways is not warranted in plants. Here, the authors construct Plant Lipid Module for Arabidopsis rosette using constraint-based modeling, demonstrate its integration in other plant metabolic models, and use it to dissect the genetic architecture of lipid metabolism. Lipids play fundamental roles in regulating agronomically important traits. Advances in plant lipid metabolism have until recently largely been based on reductionist approaches, although modulation of its components can have system-wide effects. However, existing models of plant lipid metabolism provide lumped representations, hindering detailed study of component modulation. Here, we present the Plant Lipid Module (PLM) which provides a mechanistic description of lipid metabolism in the Arabidopsis thaliana rosette. We demonstrate that the PLM can be readily integrated in models of A. thaliana Col-0 metabolism, yielding accurate predictions (83%) of single lethal knock-outs and 75% concordance between measured transcript and predicted flux changes under extended darkness. Genome-wide associations with fluxes obtained by integrating the PLM in diel condition- and accession-specific models identify up to 65 candidate genes modulating A. thaliana lipid metabolism. Using mutant lines, we validate up to 40% of the candidates, paving the way for identification of metabolic gene function based on models capturing natural variability in metabolism. KW - Biochemical networks KW - Biochemical reaction networks KW - Genetic models KW - Plant molecular biology Y1 - 2023 U6 - https://doi.org/10.1038/s41467-023-40644-9 SN - 2041-1723 VL - 14 IS - 1 PB - Springer Nature CY - London ER - TY - JOUR A1 - Nunes-Nesi, Adriano A1 - Alseekh, Saleh A1 - de Oliveira Silva, Franklin Magnum A1 - Omranian, Nooshin A1 - Lichtenstein, Gabriel A1 - Mirnezhad, Mohammad A1 - Romero Gonzalez, Roman R. A1 - Sabio y Garcia, Julia A1 - Conte, Mariana A1 - Leiss, Kirsten A. A1 - Klinkhamer, Peter Gerardus Leonardus A1 - Nikoloski, Zoran A1 - Carrari, Fernando A1 - Fernie, Alisdair R. T1 - Identification and characterization of metabolite quantitative trait loci in tomato leaves and comparison with those reported for fruits and seeds JF - Metabolomics N2 - IntroductionTo date, most studies of natural variation and metabolite quantitative trait loci (mQTL) in tomato have focused on fruit metabolism, leaving aside the identification of genomic regions involved in the regulation of leaf metabolism.ObjectiveThis study was conducted to identify leaf mQTL in tomato and to assess the association of leaf metabolites and physiological traits with the metabolite levels from other tissues.MethodsThe analysis of components of leaf metabolism was performed by phenotypying 76 tomato ILs with chromosome segments of the wild species Solanum pennellii in the genetic background of a cultivated tomato (S. lycopersicum) variety M82. The plants were cultivated in two different environments in independent years and samples were harvested from mature leaves of non-flowering plants at the middle of the light period. The non-targeted metabolite profiling was obtained by gas chromatography time-of-flight mass spectrometry (GC-TOF-MS). With the data set obtained in this study and already published metabolomics data from seed and fruit, we performed QTL mapping, heritability and correlation analyses.ResultsChanges in metabolite contents were evident in the ILs that are potentially important with respect to stress responses and plant physiology. By analyzing the obtained data, we identified 42 positive and 76 negative mQTL involved in carbon and nitrogen metabolism.ConclusionsOverall, these findings allowed the identification of S. lycopersicum genome regions involved in the regulation of leaf primary carbon and nitrogen metabolism, as well as the association of leaf metabolites with metabolites from seeds and fruits. KW - Metabolite QTL KW - Tomato KW - Leaf metabolism KW - Metabolite network Y1 - 2019 U6 - https://doi.org/10.1007/s11306-019-1503-8 SN - 1573-3882 SN - 1573-3890 VL - 15 IS - 46 PB - Springer CY - New York ER - TY - JOUR A1 - Tabatabaei, Iman A1 - Alseekh, Saleh A1 - Shahid, Mohammad A1 - Leniak, Ewa A1 - Wagner, Mateusz A1 - Mahmoudi, Henda A1 - Thushar, Sumitha A1 - Fernie, Alisdair R. A1 - Murphy, Kevin M. A1 - Schmöckel, Sandra M. A1 - Tester, Mark A1 - Müller-Röber, Bernd A1 - Skirycz, Aleksandra A1 - Balazadeh, Salma T1 - The diversity of quinoa morphological traits and seed metabolic composition JF - Scientific data N2 - Quinoa (Chenopodium quinoa Willd.) is an herbaceous annual crop of the amaranth family (Amaranthaceae). It is increasingly cultivated for its nutritious grains, which are rich in protein and essential amino acids, lipids, and minerals. Quinoa exhibits a high tolerance towards various abiotic stresses including drought and salinity, which supports its agricultural cultivation under climate change conditions. The use of quinoa grains is compromised by anti-nutritional saponins, a terpenoid class of secondary metabolites deposited in the seed coat; their removal before consumption requires extensive washing, an economically and environmentally unfavorable process; or their accumulation can be reduced through breeding. In this study, we analyzed the seed metabolomes, including amino acids, fatty acids, and saponins, from 471 quinoa cultivars, including two related species, by liquid chromatography - mass spectrometry. Additionally, we determined a large number of agronomic traits including biomass, flowering time, and seed yield. The results revealed considerable diversity between genotypes and provide a knowledge base for future breeding or genome editing of quinoa. Y1 - 2022 U6 - https://doi.org/10.1038/s41597-022-01399-y SN - 2052-4463 VL - 9 IS - 1 PB - Nature Research CY - Berlin ER - TY - JOUR A1 - Pandey, Prashant K. A1 - Yu, Jing A1 - Omranian, Nooshin A1 - Alseekh, Saleh A1 - Vaid, Neha A1 - Fernie, Alisdair R. A1 - Nikoloski, Zoran A1 - Laitinen, Roosa A. E. T1 - Plasticity in metabolism underpins local responses to nitrogen in Arabidopsis thaliana populations JF - Plant Direct N2 - Nitrogen (N) is central for plant growth, and metabolic plasticity can provide a strategy to respond to changing N availability. We showed that two local A. thaliana populations exhibited differential plasticity in the compounds of photorespiratory and starch degradation pathways in response to three N conditions. Association of metabolite levels with growth-related and fitness traits indicated that controlled plasticity in these pathways could contribute to local adaptation and play a role in plant evolution. KW - Arabidopsis thaliana KW - natural variation KW - nitrogen availability KW - photorespiration KW - plasticity Y1 - 2019 U6 - https://doi.org/10.1002/pld3.186 SN - 2475-4455 VL - 3 IS - 11 PB - John Wiley & sonst LTD CY - Chichester ER - TY - GEN A1 - Durgud, Meriem A1 - Gupta, Saurabh A1 - Ivanov, Ivan A1 - Omidbakhshfard, Mohammad Amin A1 - Benina, Maria A1 - Alseekh, Saleh A1 - Staykov, Nikola A1 - Hauenstein, Mareike A1 - Dijkwel, Paul P. A1 - Hortensteiner, Stefan A1 - Toneva, Valentina A1 - Brotman, Yariv A1 - Fernie, Alisdair R. A1 - Müller-Röber, Bernd A1 - Gechev, Tsanko S. T1 - Molecular mechanisms preventing senescence in response to prolonged darkness in a desiccation-tolerant plant T2 - Postprints der Universität Potsdam Mathematisch-Naturwissenschaftliche Reihe N2 - The desiccation-tolerant plant Haberlea rhodopensis can withstand months of darkness without any visible senescence. Here, we investigated the molecular mechanisms of this adaptation to prolonged (30 d) darkness and subsequent return to light. H. rhodopensis plants remained green and viable throughout the dark treatment. Transcriptomic analysis revealed that darkness regulated several transcription factor (TF) genes. Stress-and autophagy-related TFs such as ERF8, HSFA2b, RD26, TGA1, and WRKY33 were up-regulated, while chloroplast-and flowering-related TFs such as ATH1, COL2, COL4, RL1, and PTAC7 were repressed. PHYTOCHROME INTERACTING FACTOR4, a negative regulator of photomorphogenesis and promoter of senescence, also was down-regulated. In response to darkness, most of the photosynthesis-and photorespiratory-related genes were strongly down-regulated, while genes related to autophagy were up-regulated. This occurred concomitant with the induction of SUCROSE NON-FERMENTING1-RELATED PROTEIN KINASES (SnRK1) signaling pathway genes, which regulate responses to stress-induced starvation and autophagy. Most of the genes associated with chlorophyll catabolism, which are induced by darkness in dark-senescing species, were either unregulated (PHEOPHORBIDE A OXYGENASE, PAO; RED CHLOROPHYLL CATABOLITE REDUCTASE, RCCR) or repressed (STAY GREEN-LIKE, PHEOPHYTINASE, and NON-YELLOW COLORING1). Metabolite profiling revealed increases in the levels of many amino acids in darkness, suggesting increased protein degradation. In darkness, levels of the chloroplastic lipids digalactosyldiacylglycerol, monogalactosyldiacylglycerol, phosphatidylglycerol, and sulfoquinovosyldiacylglycerol decreased, while those of storage triacylglycerols increased, suggesting degradation of chloroplast membrane lipids and their conversion to triacylglycerols for use as energy and carbon sources. Collectively, these data show a coordinated response to darkness, including repression of photosynthetic, photorespiratory, flowering, and chlorophyll catabolic genes, induction of autophagy and SnRK1 pathways, and metabolic reconfigurations that enable survival under prolonged darkness. T3 - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 778 KW - beta-oxidation KW - craterostigma-plantagineum KW - photosynthetic apparatus KW - transcription factors KW - lipid-metabolism KW - leaf senescence KW - fatty-acid KW - arabidopsis KW - chlorophyll KW - stress Y1 - 2019 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-437588 IS - 778 SP - 1319 EP - 1338 ER - TY - JOUR A1 - Shahnejat-Bushehri, Sara A1 - Allu, Annapurna Devi A1 - Mehterov, Nikolay A1 - Thirumalaikumar, Venkatesh P. A1 - Alseekh, Saleh A1 - Fernie, Alisdair R. A1 - Mueller-Roeber, Bernd A1 - Balazadeh, Salma T1 - Arabidopsis NAC Transcription Factor JUNGBRUNNEN1 Exerts Conserved Control Over Gibberellin and Brassinosteroid Metabolism and Signaling Genes in Tomato JF - Frontiers in plant science N2 - The Arabidopsis thaliana NAC transcription factor JUNGBRUNNEN1 (AtJUB1) regulates growth by directly repressing GA3ox1 and DWF4, two key genes involved in gibberellin (GA) and brassinosteroid (BR) biosynthesis, respectively, leading to GA and BR deficiency phenotypes. AtJUB1 also reduces the expression of PIF4, a bHLH transcription factor that positively controls cell elongation, while it stimulates the expression of DELLA genes, which are important repressors of growth. Here, we extend our previous findings by demonstrating that AtJUB1 induces similar GA and BR deficiency phenotypes and changes in gene expression when overexpressed in tomato (Solanum lycopersicum). Importantly, and in accordance with the growth phenotypes observed, AtJUB1 inhibits the expression of growth-supporting genes, namely the tomato orthologs of GA3ox1, DWF4 and PIF4, but activates the expression of DELLA orthologs, by directly binding to their promoters. Overexpression of AtJUB1 in tomato delays fruit ripening, which is accompanied by reduced expression of several ripeningrelated genes, and leads to an increase in the levels of various amino acids (mostly proline, beta-alanine, and phenylalanine), gamma-aminobutyric acid (GABA), and major organic acids including glutamic acid and aspartic acid. The fact that AtJUB1 exerts an inhibitory effect on the GA/BR biosynthesis and PIF4 genes but acts as a direct activator of DELLA genes in both, Arabidopsis and tomato, strongly supports the model that the molecular constituents of the JUNGBRUNNEN1 growth control module are considerably conserved across species. KW - Arabidopsis KW - tomato KW - fruit KW - growth KW - transcription factor KW - gibberellic acid KW - brassinosteroid KW - DELLA proteins Y1 - 2017 U6 - https://doi.org/10.3389/fpls.2017.00214 SN - 1664-462X VL - 8 PB - Frontiers Research Foundation CY - Lausanne ER - TY - JOUR A1 - Alseekh, Saleh A1 - Tohge, Takayuki A1 - Wendenberg, Regina A1 - Scossa, Federico A1 - Omranian, Nooshin A1 - Li, Jie A1 - Kleessen, Sabrina A1 - Giavalisco, Patrick A1 - Pleban, Tzili A1 - Müller-Röber, Bernd A1 - Zamir, Dani A1 - Nikoloski, Zoran A1 - Fernie, Alisdair R. T1 - Identification and Mode of Inheritance of Quantitative Trait Loci for Secondary Metabolite Abundance in Tomato JF - The plant cell N2 - A large-scale metabolic quantitative trait loci (mQTL) analysis was performed on the well-characterized Solanum pennellii introgression lines to investigate the genomic regions associated with secondary metabolism in tomato fruit pericarp. In total, 679 mQTLs were detected across the 76 introgression lines. Heritability analyses revealed that mQTLs of secondary metabolism were less affected by environment than mQTLs of primary metabolism. Network analysis allowed us to assess the interconnectivity of primary and secondary metabolism as well as to compare and contrast their respective associations with morphological traits. Additionally, we applied a recently established real-time quantitative PCR platform to gain insight into transcriptional control mechanisms of a subset of the mQTLs, including those for hydroxycinnamates, acyl-sugar, naringenin chalcone, and a range of glycoalkaloids. Intriguingly, many of these compounds displayed a dominant-negative mode of inheritance, which is contrary to the conventional wisdom that secondary metabolite contents decreased on domestication. We additionally performed an exemplary evaluation of two candidate genes for glycolalkaloid mQTLs via the use of virus-induced gene silencing. The combined data of this study were compared with previous results on primary metabolism obtained from the same material and to other studies of natural variance of secondary metabolism. Y1 - 2015 U6 - https://doi.org/10.1105/tpc.114.132266 SN - 1040-4651 SN - 1532-298X VL - 27 IS - 3 SP - 485 EP - 512 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Rodriguez Cubillos, Andres Eduardo A1 - Tong, Hao A1 - Alseekh, Saleh A1 - de Abreu e Lima, Francisco Anastacio A1 - Yu, Jing A1 - Fernie, Alisdair R. A1 - Nikoloski, Zoran A1 - Laitinen, Roosa A. E. T1 - Inheritance patterns in metabolism and growth in diallel crosses of Arabidopsis thaliana from a single growth habitat JF - Heredity N2 - Metabolism is a key determinant of plant growth and modulates plant adaptive responses. Increased metabolic variation due to heterozygosity may be beneficial for highly homozygous plants if their progeny is to respond to sudden changes in the habitat. Here, we investigate the extent to which heterozygosity contributes to the variation in metabolism and size of hybrids of Arabidopsis thaliana whose parents are from a single growth habitat. We created full diallel crosses among seven parents, originating from Southern Germany, and analysed the inheritance patterns in primary and secondary metabolism as well as in rosette size in situ. In comparison to primary metabolites, compounds from secondary metabolism were more variable and showed more pronounced non-additive inheritance patterns which could be attributed to epistasis. In addition, we showed that glucosinolates, among other secondary metabolites, were positively correlated with a proxy for plant size. Therefore, our study demonstrates that heterozygosity in local A. thaliana population generates metabolic variation and may impact several tasks directly linked to metabolism. Y1 - 2018 U6 - https://doi.org/10.1038/s41437-017-0030-5 SN - 0018-067X SN - 1365-2540 VL - 120 IS - 5 SP - 463 EP - 473 PB - Nature Publ. Group CY - London ER - TY - JOUR A1 - Malinova, Irina A1 - Kunz, Hans-Henning A1 - Alseekh, Saleh A1 - Herbst, Karoline A1 - Fernie, Alisdair R. A1 - Gierth, Markus A1 - Fettke, Jörg T1 - Reduction of the cytosolic phosphoglucomutase in arabidopsis reveals impact on plant growth, seed and root development, and carbohydrate partitioning JF - PLoS one N2 - Phosphoglucomutase (PGM) catalyses the interconversion of glucose 1-phosphate (G1P) and glucose 6-phosphate (G6P) and exists as plastidial (pPGM) and cytosolic (cPGM) isoforms. The plastidial isoform is essential for transitory starch synthesis in chloroplasts of leaves, whereas the cytosolic counterpart is essential for glucose phosphate partitioning and, therefore, for syntheses of sucrose and cell wall components. In Arabidopsis two cytosolic isoforms (PGM2 and PGM3) exist. Both PGM2 and PGM3 are redundant in function as single mutants reveal only small or no alterations compared to wild type with respect to plant primary metabolism. So far, there are no reports of Arabidopsis plants lacking the entire cPGM or total PGM activity, respectively. Therefore, amiRNA transgenic plants were generated and used for analyses of various parameters such as growth, development, and starch metabolism. The lack of the entire cPGM activity resulted in a strongly reduced growth revealed by decreased rosette fresh weight, shorter roots, and reduced seed production compared to wild type. By contrast content of starch, sucrose, maltose and cell wall components were significantly increased. The lack of both cPGM and pPGM activities in Arabidopsis resulted in dwarf growth, prematurely die off, and inability to develop a functional inflorescence. The combined results are discussed in comparison to potato, the only described mutant with lack of total PGM activity. Y1 - 2014 U6 - https://doi.org/10.1371/journal.pone.0112468 SN - 1932-6203 VL - 9 IS - 11 PB - PLoS CY - San Fransisco ER - TY - JOUR A1 - Durgud, Meriem A1 - Gupta, Saurabh A1 - Ivanov, Ivan A1 - Omidbakhshfard, Mohammad Amin A1 - Benina, Maria A1 - Alseekh, Saleh A1 - Staykov, Nikola A1 - Hauenstein, Mareike A1 - Dijkwel, Paul P. A1 - Hortensteiner, Stefan A1 - Toneva, Valentina A1 - Brotman, Yariv A1 - Fernie, Alisdair R. A1 - Müller-Röber, Bernd A1 - Gechev, Tsanko S. T1 - Molecular Mechanisms Preventing Senescence in Response to Prolonged Darkness in a Desiccation-Tolerant Plant JF - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants N2 - The desiccation-tolerant plant Haberlea rhodopensis can withstand months of darkness without any visible senescence. Here, we investigated the molecular mechanisms of this adaptation to prolonged (30 d) darkness and subsequent return to light. H. rhodopensis plants remained green and viable throughout the dark treatment. Transcriptomic analysis revealed that darkness regulated several transcription factor (TF) genes. Stress-and autophagy-related TFs such as ERF8, HSFA2b, RD26, TGA1, and WRKY33 were up-regulated, while chloroplast-and flowering-related TFs such as ATH1, COL2, COL4, RL1, and PTAC7 were repressed. PHYTOCHROME INTERACTING FACTOR4, a negative regulator of photomorphogenesis and promoter of senescence, also was down-regulated. In response to darkness, most of the photosynthesis-and photorespiratory-related genes were strongly down-regulated, while genes related to autophagy were up-regulated. This occurred concomitant with the induction of SUCROSE NON-FERMENTING1-RELATED PROTEIN KINASES (SnRK1) signaling pathway genes, which regulate responses to stress-induced starvation and autophagy. Most of the genes associated with chlorophyll catabolism, which are induced by darkness in dark-senescing species, were either unregulated (PHEOPHORBIDE A OXYGENASE, PAO; RED CHLOROPHYLL CATABOLITE REDUCTASE, RCCR) or repressed (STAY GREEN-LIKE, PHEOPHYTINASE, and NON-YELLOW COLORING1). Metabolite profiling revealed increases in the levels of many amino acids in darkness, suggesting increased protein degradation. In darkness, levels of the chloroplastic lipids digalactosyldiacylglycerol, monogalactosyldiacylglycerol, phosphatidylglycerol, and sulfoquinovosyldiacylglycerol decreased, while those of storage triacylglycerols increased, suggesting degradation of chloroplast membrane lipids and their conversion to triacylglycerols for use as energy and carbon sources. Collectively, these data show a coordinated response to darkness, including repression of photosynthetic, photorespiratory, flowering, and chlorophyll catabolic genes, induction of autophagy and SnRK1 pathways, and metabolic reconfigurations that enable survival under prolonged darkness. Y1 - 2018 U6 - https://doi.org/10.1104/pp.18.00055 SN - 0032-0889 SN - 1532-2548 VL - 177 IS - 3 SP - 1319 EP - 1338 PB - American Society of Plant Physiologists CY - Rockville ER -