Contrasting Metabolisms in Green and White Leaf Sectors of Variegated Pelargonium zonale—An Integrative Transcriptomic and Metabolomic Study

Abstract

The photosynthetically active green leaf (GL) and non-active white leaf (WL) tissues of variegated Pelargonium zonale provide an excellent model system for studying processes associated with photosynthesis and sink-source interactions, enabling the same microenvironmental conditions. By combining differential transcriptomics and metabolomics, we identified the main differences between these two metabolically contrasting tissues. Genes related to photosynthesis and associated pigments, the Calvin–Benson cycle, fermentation, and glycolysis were strongly repressed in WL. On the other hand, genes related to nitrogen and protein metabolism, defence, cytoskeletal components (motor proteins), cell division, DNA replication, repair and recombination, chromatin remodelling, and histone modifications were upregulated in WL. A content of soluble sugars, TCA intermediates, ascorbate, and hydroxybenzoic acids was lower, while the concentration of free amino acids (AAs), hydroxycinnamic acids, and several quercetin and kaempferol glycosides was higher in WL than in GL. Therefore, WL presents a carbon sink and depends on photosynthetic and energy-generating processes in GL. Furthermore, the upregulated nitrogen metabolism in WL compensates for the insufficient energy from carbon metabolism by providing alternative respiratory substrates. At the same time, WL serves as nitrogen storage. Overall, our study provides a new genetic data resource for the use of this excellent model system and for ornamental pelargonium breeding and contributes to uncovering molecular mechanisms underlying variegation and its adaptive ecological value.

Red-Light Transmittance Changes in Variegated Pelargonium zonale—Diurnal Variation in Chloroplast Movement and Photosystem II Efficiency

“…The biphasic response of Phot1 triggered by higher light intensities and blue light of 16 µmol photons m −2 s −1 , with partial chloroplast avoidance preceding the accumulation phase, has been described previously [ 52 , 53 ]. The kinetics obtained in P. zonale leaves can be explained by the fact that both chloroplast accumulation and avoidance occur simultaneously with the avoidance response starting and proceeding faster than the accumulation response, which has a longer lifetime [ 16 , 54 ]. In conclusion, the observed reversible and complex kinetics of T in GS of variegated P. zonale indicated that the interplay between accumulation and avoidance response of chloroplasts is required to maintain their optimal position within the cell in terms of photosynthetic efficiency.…”

“…Very recently, we performed a de novo transcriptome analysis of P. zonale and, for the first time, analysed the differentially expressed genes (DEGs) in GS and WS. Prediction of the subcellular location of a protein encoded by selected DEGs (published in [ 54 ]) was conducted by WoLF-PSORT tool [ 66 ].…”

Metabolomics and Transcriptomics Analyses Reveals the Molecular Regulatory Mechanisms of Walnut (Juglans regia L.) Embryos in Response to Shade Treatment

“…However, due to the complexity of plant biological processes, transcriptome data cannot accurately describe the macro events occurring in biological systems. In recent years, the combination of metabolomics and transcriptome analyses has been widely used in research conducted in the field to study plants, which can more systematically and comprehensively explore the mechanism of metabolite synthesis [ 16 , 17 , 18 ].…”

Carbon and Nitrogen Allocation between the Sink and Source Leaf Tissue in Response to the Excess Excitation Energy Conditions

“…Leaf variegation (e.g., in Pelargonium zonale) has proven to be a suitable model system to study source-sink interactions in terms of carbon and nitrogen allocation within the same leaf under the same microenvironmental conditions [19,20]. These leaves contain photosynthetically inactive white leaf tissue (WL) at the leaf margin and photosynthetically active green leaf tissue (GL) in the leaf centre.…”

“…In our previous work [19], the differential transcriptomic analysis of the gene expression of P. zonale GL and WL under optimal growth conditions was performed for the first time. It was found that the WL tissue had a higher content of nitrogenous compounds, especially free amino acids (AAs), compared to GL.…”