Metabolic analysis of the regulatory mechanism of sugars on secondary flowering in Magnolia

Abstract

Background Magnolia, a traditional and important ornamental plant in urban greening, has been cultivated for about 2000 years in China for its elegant flower shape and gorgeous flower color. Most varieties of Magnolia bloom once a year in spring, whereas a few others, such as Magnolia liliiflora Desr. ‘Hongyuanbao’, also bloom for the second time in summer or early autumn. Such a twice flowering trait is desirable for its high ornamental value, while its underlying mechanism remains unclear. Methods Paraffin section was used to show the flowering time and phenotypic changes of M. liliiflora ‘Hongyuanbao’ during the twice flowering periods from March 28 to August 25, 2018. Gas chromatography-mass spectrometry (GC-MS) was then performed to explore the chemical metabolites through the twice flower bud differentiation process in ‘Hongyuanbao’, and the metabolites were screened and identified by orthogonal projection to latent structures discriminant analysis (OPLS-DA). Kyoto Encyclopedia of Genes and Genomes pathway enrichment analysis (KEGG) was used to reveal the relationship between the sugar metabolites and twice-flowering characteristic. To further investigate the potential role of sucrose and trehalose on flowering regulation of ‘Hongyuanbao’, the plants once finished the spring flowering were regularly sprayed with sucrose and trehalose solutions at 30 mM, 60 mM, and 90 mM concentrations from April 22, 2019. The flower bud differentiation processes of sprayed plants were observed and the expression patterns of the genes involved in sucrose and trehalose metabolic pathways were studied by quantitative reverse transcription PCR (qRT-PCR). Results It showed that ‘Hongyuanbao’ could complete flower bud differentiation twice in a year and flowered in both spring and summer. The metabolites of flower bud differentiation had a significant variation between the first and second flower buds. Compared to the first flower bud differentiation process, the metabolites in the sucrose and trehalose metabolic pathways were significantly up-regulated during the second flower bud differentiation process. Besides that, the expression levels of a number of trehalose-6-phosphate synthase (TPS) genes including MlTPS1, MlTPS5, MlTPS6, MlTPS7 and MlTPS9 were substantially increased in the second flower differentiation process compared with the first process. Exogenous treatments indicated that compared to the control plants (sprayed with water, CK), all three concentrations of trehalose could accelerate flowering and the effect of 60 mM concentration was the most significant. For the sucrose foliar spray, only the 60 mM concentration accelerated flowering compared with CK. It suggested that different concentration of trehalose and sucrose might have different effects. Expression analysis showed that sucrose treatment increased the transcription levels of MlTPS5 and MlTPS6, whereas trehalose treatment increased MlTPS1, showing that different MlTPS genes took part in sucrose and trehalose metabolic pathways respectively. The expression levels of a number of flowering-related genes, such as MlFT, MlLFY, and MlSPL were also increased in response to the sprays of sucrose and trehalose. Conclusions We provide a novel insight into the effect of sucrose and trehalose on the flowering process in Magnolia. Under the different sugar contents treatments, the time of flower bud differentiation of Magnolia was advanced. Induced and accelerated flowering in response to sucrose and trehalose foliar spray, coupled with elevated expression of trehalose regulatory and response genes, suggests that secondary flower bud formation is a promoted by altered endogenous sucrose and trehalose levels. Those results give a new understanding of sucrose and trehalose on twice-flowering in Magnolia and provide a preliminary speculation for inducing and accelerating the flowering process in Magnolia.

Nutrient Composition and Antioxidant Activity of Cercis chinensis Flower in Response to Different Development Stages

“…Sugar, as the fundamental molecule of carbon metabolism, can serve as an important energy substance throughout the entire life cycle of plants. In addition, sugar can interact with other inorganic regulatory networks as a signaling molecule, thus affecting the transformation of plant from vegetative growth to reproductive growth [38]. The proportion of different types of sugars determines the physical and chemical properties of flower buds and flowers, and the metabolic process of sugars affects the amount and form of sugars stored in flower buds and flowers [39].…”

Integrated transcriptome, metabolome and phytohormone analysis reveals developmental differences between the first and secondary flowering in Castanea mollissima

“…The fruits gradually increase in size and colour and ripen in the summer and autumn. Some plants, such as pear trees ( Wei et al., 2022 ) and magnolias ( Xuan et al., 2022 ), exhibit an anomaly in flowering twice a year under certain conditions. For ornamental plants, the second flowering is due to its extended flowering period and popularity ( Iwata et al., 2012 ; Xuan et al., 2022 ; Xue et al., 2022 ); however, for perennial fruit trees, the second flowering and fruiting consume large amounts of nutrients, weakening the tree.…”

“…Some plants, such as pear trees ( Wei et al., 2022 ) and magnolias ( Xuan et al., 2022 ), exhibit an anomaly in flowering twice a year under certain conditions. For ornamental plants, the second flowering is due to its extended flowering period and popularity ( Iwata et al., 2012 ; Xuan et al., 2022 ; Xue et al., 2022 ); however, for perennial fruit trees, the second flowering and fruiting consume large amounts of nutrients, weakening the tree. The cold resistance of plants during winter is weakened, resulting in a reduced number of flowers and fruit production in the following year ( Qiu et al., 2019 ).…”