Integrated transcriptomic and metabolomic analysis suggests a potential regulatory network underlying leaf color transition in Ulmus pumila ‘Jinye’

Ulmus pumila ‘Jinye’ is valued for its bright golden leaves, but this coloration is unstable during development, leading to a “regreening” phenomenon that reduces its ornamental value. Understanding the molecular mechanism underlying this transition is essential for stabilizing the golden leaf phenotype. This study investigates the physiological, structural, and molecular changes accompanying regreening and tests whether the Golden stage represents a state of hormone-mediated developmental arrest.

The regreening process was characterized across three stages: Golden, Yellowish-Green (YG), and Green. The color transition from golden to green was attributed to a marked increase in the chlorophyll-to-carotenoid ratio, resulting from net chlorophyll accumulation against a stable carotenoid background. This metabolic change was accompanied by extensive reorganization of leaf anatomy and chloroplast ultrastructure. Golden stage chloroplasts exhibited loosely stacked thylakoids, indicating delayed development, while YG and Green stages showed progressive structural maturation alongside features of early senescence, including indistinct thylakoid membranes and degenerating mitochondrial cristae. Transcriptomic and metabolomic analyses revealed coordinated reprogramming of pigment metabolism. Chlorophyll biosynthesis genes (HEMA, CHLH, CAO) were upregulated while degradation genes (NYC-like) were downregulated, driving chlorophyll accumulation. Concurrently, carotenoid biosynthesis genes, including the MEP pathway gene DXS and core biosynthetic gene PSY3, were suppressed, while cleavage genes (CCDs) were induced, leading to reduced carotenoid accumulation. Metabolomic data showed no accumulation of chlorophyll intermediates, suggesting a delay between transcriptional activation and functional enzyme assembly. Endogenous hormone quantification showed that multiple bioactive gibberellins (GA₁, GA₃, GA₄) and abscisic acid (ABA) were significantly elevated in the Golden stage compared to the YG stage. Exogenous application of GA₃ and ABA in combination suppressed regreening and maintained the golden phenotype. This co-treatment reproduced the transcriptional signature of the Golden stage by upregulating the chlorophyll degradation gene NYC-like while downregulating both the carotenoid biosynthesis gene PSY3 and cleavage genes CCDs.

These findings demonstrate that the Golden stage in U. pumila ‘Jinye’ represents a state of developmental arrest synergistically maintained by elevated GA and ABA levels. This hormonal environment establishes a transcriptional program that maintains pigment metabolism into a high carotenoid/chlorophyll ratio and delays chloroplast maturation. Regreening results from the release of this arrest, coupling pigment metabolic reprogramming with the resumption of chloroplast development. This conceptual framework advances our understanding of leaf color regulation in woody plants and identifies GA/ABA signaling as potential targets for extending the ornamental phase of golden-leaf cultivars.