Integrative metabolome and transcriptome of different tree size reveal wood formation in Corymbia citriodora

Corymbia citriodora wood holds extensive application value; however, due to the cross-pollination nature of C. citriodora and the significant genetic variation among offspring, a phenomenon is observed in plantations where trees with the same parental lineage exhibit varying diameter at breast height (DBH). In this study, we hypothesized that the observed DBH variation reflects two divergent adaptation strategies under winter conditions: smaller trees may exhibit heightened cold sensitivity, activating stress responses and entering early dormancy, whereas larger trees may sustain cambial activity through coordinated regulation of cell-cycle genes and carbohydrate metabolism.

Metabolomics showed large trees enriched in phenolic compounds like picroside I and orientin. Transcriptomics revealed their genes were enriched in cell cycle and phenylalanine/tyrosine metabolism pathways, whereas small trees were enriched in abscisic acid (ABA) pathways. Integrated analysis revealed three patterns of transcript-metabolite coordination: (i) concordant upregulation (e.g., shikimate dehydrogenase (SDH)-shikimic acid), (ii) discordant regulation suggesting post-transcriptional control (raffinose accumulation without raffinose synthase (RFS) upregulation in small trees), and (iii) pathway-level flux redirection (phenylpropanoid pathway). Systematically, during winter, small trees exhibited stress-sensitive signatures, characterized by 9-cis-epoxycarotenoid dioxygenase (NCED), pyrabactin resistance/pyrabactin resistance-like (PYR/PYL), ABA-responsive element binding factor (ABF) upregulation, accumulation of raffinose, and transcriptional shift toward lignification (cinnamyl-alcohol dehydrogenase (CAD), peroxidase upregulation). Conversely, large trees showed molecular profiles indicative of stronger adaptability, with transcriptional signatures consistent with continued cell division (E2F transcription factor 3 (E2F3), mini-chromosome maintenance (MCM2/4/5/6) upregulation), cytoskeletal organization (kinesin KIN12B), and active carbohydrate metabolism (sucrose synthase (SUS), trehalose-6-phosphate phosphatase (TPP), alpha-amylase (AMY) upregulation), accumulating cinnamate and shikimic acid.

This study advances understanding of tree growth variation by demonstrating that winter conditions reveal divergent adaptation strategies linked to DBH. The key conceptual advance is the integration of stress signaling, carbon metabolism, and cell-wall regulation into a unified framework where differential dormancy timing explains within-family growth variation. Large trees maintain a permissive growth state through coordinated upregulation of cell-cycle, cytoskeletal, and biosynthetic genes, while small trees exhibit coordinated stress responses that accelerate dormancy. These findings provide species-specific targets for functional validation-including E2F3, KIN12B, and NCED-and suggest that breeding for sustained winter cambial activity could enhance biomass production in subtropical plantations.