Multi-omics reveals collapse of flavonoid, hormone and carbohydrate networks underlying sterility in Lagerstroemia indica ‘Xiangyun’

Sterility is an important trait in ornamental plants because it can prolong flowering, reduce fruiting burden, and increase horticultural and industrial value. Lagerstroemia indica L. is an important ornamental woody species and a potential source of pharmacologically active metabolites and essential oils, yet the reproductive sterility mechanism of the sterile cultivar ‘Xiangyun’ remains unclear. This study aimed to clarify the cytological, physiological, transcriptomic, and metabolomic basis of sterility in ‘Xiangyun’ by comparing sterile and fertile floral buds at different developmental stages. Cytological observations showed that sterile flowers developed indehiscent anthers with collapsed, non-viable pollen grains and ovules lacking functional embryo sacs, indicating concurrent defects in male and female gametophyte development. Physiological analyses revealed marked reductions in soluble sugars, soluble proteins, and proline, together with increased malondialdehyde (MDA) content and altered antioxidant enzyme activities, consistent with oxidative stress and energy deficiency. Transcriptomic and metabolomic analyses further demonstrated broad repression of flavonoid biosynthesis, particularly through the downregulation of chalcone synthase ( CHS ) and flavonol synthase ( FLS ), accompanied by depletion of kaempferol, quercetin, and related flavonols. Plant hormone and carbohydrate pathways were also disrupted: indole-3-acetic acid (IAA) and abscisic acid (ABA) signaling became imbalanced, whereas sucrose and glucose metabolism was impaired through reduced expression of sucrose synthase and key glycolytic genes. Furthermore, stage-resolved multi-omics reanalysis revealed coordinated module-level coupling among flavonoid, carbohydrate, redox, hormone, and reproductive-development pathways, and prioritized MYB26 and MYB108 as evidence-ranked candidate hub transcription factors. Taken together, these results support a molecular model in which transcriptional regulatory disruption leads to the coordinated collapse of flavonoid, hormone, and carbohydrate networks, ultimately causing dual gametophytic sterility in ‘Xiangyun’. This study provides a mechanistic framework for understanding sterility in Lagerstroemia indica and offers a basis for the breeding and utilization of sterile ornamental germplasm.