Abstract
BACKGROUND: Sugar beet (Beta vulgaris L.) is a globally important sucrose-producing crop. As a “nitrogen (N)-responsive species”, it specifically relies on precise N management to maximize agroeconomic potential. However, excessive N application reduces sucrose accumulation efficiency and elevates non-sucrose constituents despite increasing root biomass. Clarifying the molecular regulatory mechanisms underlying low nitrogen (LN) response is therefore essential for improving nitrogen use efficiency (NUE) of sugar beet. RESULTS: Comparative transcriptomics of sugar beet germplasm ‘780016B/12 Superior’ under normal (CV, 5 mmol/L N) and low nitrogen (LN, 0.5 mmol/L N) conditions after 12 h of treatment identified 120 and 254 differentially expressed long non-coding RNAs (DELs) in foliage and roots, respectively. Functional annotation of 1,454 long noncoding RNA-message RNA (lncRNA-mRNA) pairs (trans/cis = 3.47:1) revealed the coordinated regulation of DEL-target genes in nitrogen metabolism, transmembrane transport, and plant hormone signal transduction. Within these LN responsive networks, lncRNAs of XR_791134.2 and LNC_011801 functioned as key components, which correlated with glutamine synthetase (GS2)-mediated ammonium assimilation and auxin transporter-like protein (AUX2/3/4) suppression redirecting nitrogen resources, respectively. Additionally, competing endogenous RNA (ceRNA) networks further integrated hormonal signaling with nitrogen sensing. Specifically, lncRNA LNC_016830 is situated at a critical junction point, that interacted with miR396a/b-5p to regulate auxin-sensitive transcription factors GRF7/9 and coordinated ABA signaling through CRWN3-mediated ABI5 degradation. Crucially, most of ceRNA-associated mRNAs were targets of growth-suppressing hormones, including the brassinosteroid receptor SR160, a dual regulator that links lncRNA networks to steroid-mediated stress responses. CONCLUSIONS: This study reveals lncRNAs as key correlates balancing nitrogen assimilation and developmental plasticity in sugar beet, and provides molecular targets for breeding high NUE cultivars. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-025-12301-6.