LncRNA-mediated early regulatory networks in sugar beet (Beta vulgaris L.) response to low nitrogen

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. 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. 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.