Transcriptomic and metabolomic unraveling of nitrogen use efficiency in sorghum: the quest for molecular adaptations to low-nitrogen stress

Sorghum (Sorghum bicolor L. Moench), renowned for its resilience in marginal environments, frequently encounters productivity limitations due to insufficient nitrogen (N) availability. This investigation employed transcriptomic and metabolomic approaches to elucidate the mechanisms underlying nitrogen use efficiency (NUE) in two sorghum genotypes, 398B and CS3541, exhibiting contrasting NUE responses to low-N stress. N deficiency significantly diminished plant height, root dry weight, and leaf dry weight in both genotypes, while markedly increasing root length. Notably, 398B demonstrated a pronounced increase in root length and exhibited higher nitrogen uptake efficiency (NUpE) and utilization efficiency (NUtE) compared to CS3541. Transcriptomic analyses revealed that starch and sucrose metabolism, as well as phenylpropanoid biosynthesis pathways, were significantly enriched in both genotypes, indicative of enhanced carbon (C) and N metabolism. Notably, two low-affinity nitrate transporter genes (Sobic.001G302800.v3.2, NRT1/PTR6.3 and Sobic.004G193000.v3.2, NRT1/PTR6.4) were upregulated in 398B roots under N deficiency, suggesting a crucial role in facilitating N uptake. Metabolomic profiling of sorghum leaves under low-N conditions highlighted an accumulation of phenolic acids, flavonoids, flavanols, and saccharides in 398B, suggesting improved N utilization and assimilation. Overall, integrated transcriptome and metabolome analyses identified key genes and metabolites associated with NUE. Our findings provide novel insights into the genetic and molecular basis of NUE in sorghum, particularly emphasizing the role of root structural adaptations and the regulation of specific transporter genes in enhancing NUpE. Additionally, our study underscored the importance of metabolic adjustments in leaves for improving NUtE. These results contribute to the development of sorghum genotypes with enhanced NUE, offering the potential for sustainable agricultural practices in low-N environments.