Nitrogen deficiency impacts growth and modulates carbon metabolism in maize

Abstract

Nitrogen (N) deficiency in maize regulates carbon (C) metabolism by enhancing sugar and starch metabolism and related gene expression in both shoots and roots, while increasing root competition for assimilates causing carbohydrate accumulation in leaves and sheaths due reduced translocation to sink tissues. Soluble sugars are vital for plant development, with nitrogen (N) availability playing a key role in their distribution across plant organs, ultimately shaping growth patterns. However, the regulatory mechanisms governing carbon (C) assimilate allocation and utilization under different N forms remain unclear. This study examined C fixation, utilization, and spatial distribution in hydroponically grown maize seedlings subjected to four N treatments: 1 mM NO₃⁻ (low N, LN), 2 mM NO₃⁻ (medium N), 10 mM NO₃⁻ (high N), and 1 mM NH₄⁺ (low ammonium, LA). LN treatment significantly increased soluble sugar and starch contents while promoting greater root biomass at the expense of shoot biomass, leading to a higher root-to-shoot assimilate allocation. The activities of sugar and starch metabolism enzymes were more tightly regulated in both shoots and roots under LN, indicating enhanced C utilization and increased competition for assimilates, particularly in the root. Key genes involved in above-ground sugar and starch metabolism, ZmSPS1, ZmSuSy1, ZmCINV1, ZmVINV1, ZmCWINV1, ZmSTP2, ZmSUC2, ZmSWEET14, ZmSS1, ZmAMY1, ZmBAM1, and ZmAGPase1, were upregulated under LN, correlating with enhanced enzyme activity and resulting increased sugar and starch accumulation. Starch and sucrose accumulated more in LN-treated leaves than in other N treatments, with starch primarily stored in leaf tips and sucrose concentrated in the leaf sheath. This pattern suggests that excess C accumulation results from inefficient C utilization in sink tissues rather than impaired C assimilation. These findings provide new insights into how LN modulates C partitioning between leaves and roots for stress adaptation, highlighting the importance of improving C utilization in sink tissues to mitigate N deficiency and enhance plant growth.

Keywords: Carbon partitioning and accumulation; Low nitrogen; Root-to-shoot ratio; Sink–source dynamics; Sugar and starch metabolism.

Fig. 1

Effect of different nitrogen forms on glucose, fructose, sucrose, and starch content in the leaves (A, C, E, G) and roots (B, D, F, H) of maize inbred line TX-40 J. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW fresh weight; LN low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 2

Effect of different nitrogen forms on sucrose phosphate synthase, sucrose synthase, sucrose synthase, ADP-glucose pyrophosphorylase and starch synthase activity in the leaves (A, C, E, G) and roots (B, D, F, H) of maize inbred line TX-40 J. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW fresh weight; LN low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 3

Effect of different nitrogen forms on the expression pattern of sugar-metabolizing genes. Expression level of ZmSuSy1, ZmSPS1, ZmCINV1, and ZmVINV1 in the leaves (A, C, E, G) and roots (B, D, F, H) of maize inbred line TX-40 J. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW fresh weight; LN low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 4

Effect of different nitrogen forms on the expression pattern of sugar-metabolizing and sucrose transporter genes. Expression level of ZmCWINV1, ZmSTP2, ZmSUC2, and ZmSWEET14 in the leaves (A, C, E, G) and roots (B, D, F, H) of maize inbred line TX-40 J. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW fresh weight; LN low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 5

Effect of different nitrogen forms on the expression pattern of starch metabolizing genes. Expression level of ZmSS1, ZmAMY1, ZmBAM1, and ZmAGPase1 in the leaves (A, C, E, G) and roots (B, D, F, H) of maize inbred line TX-40 J. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW fresh weight; LN low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 6

Diurnal changes in leaf sucrose (A) and starch (B) at 20 days after treatment (DAT) and leaf sucrose (C) and starch (D) at 40 DAT under different nitrogen treatments. Samples were collected at 7:00, 12:00, 17:00, 22:00, and 7:00 on the second day. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW fresh weight; LN low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 7

Sucrose (A) and starch (B) synthesis and sucrose (C) and starch (D) degradation in the leaves of maize inbred line TX-40 J grown under varying nitrogen treatments. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW, fresh weight; LN, low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 8

Leaf sucrose (A) and starch (B) at 20 DAT, and leaf sucrose (C) and starch (D) at 40 DAT in different tissues under various nitrogen form treatments. Data are presented as mean ± SE (n = 6). Statistical significance was determined using Tukey’s multiple range test (P ≤ 0.05), with different letters indicating significant differences between treatments. FW fresh weight; LN low nitrogen (N deficiency); MN moderate nitrogen; HN high nitrogen; LA low ammonium treatment

Fig. 9

A proposed model of sugar regulation in maize seedlings in response to N deficiency (low nitrogen; LN). LN triggers a sugar-mediated tandem reaction, enhancing maize tolerance to N deficiency. N limitation stress modifies the expression of key regulatory metabolic genes and the activities of sugar metabolism enzymes. This modulation influences sugar accumulation and activates sugar transporter transcription, thereby regulating sugar allocation for environmental adaptation. Upward red arrows represent upregulated components