Plastoglobules compartmentalize nitrogen assimilation in maize

Article Plastoglobules compartmentalize nitrogen assimilation in maize https://doi.org/10.1038/s41586-026-10610-8 Received: 8 September 2025 Accepted: 29 April 2026 Di Chen1,9, Lulu Gao1,9, Shujun Li1,9, Yiqiu Cheng2,3, Xiaoxian Wu2, Wenhao Li1, Jinman Zhang1, Xueling Fu1, Pan Xiang1, Lu Sun1, Zhiteng Chen1, Hua Zhang1, Youliang Li1, Shiqi Luo1, Chong You1, Linhan Sun4, Xing Huang2, Yidong Zhu2, Xing Zeng5, Wenqin Wang6, Yan He7, Haihai Wang2, Yu Zhang2, Xuewei Chen1, Yongrui Wu2,8 ✉ & Yongcai Huang1 ✉ Published online: xx xx xxxx Open access Check for updates Efficient nitrogen assimilation is important for sustainable agriculture1, yet its subcellular organization remains unknown. Here we show that plastoglobules (PGs) in the chloroplasts of mesophyll cells function as a metabolic hub that orchestrates nitrogen utilization in maize. Nitrogen-responsive dynamics of PGs represent a conserved feature across plant species. We identify two key enzymes, nitrite reductase 2 (ZmNIR2) and glutamine synthetase 1 (ZmGLN1), specifically targeted to PGs by a chloroplast transit peptide and hydrophobic region. Cryogenic electron microscopy analysis of recombinant ZmGLN1 shows a decameric complex, enabling a metabolon with ZmNIR2 for enhanced efficiency. Among two NIR and six GLN enzymes, ZmNIR2 and ZmGLN1 are the primary PG-localized components that orchestrate sub-organellar nitrogen assimilation and dictate nitrogen use efficiency. Genetic variation in ZmNIR2 splicing in cultivated germplasm generates a PG-targeted isoform (ZmNIR2T1) that boosts NUE. Our work establishes PGs as a central compartment for primary nitrogen assimilation, providing a promising strategy to develop high-NUE crops for global food security. Nitrogen (N) is essential for plant growth and agricultural productivity, directly underpinning global food security. However, improving crop nitrogen use efficiency (NUE) remains a global challenge. Approximately 70% of applied N fertilizer is inefficiently used, with maize NUE often below 30% (ref. 1). This inefficiency causes economic burdens and environmental degradation. Enhancing crop NUE is an urgent imperative. Maize is a globally important cereal crop for food, feed and industry2. As a highly domesticated C4 plant, maize exhibits a strong physiological interdependence among its growth, development and nitrogen utilization3. Many agricultural systems worldwide are at present grappling with the dual challenges of yield dependence on increased nitrogen input and inherently low NUE, highlighting an urgent need for fundamental breakthroughs in nitrogen utilization mechanisms in crops4,5. Maize NUE is a complex trait influenced by nitrogen absorption, assimilation and remobilization. Nitrogen assimilation is important for converting inorganic nitrogen into organic forms, directly affecting growth and yield. Although plants primarily absorb nitrate (NO3−) and ammonium (NH4+), the subcellular organization of this pathway remains a key determinant of efficiency. Maize, a typical C4 plant, possesses Kranz anatomy in its leaves, characterized by concentric layers of outer mesophyll cells (MCs) and inner bundle sheath cells (BSCs) that tightly encase the vascular bundles. Previous studies have shown that the key enzymes for primary nitrogen assimilation, nitrate reductase (NR) and nitrite reductase (NIR), are localized exclusively in MCs6. By contrast, although glutamine synthetase (GLN, also known as GS) is present in both cell types, ferredoxin-dependent glutamate synthase (Fd-GOGAT) is almost entirely confined to the chloroplasts of BSCs7. Consequently, the proposed model for the cellular compartmentalization of nitrogen assimilation suggests that, during primary nitrogen assimilation, MCs harbouring NR, NIR and GLN play an important part in synthesizing glutamine from NO3−. Following root uptake and transport to the leaves by the vasculature, NO3− diffuses into MCs. In the cytoplasm, NR reduces NO3− to nitrite (NO2−) using nicotinamide adenine dinucleotide (NADH) as an electron donor8,9. Subsequently, NO2− is transported into chloroplasts, where NIR reduces it to NH4+ using reduced Fd supplied by the photosynthetic electron transport chain. GLN then converts the free NH4+ into glutamine (Gln), thereby facilitating the conversion of inorganic to organic nitrogen10,11. Concurrently, the high level of Fd-GOGAT present in BSCs may drive substantial glutamate synthesis, completing the GS-GOGAT cycle required for the synthesis of amino acids and other organic compounds12. It is important to note that NO2− and NH4+ are intermediates in early nitrogen assimilation; their accumulation to toxic levels can damage plant cells13. Therefore, the spatial organization provided by cellular compartmentalization is crucial for ensuring orderly nitrogen assimilation, facilitating both rapid nitrogen processing and the detoxification of metabolic intermediates. Although mutant analyses and quantitative trait locus State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu, China. 2State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology & Ecology, Chinese Academy of Sciences, Shanghai, China. 3University of the Chinese Academy of Sciences, Beijing, China. 4Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, PA, USA. 5College of Agriculture, Northeast Agricultural University, Harbin, China. 6Shanghai Key Laboratory of Plant Molecular Sciences, Shanghai Collaborative Innovation Center of Plant Germplasm Resources Development, College of Life Sciences, Shanghai Normal University, Shanghai, China. 7Key Laboratory of Seed Innovation, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China. 8 Shanghai Academy of Natural Sciences, Shanghai, China. 9These authors contributed equally: Di Chen, Lulu Gao, Shujun Li. ✉e-mail: ; 1 Nature | www.nature.com | 1 Article cloning have identified several nitrogen utilization genes, such as nitrate transporter1.1B (NRT1.1B), GROWTH-REGULATING FACTOR 4 (GRF4), TEOSINTE-BRANCHED1/CYCLOIDEA/PCF 19 (TCP19), NITROGENMEDIATED TILLER GROWTH RESPONSE 5 (NGR5) in rice (Oryza sativa L.) and TEOSINTE HIGH PROTEIN 9 (THP9) in maize, and validated their roles in enhancing NUE14–18, the patterns of nitrogen assimilation within internal subcellular compartments, as well as the core mechanisms regulating them, need to be explained. Cells contain various distinct, compartmentalized structures, including organelles and membrane-less biomolecular condensates, which are essential for survival and the efficient execution of biological functions. These compartments provide spatial organization and serve as independent microenvironments for biochemical reactions, thereby facilitating the orderly and efficient progression of intra (...truncated)