Post-anthesis dry matter production and leaf nitrogen distribution are associated with root-derived cytokinins gradient in rice

doi:10.1016/j.jia.2024.02.010

Journal of Integrative Agriculture

2025, Vol. 24

Issue (6): 2106-2122 DOI: 10.1016/j.jia.2024.02.010

Crop Science

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Post-anthesis dry matter production and leaf nitrogen distribution are associated with root-derived cytokinins gradient in rice

Kuanyu Zhu¹, Yuemei Xu¹, Zhiwei Sun¹, Yajun Zhang¹, Weiyang Zhang¹, Yunji Xu², Junfei Gu¹, Hao Zhang¹, Zhiqin Wang^1#, Lijun Liu¹, Jianhua Zhang³, Jianchang Yang¹

¹Jiangsu Key Laboratory of Crop Genetics and Physiology/Jiangsu Key Laboratory of Crop Cultivation and Physiology/Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops/Agricultural College, Yangzhou University, Yangzhou 225009, China

²Joint International Research Laboratory of Agriculture and Agri-Product Safety of Ministry of Education and Yangzhou University, Yangzhou 225009, China

³Department of Biology, Hong Kong Baptist University, Hong Kong 999077, China

Highlights
● A steeper nitrogen (N) distribution can enhance N utilization efficiency and dry matter production in rice.
● Such N distribution is driven by a larger gradient of zeatin (Z) and zeatin riboside (ZR) levels in leaves.
● Higher root activity is essential for maintaining the gradient of Z+ZR levels.

Abstract
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摘要

调整叶片氮分布来匹配光梯度分布，对于促进作物冠层干物质生产和提高氮利用效率至关重要。然而，有关根源细胞分裂素梯度与水稻叶片氮分布之间的关系及其对干物质生产的影响和潜在机制，知之甚少。本研究采用了2个粳型氮高效品种（NEVs）和2个粳型氮低效品种（NIVs）种植于大田，且它们之间光消减系数（K_L）差异较小，设置了4个施氮量（0、90、180和360 kg N ha⁻¹）水平。结果表明，在较低的施氮量（0-180 kg N ha⁻¹）下，与NIVs相比，NEVs在成熟期具有较高的地上部干物重、产量和植株内在氮利用率（IE_N），但两类品种的总吸氮量接近。与NIVs相比，NEVs在灌浆中前期，叶片中呈现出更大的氮分布梯度，即较高的氮衰减系数（K_N）；较大的氮分布梯度在较低的施氮量下，促进了NEVs花后的光合生产。此外，与NIVs相比，NEVs叶片中玉米素（Z）+玉米素核苷（ZR）梯度较大（即上部叶与下部叶之间的Z+ZR水平比值高）、下部叶中氮输出和根中装载细胞分裂素的关键基因表达水平较高以及上部叶中氮同化相关的酶活性也较强。相关分析和随机森林分析表明，Z+ZR梯度、K_N和干物质生产之间呈极显著正相关，并且较大的Z+ZR梯度促进了氮在下部叶片中的输出和在上部叶片中的同化，对K_N和干物质生产具有显著的贡献作用。这一过程也与NEVs较高的根系活性密切相关，包括根系氧化力、根中Z+ZR含量和Z+ZR的装载能力。我们通过往根部浇灌根系活性促进剂和抑制剂验证了这一结果。有趣的是，在施氮量为360 kg N ha⁻¹时，NEVs和NIVs都展现出无差异的植物性状且达到了超高产水平（产量超过10.5 t ha⁻¹），但两类品种的IE_N非常低。总之，水稻叶片中较高的Z+ZR梯度可以提高K_N和干物质生产，但需要保持较高的根系活力，进而获得高产和氮高效利用。今后需要进一步探索和开发减氮的栽培措施，以实现氮高效水稻品种的超高产潜力。

Abstract

Aligning leaf nitrogen (N) distribution to match the light gradient is crucial for maximizing canopy dry matter production (DMP) and improving N utilization efficiency. However, the relationship between the gradient of root-derived cytokinins and N distribution in rice leaves and its impact on DMP and the underlying mechanisms remains poorly understood. A two-year field experiment was conducted using two japonica N-efficient varieties (NEVs) and two japonica N-inefficient varieties (NIVs) under four different N rates (0, 90, 180, and 360 kg N ha⁻¹). These selected varieties exhibited similar values in the coefficient of light extinction (K_L). Results showed that at lower N rates (0–180 kg N ha⁻¹), the NEVs exhibited greater dry matter weight at maturity, higher grain yield, and improved internal N use efficiency (IE_N) compared to the NIVs, despite possessing comparable total N uptake. Compared with the NIVs, the NEVs exhibited a more pronounced nitrogen distribution gradient in leaves, as indicated by the coefficient of nitrogen extinction (K_N) values during the middle and early grain-filling stages. This enhanced gradient led to improved coordination between light and nitrogen, resulting in greater photosynthetic production, particularly at lower N rates. Furthermore, the NEVs demonstrated a larger gradient of zeatin (Z)+zeatin riboside (ZR) in leaves (i.e., higher ratios of Z+ZR levels between upper and lower leaves), enhanced expression levels of genes related to N export in lower leaves and Z+ZR loading in the root, respectively, elevated enzymes activities related to N assimilation in upper leaves, in relative to the NIVs. Correlation and random forest analyses demonstrated a strong positive correlation between the Z+ZR gradient, K_N, and DMP, and the gradient facilitated the export of N from lower leaves and its assimilation in upper leaves, contributing significantly to both K_Nand DMP. This process was closely linked to root activity, including root oxidation activity, root Z+ZR content, and Z+ZR loading capacity, as confirmed by applying an inhibitor or a promoter of cytokinins biosynthesis to roots. Interestingly, at the N rate of 360 kg N ha⁻¹, both NEVs and NIVs showed indistinguishable plant traits, achieving a super high-yielding level (over 10.5 t ha⁻¹) but with remarkably low IE_N. The results suggest that increasing the Z+ZR gradient can improve K_N and DMP, where it needs to maintain higher root activity, thus leading to high yield and high IE_N. Further research is needed to explore and develop cultivation practices with reduced N to unlock the super-high-yielding potential of the NEVs.

Keywords: rice (Oryza sativa L.) grain yield dry matter production cytokinins gradient N distribution internal N use efficiency

Received: 06 October 2023 Online: 08 February 2024 Accepted: 12 December 2023

Fund:

This work was supported by the National Natural Science Foundation of China (32301930, 32071943, 32272198, and 32372214), the Major Program of the Ministry of Agriculture and Rural Affairs of China (FSNK202218080316), the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD-2020-01), the Jiangsu Funding Program for Excellent Postdoctoral Talent, China (2022ZB618), the Government Funding to the Chinese University of Hong Kong State Key Laboratory of Agrobiotechnology via Innovation and Technology Commission, China (2022/23–2023/24), and the National Key Research and Development Program of China (2022YFD2300304).

About author: Kuanyu Zhu, Tel/Fax: +86-514-87979317, E-mail: kyzhu@yzu.edu.cn; #Correspondence Zhiqin Wang, Tel/Fax: +86-514-87979317, E-mail: zqw@yzu.edu.cn

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Kuanyu Zhu, Yuemei Xu, Zhiwei Sun, Yajun Zhang, Weiyang Zhang, Yunji Xu, Junfei Gu, Hao Zhang, Zhiqin Wang, Lijun Liu, Jianhua Zhang, Jianchang Yang. 2025. Post-anthesis dry matter production and leaf nitrogen distribution are associated with root-derived cytokinins gradient in rice. Journal of Integrative Agriculture, 24(6): 2106-2122.

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