Systemic regulation of nodule structure and assimilated carbon distribution by nitrate in soybean

Sha Li; Chengbin Wu; Hao Liu; Xiaochen Lyu; Fengsheng Xiao; Shuhong Zhao; Chunmei Ma; Chao Yan; Zhilei Liu; Hongyu Li; Xuelai Wang; Zhenping Gong

doi:10.3389/fpls.2023.1101074

Systemic regulation of nodule structure and assimilated carbon distribution by nitrate in soybean

Front Plant Sci. 2023 Feb 6:14:1101074. doi: 10.3389/fpls.2023.1101074. eCollection 2023.

Authors

Sha Li¹, Chengbin Wu¹, Hao Liu², Xiaochen Lyu², Fengsheng Xiao², Shuhong Zhao³, Chunmei Ma², Chao Yan², Zhilei Liu¹, Hongyu Li², Xuelai Wang², Zhenping Gong²

Affiliations

¹ College of Resources and Environment, Northeast Agricultural University, Harbin, China.
² College of Agriculture, Northeast Agricultural University, Harbin, China.
³ College of Engineering, Northeast Agricultural University, Harbin, China.

Abstract

Background: The nitrate regulates soybean nodulation and nitrogen fixation systemically, mainly in inhibiting nodule growth and reducing nodule nitrogenase activity, but the reason for its inhibition is still inconclusive.

Methods: The systemic effect of nitrate on nodule structure, function, and carbon distribution in soybean (Glycine max (L.) Merr.) was studied in a dual-root growth system, with both sides inoculated with rhizobia and only one side subjected to nitrate treatment for four days. The non-nodulating side was genetically devoid of the ability to form nodules. Nutrient solutions with nitrogen concentrations of 0, 100, and 200 mg L^-1 were applied as KNO₃ to the non-nodulating side, while the nodulating side received a nitrogen-free nutrient solution. Carbon partitioning in roots and nodules was monitored using ¹³C-labelled CO₂. Other nodule responses were measured via the estimation of the nitrogenase activity and the microscopic observation of nodule ultrastructure.

Results: Elevated concentrations of nitrate applied on the non-nodulating side caused a decrease in the number of bacteroids, fusion of symbiosomes, enlargement of the peribacteroid spaces, and onset of degradation of poly-β-hydroxybutyrate granules, which is a form of carbon storage in bacteroids. These microscopic observations were associated with a strong decrease in the nitrogenase activity of nodules. Furthermore, our data demonstrate that the assimilated carbon is more likely to be allocated to the non-nodulating roots, as follows from the competition for carbon between the symbiotic and non-symbiotic sides of the dual-root system.

Conclusion: We propose that there is no carbon competition between roots and nodules when they are indirectly supplied with nitrate, and that the reduction of carbon fluxes to nodules and roots on the nodulating side is the mechanism by which the plant systemically suppresses nodulation under nitrogen-replete conditions.

Keywords: carbon distribution; dual-root soybean; nitrate; nodule structure; symbiosome.

Grants and funding

This work was supported by the National Key Research and Development Programme, Integration and Demonstration of High Quality, Simple and Efficient Cultivation Techniques for Soybean: [Grant Number 2020YFD1000903]; Heilongjiang Provincial Postdoctoral Science Foundation [NO. LBH-Z22074].