Multi-omics analysis on an agroecosystem reveals the significant role of organic nitrogen to increase agricultural crop yield

Significance In 1840, Justus von Liebig proposed the theory of mineral plant nutrition, through the invention of the Haber–Bosch process, leading to the industrialization of chemical fertilizer (inorganic nitrogen) to feed the human population. Because the excessive use of chemical fertilizer has led to numerous environmental problems, understanding the agroecosystem that contains plants, microbes, and soils is necessary for sustainable agriculture. We revealed the network structure of an agroecosystem established with different management practices and identified that organic nitrogen is a key component contributing to crop yield under the condition of soil solarization, even in the presence of inorganic nitrogen. Our finding provides a potential solution to make crop production more sustainable by utilizing organic nitrogen induced by soil solarization.
Both inorganic fertilizer inputs and crop yields have increased globally, with the concurrent increase in the pollution of water bodies due to nitrogen leaching from soils. Designing agroecosystems that are environmentally friendly is urgently required. Since agroecosystems are highly complex and consist of entangled webs of interactions between plants, microbes, and soils, identifying critical components in crop production remain elusive. To understand the network structure in agroecosystems engineered by several farming methods, including environmentally friendly soil solarization, we utilized a multiomics approach on a field planted with Brassica rapa. We found that the soil solarization increased plant shoot biomass irrespective of the type of fertilizer applied. Our multiomics and integrated informatics revealed complex interactions in the agroecosystem showing multiple network modules represented by plant traits heterogeneously associated with soil metabolites, minerals, and microbes. Unexpectedly, we identified soil organic nitrogen induced by soil solarization as one of the key components to increase crop yield. A germ-free plant in vitro assay and a pot experiment using arable soils confirmed that specific organic nitrogen, namely alanine and choline, directly increased plant biomass by acting as a nitrogen source and a biologically active compound. Thus, our study provides evidence at the agroecosystem level that organic nitrogen plays a key role in plant growth.