Phosphorus availability influences disease-suppressive soil microbiome through plant-microbe interactions
Yifan Cao,
Zongzhuan Shen,
Na Zhang,
Xuhui Deng,
Linda S. Thomashow,
Ian Lidbury,
Hongjun Liu,
Rong Li,
Qirong Shen,
George A. Kowalchuk
Affiliations
Yifan Cao
The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University
Zongzhuan Shen
The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University
Na Zhang
The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University
Xuhui Deng
The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University
Linda S. Thomashow
Wheat Health, Genetics and Quality Research Unit, Washington State University
Ian Lidbury
Molecular Microbiology, School of Biosciences, University of Sheffield
Hongjun Liu
The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University
Rong Li
The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University
Qirong Shen
The Sanya Institute of the Nanjing Agricultural University, Key Lab of Organic-Based Fertilizers of China, Jiangsu Provincial Key Lab for Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University
George A. Kowalchuk
Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, Utrecht University
Abstract Background Soil nutrient status and soil-borne diseases are pivotal factors impacting modern intensive agricultural production. The interplay among plants, soil microbiome, and nutrient regimes in agroecosystems is essential for developing effective disease management. However, the influence of nutrient availability on soil-borne disease suppression and associated plant-microbe interactions remains to be fully explored. T his study aims to elucidate the mechanistic understanding of nutrient impacts on disease suppression, using phosphorous as a target nutrient. Results A 6-year field trial involving monocropping of tomatoes with varied fertilizer manipulations demonstrated that phosphorus availability is a key factor driving the control of bacterial wilt disease caused by Ralstonia solanacearum. Subsequent greenhouse experiments were then conducted to delve into the underlying mechanisms of this phenomenon by varying phosphorus availability for tomatoes challenged with the pathogen. Results showed that the alleviation of phosphorus stress promoted the disease-suppressive capacity of the rhizosphere microbiome, but not that of the bulk soil microbiome. This appears to be an extension of the plant trade-off between investment in disease defense mechanisms versus phosphorus acquisition. Adequate phosphorus levels were associated with elevated secretion of root metabolites such as L-tryptophan, methoxyindoleacetic acid, O-phosphorylethanolamine, or mangiferin, increasing the relative density of microbial biocontrol populations such as Chryseobacterium in the rhizosphere. On the other hand, phosphorus deficiency triggered an alternate defense strategy, via root metabolites like blumenol A or quercetin to form symbiosis with arbuscular mycorrhizal fungi, which facilitated phosphorus acquisition as well. Conclusion Overall, our study shows how phosphorus availability can influence the disease suppression capability of the soil microbiome through plant-microbial interactions. These findings highlight the importance of optimizing nutrient regimes to enhance disease suppression, facilitating targeted crop management and boosting agricultural productivity. Video Abstract
