Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula

• Published in: Plant, cell and environment cell and environment, 2019-01, Vol.42 (1), p.270-284
• Main Authors: Kafle, Arjun, Garcia, Kevin, Wang, Xiurong, Pfeffer, Philip E., Strahan, Gary D., Bücking, Heike
• Format: Article
• Language: English
• Subjects: Access control; Alfalfa; arbuscular mycorrhizal symbiosis; Arbuscular mycorrhizas; Carbon; Carbon - metabolism; carbon transport; Demand; Ensifer meliloti; Fungi; Gene expression; Host Microbial Interactions - physiology; Host plants; Legumes; Medicago truncatula; Medicago truncatula - metabolism; Medicago truncatula - microbiology; Medicago truncatula - physiology; Membrane Transport Proteins - metabolism; Mycorrhizae - metabolism; Mycorrhizae - physiology; Nitrogen; Nitrogen - metabolism; nitrogen uptake; Nitrogenase - metabolism; Nutrient uptake; Nutrients; Phosphorus - metabolism; Plant Proteins - metabolism; Plant Roots - metabolism; Plant Roots - microbiology; rhizobia; Rhizophagus irregularis; Sucrose; sucrose transport; sucrose uptake transporter (SUT); Sugar; sugars will eventually be exported transporter (SWEET); Symbionts; Symbiosis; Transcriptome
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13359

Legumes form tripartite interactions with arbuscular mycorrhizal fungi and rhizobia, and both root symbionts exchange nutrients against carbon from their host. The carbon costs of these interactions are substantial, but our current understanding of how the host controls its carbon allocation to individual root symbionts is limited. We examined nutrient uptake and carbon allocation in tripartite interactions of Medicago truncatula under different nutrient supply conditions, and when the fungal partner had access to nitrogen, and followed the gene expression of several plant transporters of the Sucrose Uptake Transporter (SUT) and Sugars Will Eventually be Exported Transporter (SWEET) family. Tripartite interactions led to synergistic growth responses and stimulated the phosphate and nitrogen uptake of the plant. Plant nutrient demand but also fungal access to nutrients played an important role for the carbon transport to different root symbionts, and the plant allocated more carbon to rhizobia under nitrogen demand, but more carbon to the fungal partner when nitrogen was available. These changes in carbon allocation were consistent with changes in the SUT and SWEET expression. Our study provides important insights into how the host plant controls its carbon allocation under different nutrient supply conditions and changes its carbon allocation to different root symbionts to maximize its symbiotic benefits. Legumes are simultaneously colonized with arbuscular mycorrhizal fungi and rhizobia bacteria, and both root symbionts play a key role for the nutrient uptake of this agronomically important group of plants. The host plant allocates a significant amount of its photosynthates to both root symbionts, and this carbohydrate supply acts as an important trigger for symbiont function. We studied the nutrient uptake and carbon allocation in tripartite interactions and examined the gene expression of several plant transporters of the Sucrose Uptake Transporter (SUT) and Sugars Will Eventually be Exported Transporter (SWEET) family and found that plant nutrient demand but also fungal access to nutrients play an important role for the carbon transport to both root symbionts. The expression of several SUT and SWEET transporters was consistent with the observed changes in carbon allocation, and our study provides novel insights into the regulatory mechanisms that control the carbon transport to both root symbionts.