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

Authors: KAFLE, ARJUN - South Dakota State University; GARCIA, KEVIN - South Dakota State University; WANG, XIURONG - South Dakota State University; Pfeffer, Philip; Strahan, Gary; BUCKING, HEIKE - South Dakota State University

Submitted to: Plant Cell and Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/28/2018
Publication Date: 6/2/2018
Citation: Kafle, A., Garcia, K., Wang, X., Pfeffer, P., Strahan, G.D., Bucking, H. 2018. Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula. Plant Cell and Environment. 42:270-284. https://doi.org/10.1111/pce.13359.
DOI: https://doi.org/10.1111/pce.13359

Interpretive Summary: Approximately 88% of legumes are able to form tripartite interactions, and can be simultaneously colonized with N-fixing bacteria and AM fungi. These associations can potentially contribute to the nutrient efficiency of this important group of crops. The capability of legumes to form tripartite interactions has the potential to increase the fitness of both the host and the different symbiont species. However, nutrient dynamics in tripartite interactions are currently only poorly understood. We seek to enhance our understanding of the ecological, physiological and molecular factors that determine the benefits (or lack thereof) of simultaneous colonization by different species of competing N-fixing bacteria and fungal symbionts. In collaboration with Dr. Heike Bucking and graduate students at South Dakota State University and Dr. Xiurong Wang of South China Agricultural University, we studied the pathways of nitrogen uptake of the tripartite legume plant Medicago truncatela. Separated roots of these plants were each colonized with nitrogen fixing Rhizobium irregularis or mycorrhizal fungi Glomus aggregatum, respectively. 15N labeled NH4CL was used as the transported nutrient from the colonizing mycorrhiza, whereas natural abundance 14N N2, derived from from air was used as the Rhizobium source of fixed 14NH4+ transported to the plant roots. By determining the 15N enrichment levels of the plant root and shoot tissues we were able to evaluate movement of nitrogen to the host through these respective pathways under a variety of conditions which include limited carbon and phosphorus availability. Our results provide important insight into how the host plant controls its carbon allocation to different root symbionts and is able to maximize its symbiotic benefits in a tripartite system. This information will be key in the development of strategies and future attempts to simultaneously maximize both root symbionts for increased yield of legumes under low or reduced fertilizer input conditions.

Technical Abstract: Legumes form tripartite interactions with arbuscular mycorrhizal (AM) fungi and rhizobia bacteria, and both root symbionts exchange nutrients for carbohydrates 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 to different root symbionts in Medicago truncatula under different nutrient supply conditions, and when the fungal partner had access to nitrogen, and followed the gene expression of three sucrose transporters from the SUT family, MtSUT1-1, MtSUT2, and MtSUT4-1. Tripartite interactions led to synergistic growth responses and stimulated the phosphate and nitrogen uptake of the plant. Nutrient demand played an important role for carbon allocation. The plant allocated more carbon to rhizobia under low nitrogen conditions, but proportionally more carbon to the fungal symbiont under high nitrogen conditions. These changes in carbon allocation were consistent with SUT transporter expression, and MtSUT2 and MtSUT4-1 expression was correlated to the carbon transport to different root symbionts. Our study provides important insights into how the host plant controls its carbon allocation to different root symbionts, and is able to maximize its symbiotic benefits in tripartite interactions.