Nutrient exchange in arbuscular mycorrhizal symbiosis from a thermodynamic point of view

Abstract

Summary To obtain insights into the dynamics of nutrient exchange in arbuscular mycorrhizal ( AM ) symbiosis, we modelled mathematically the two‐membrane system at the plant–fungus interface and simulated its dynamics. In computational cell biology experiments, the full range of nutrient transport pathways was tested for their ability to exchange phosphorus (P)/carbon (C)/nitrogen (N) sources. As a result, we obtained a thermodynamically justified, independent and comprehensive model of the dynamics of the nutrient exchange at the plant–fungus contact zone. The predicted optimal transporter network coincides with the transporter set independently confirmed in wet‐laboratory experiments previously, indicating that all essential transporter types have been discovered. The thermodynamic analyses suggest that phosphate is released from the fungus via proton‐coupled phosphate transporters rather than anion channels. Optimal transport pathways, such as cation channels or proton‐coupled symporters, shuttle nutrients together with a positive charge across the membranes. Only in exceptional cases does electroneutral transport via diffusion facilitators appear to be plausible. The thermodynamic models presented here can be generalized and adapted to other forms of mycorrhiza and open the door for future studies combining wet‐laboratory experiments with computational simulations to obtain a deeper understanding of the investigated phenomena.

Identification of Long Non-Coding RNAs and the Regulatory Network Responsive to Arbuscular Mycorrhizal Fungi Colonization in Maize Roots

“…The recognition and the maintenance of the symbiosis between plants and AM fungi is complex [13,55]. The signal molecules which mediate the recognition between plants and AM fungi have been identified [15,56].…”

Nutrient cycling is an important mechanism for homeostasis in plant cells

“…Instead they communicate with each other via the cytosolic concentrations (Vincent et al, 2017; Horaruang et al, 2020). Previous studies have shown that membrane sandwiches exhibit another level of dynamics (Gajdanowicz et al, 2011; Schott et al, 2016; Dreyer et al, 2017; Dreyer et al, 2019). Therefore, nutrient homeostasis was also investigated with respect to these dynamics.…”

“…Nevertheless, transporter types can be mathematically described, allowing deep insights into the dynamics of transporter networks by computational analyses (Dreyer and Michard, 2020). Computational modelling helped already to better understand guard cell movement (Hills et al, 2012; Blatt et al, 2014), the role of K + gradients in energizing phloem (re-)loading processes (Gajdanowicz et al, 2011; Dreyer et al, 2017), the nutrient exchange in mycorrhizal symbioses (Schott et al, 2016; Dreyer et al, 2019; Nizam et al, 2019), the mechanism and potential consequences of vacuolar excitability (Jaslan et al, 2019; Dindas et al, 2021) and touch-sensitive signaling in trigger hairs of the Venus flytrap (Iosip et al, 2020).…”

Overcoming the Challenges to Enhancing Experimental Plant Biology With Computational Modeling

“…Pattern models are rarely applied at this scale of plant biology, often asking questions about spatiotemporal gene expression or regulation patterns (Geng et al, 2013), or developmental patterning (Di Mambro et al, 2017). Models of cellular processes include circadian clock and signaling (Grima et al, 2018), the cell cycle (Roodbarkelari et al, 2010), gene expression (Greenwood et al, 2019), development and cell fate (van Berkel et al, 2013), membrane batteries (Dreyer et al, 2019), photosynthesis (Brian and Hahn, 1987), and carbon flux through metabolic pathways (Allen et al, 2009;Orth et al, 2010).…”