Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis

Abstract

Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be "enslaved." Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.

The expression of GintPT, the phosphate transporter of Rhizophagus irregularis, depends on the symbiotic status and phosphate availability

“…5). Since it has been proposed that the exchange of Pi versus carbon compounds in AM symbiosis is interconnected (Kiers et al 2011), we also investigated the expression profile of GintMST2, the R. irregularis hexose transporter recently characterized by Helber et al (2011) in arbusculated cells. The gene is in fact possibly involved in the uptake of hexoses released by the plant in the periarbuscular space.…”

“…The detection of GintPT transcripts in spores could be related to the growth conditions created by ROCs: A. rhizogenes-transformed roots are grown in a C-rich medium, which becomes depleted during the 2-month period of mycorrhizal colonization. Under these conditions, we can speculate that the nutrient exchange model, according to which the symbionts can reciprocally stimulate a C or P flux by providing nutrients to the other partner (Kiers et al 2011), becomes altered. The host is not able to reward the fungus in the best way by providing C, and on the other hand, R. irregularis, which is considered a cooperative fungal species (Kiers et al 2011), stores Pi resources in the spores.…”

“…In spite of the huge amount of data that deal with the transfer of the fungal Pi towards the plant, a molecular analysis which examines the expression dynamics of the fungal PT along the diverse stages of the symbiosis and in the context of the nutritional exchanges with the plant is not available. To reach this goal, we used root organ cultures (ROCs) and bicompartimented Petri dishes (Hammer et al 2011;Kiers et al 2011), since this system allows both plant and fungal compartments to be manipulated. We therefore examined the expression profile of the highaffinity PT gene (GintPT) of the AM fungus R. irregularis in the fungal structures (spores, ERM and arbuscules) and under different Pi availability as well as the impact of the plant connection on GintPT expression.…”

“…We therefore examined the expression profile of the highaffinity PT gene (GintPT) of the AM fungus R. irregularis in the fungal structures (spores, ERM and arbuscules) and under different Pi availability as well as the impact of the plant connection on GintPT expression. As a further step, since the exchange of nutrients is considered the driving force for the evolutionary stability of AM symbiosis (Parniske 2008;Humphreys et al 2010;Kiers et al 2011), we wondered whether the dynamics of the fungal GintPT expression could be related to that of other plant and fungal genes involved in nutrients exchanges. We therefore investigated the MtPT4 gene, encoding a phosphate transporter of Medicago truncatula, which is expressed in arbuscule-containing cells and is responsible for the uptake of Pi released by the fungus in the periarbuscular space (Harrison et al 2002;Javot et al 2007).…”

Gr and hp-1 tomato mutants unveil unprecedented interactions between arbuscular mycorrhizal symbiosis and fruit ripening

“…Both partners gain an advantage from the symbiosis; the fungus supplies the plant with mineral nutrients (mainly phosphate) increasing, plant biomass and improving its resistance to pathogens and environmental stresses including oxidative stress conditions (Garcia-Sànchez et al 2014), while the host provides organic carbon to the fungus (Bonfante and Genre 2010). Plant and fungal nutrition is thus mutually improved (Kiers et al 2011). Experimental evidence reveals that AMF both improve plant health and growth as natural biofertilisers and enhance organoleptic and nutritional traits of edible crops (Salvioli and Bonfante 2013).…”