Can optimality models and an ‘optimality research program’ help us understand some plant–fungal relationships?

Abstract

metabolites, clearly indicating the importance of metabolomics type studies to point the way toward a mechanistic explanation of grassendophyte-herbivore interactions.Grass species are often hosts of symbiotic clavicipitaceous endophytic fungi 1 residing in the apoplastic spaces of above ground plant parts and usually not causing any visible symptoms of infection. [2][3][4] These fungal symbionts confer protection from insect herbivory to their host plants through alkaloids, 5-8 some of which (ergovaline, lolitrem B) are also toxic to grazing mammals. 9,10 Natural endophyte strains lacking these mammalian toxins, but still retaining at least some of their insect deterring features, have been commercialized and are now widely used in ryegrass and tall fescue based pastures. 11,12 Insights into Molecular Grass-Endophyte InteractionsIn a previous study 13,14 we infected two ryegrass cultivars differing in their water soluble carbohydrate (WSC) content with three N. lolii strains (common strain CS-produces peramine, lolitrem B and ergovaline; AR1-produces peramine only; AR37-produces janthitrems only), and grew them at two nitrogen (N) levels. We quantified endophyte concentrations and 66 metabolic variables in the symbiotic tissue. Major findings were: Both, high N supply and high WSC content reduced fungal endophyte and alkaloid concentrations by approx. half, resulting in a 75% reduction in the high sugar cultivar at high N. A principal component analysis with subsequent factor rotation of the metabolic variables showed that (i) at high N proteins, major amino acids, organic acids and lipids were increased; WSCs, chlorogenic acid and fibers were decreased; (ii) the high sugar cultivar AberDove had reduced levels of nitrate, most minor amino acids, sulfur and fibers, whereas WSCs, CGA, and methionine were increased; (iii) plants infected with endophytes had increased levels of WSCs, some organic acids, lipids and CGA, whereas nitrate and several amino acids, esp., L-asparagine, were decreased.Several of these metabolites have been linked to plant quality for various herbivores. [15][16][17][18][19][20] We were interested in whether such changes in plant quality could be linked directly to herbivore performance (rather than indirectly via a treatment effect). Insect Herbivore Performance and Plant Metabolic QualityAfter harvesting the blades, plants were enclosed in plastic boxes and two alate adults of Rhopalosiphum padi L. were added to each plant. In addition to these aphids, two other aphid species, Sitobion nr frageriae and Aploneura lentisci, a variety of thrip (Frankliniella Pasture grasses are often infected with symbiotic fungal endophytes and benefits for host plants arising out of these associations are generally ascribed to endophyte produced anti-herbivorous alkaloids. We tested the effects of (i) infection with three strains of endophytes differing in their alkaloid profiles, (ii) high vs. low nitrogen (N) supply, and (iii) ryegrass cultivars with high vs. control levels of water soluble carbohydrates...

Metabolite analysis of the effects of elevated CO2 and nitrogen fertilization on the association between tall fescue (Schedonorus arundinaceus) and its fungal symbiont Neotyphodium coenophialum

“…It is unknown whether host plants can exert control over the degree of endophyte growth (Ryan et al . ).…”

“…Although these mechanisms have yet to be elucidated, nutrient exchange between plant and fungal partners seems to play an important role (Kiers & Denison ; Ryan et al . ; Draper, Rasmussen & Zubair ). Thus, changes in environmental variables that can alter plant resource allocation may have implications for the way in which symbiotic partners interact.…”

Metabolomics of forage plants: a review

“…In all cases the heterotrophic microorganisms depend on carbon and energy provided by their autotrophic host plants. How a mutualistic co-operation (both partners benefit) between the symbiotic partners is maintained over the course of evolution and especially how the partners prevent each other from 'cheating' (only one partner benefits) is still debated, but control of metabolite/nutrient exchange between the partners seems to play an important role (Kiers and Denison, 2008;Ryan et al, 2008;Draper et al, 2011).…”

Occam’s Razor Cuts Both Ways: Endophytes, Resource Allocation, Herbivory, and Mutualism: A Reply to Rudgers et al.

“…I agree with them on one key point: life span demographic experiments are essential to test how vertically transmitted endophytes alter life-history traits and the consequences for lifetime host fitness. I also agree that it is necessary to clearly define what lifetime fitness means for each organism and the appropriate ways for measuring it (e.g., Ryan et al 2008). For experimental studies, it is also essential to control and manipulate plant and endophyte genotype and environmental variation, including herbivory.…”

“…Rudgers et al's (2010) third main criticism is that my study provided no data on endophyte fitness. Measuring how shifts in resource allocation affect symbiont lifetime fitness is perhaps even more difficult than determining effects on host fitness (e.g., Ryan et al 2008). One necessary component of the endophytes-as-reproductive-parasites hypothesis is that early host reproduction benefits endophytes because infections can be lost in later host ontogeny.…”