Metabolic Profiles ofLolium perenneAre Differentially Affected by Nitrogen Supply, Carbohydrate Content, and Fungal Endophyte Infection    

Abstract

Lolium perenne cultivars differing in their capacity to accumulate water soluble carbohydrates (WSCs) were infected with three strains of fungal Neotyphodium lolii endophytes or left uninfected. The endophyte strains differed in their alkaloid profiles. Plants were grown at two different levels of nitrogen (N) supply in a controlled environment. Metabolic profiles of blades were analyzed using a variety of analytical methods. A total of 66 response variables were subjected to a principle components analysis and factor rotation. The first three rotated factors (46% of the total variance) were subsequently analyzed by analysis of variance. At high N supply nitrogenous compounds, organic acids and lipids were increased; WSCs, chlorogenic acid (CGA), and fibers were decreased. The high-sugar cultivar 'AberDove' had reduced levels of nitrate, most minor amino acids, sulfur, and fibers compared to the control cultivar 'Fennema', whereas WSCs, CGA, and methionine were increased. In plants infected with endophytes, nitrate, several amino acids, and, magnesium were decreased; WSCs, lipids, some organic acids, and CGA were increased. Regrowth of blades was stimulated at high N, and there was a significant endophyte 3 cultivar interaction on regrowth. Mannitol, a fungal specific sugar alcohol, was significantly correlated with fungal biomass. Our findings suggest that effects of endophytes on metabolic profiles of L. perenne can be considerable, depending on host plant characteristics and nutrient supply, and we propose that a shift in carbon/N ratios and in secondary metabolite production as seen in our study is likely to have impacts on herbivore responses.

Fungal grass endophytes and arthropod communities: lessons from plant defence theory and multitrophic interactions

“…Once again, the presumed primary mechanism for these community-wide effects is endophytic alkaloids that may modulate abundances and diversity of consumers (herbivores and detritivores), competitors (other conspecific or heterospecific plants) and consumers of plant consumers (predators and parasites). However, endophytic infections also cause other phenotypic changes in the host grasses in terms of growth and reproductive allocation (Faeth 2009), physiology (e.g., Morse et al 2002), water, nutrient and metabolite content (e.g., Rasmussen et al 2008), and oxidative stress protection (e.g., White & Torres 2010), all of which may also affect associated animal and plant communities. Furthermore, alkaloids are rarely measured in studies of the effect of endophyte infection at the community level (but see Jani et al 2010).…”

Advanced Data-Mining Strategies for the Analysis of Direct-Infusion Ion Trap Mass Spectrometry Data from the Association of Perennial Ryegrass with Its Endophytic Fungus,Neotyphodium lolii

“…Fang and Bendiak, 2007) suggest more extensive MS n analysis may provide additional structural information. As was shown previously (Rasmussen et al, 2007(Rasmussen et al, , 2008, endophyte infection resulted in higher levels of some of the sugars, which might indicate that the increased sink strength in the infected tissue results in a higher turnover of high DP fructans with a concomitant increase in low DP oligosaccharides. Although the exact mechanism for this pattern of accumulation remains to be elucidated, it has been documented (for review, see Chalmers et al, 2005) that the base of youngest leaves and the sheath of the more mature leaves represent the organs where fructosyltransferase activities, fructan accumulation, and remobilization in perennial ryegrass is most active, and where several fructan metabolism genes are expressed.…”

“…As discussed in detail above, the hexitol (m/z 205) present in endophyte-infected plants only is probably mannitol. Mannitol appears to be a very common polyol in fungi (Lewis and Smith, 1967) and has been reported to accumulate in endophyte-infected tall fescue (Richardson et al, 1992) and perennial ryegrass plants (Harwood, 1954;Johnson et al, 2006;Rasmussen et al, 2008). Although mannitol has been implicated as an osmoprotectant in the resurrection plant Myrothamnus flabellifolia (Bianchi et al, 1993) and in transgenic Arabidopsis (Arabidopsis thaliana) expressing a celery (Apium graveolens) Man-6-P reductase (Sickler et al, 2007) as well as in Nicotiana tabacum expressing a mannitol-1-P dehydrogenase (Karakas et al, 1997), a study in tall fescue indicates that mannitol levels in endophyteinfected plants are not increased under drought stress (Richardson et al, 1992).…”

“…Considerable research efforts have been focused on the biosynthesis, accumulation, and ecological consequences of these fungal alkaloids (for review, see Schardl, 2001;Clay and Schardl, 2002;Schardl et al, 2004). Much less is known about the impacts of fungal endophytes on general host plant performance and metabolism, and recent publications indicate that the effects of fungal endophytes on plant metabolism might be of importance to the understanding of ecosystem-wide impacts of the grassendophyte symbiosis (Hunt et al, 2005;Cheplick, 2007;Krauss et al, 2007;Rasmussen et al, 2007Rasmussen et al, , 2008.…”

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

“…In 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.…”