Kari Saikkonen

Defensive mutualism between plants and endophytic fungi

Endophyte-grass symbiosis is generally considered to be a classic example of microbe-plant symbiosis in which the fitness of the microbial symbiont and its host plant is closely linked, and thus, presumed to align the interests of partners toward mutually beneficial cooperation. Accumulating evidence seems to suggest that defensive mutualism provides the best framework for understanding plant-endophyte interactions in general. We conducted a meta-analysis of 99 published studies on 36 plant (inc. both grass and tree species), 62 herbivore and 17 predator or parasitoid taxons to test the importance of defensive mutualism in multitrophic interactions. In general, statistical perusal revealed that we still know little about these seemingly well-studied biological interactions. The conceptual framework for endophyte-grass interactions has largely been based on endophyte-plant-herbivore studies of two, economically important, artificially selected and introduced agricultural grass species, tall fescue and perennial ryegrass, and two generalist invertebrate pests. Only 10 original publications provided data of higher trophic levels. Consistent with the defensive mutualism hypothesis, the meta-analysis indicates that endophytes slightly increase grass resistance to herbivores, and the defensive mutualism appears to be most commonly detected in systemic and vertically transmitted grass endophytes compared to horizontally transmitted tree endophytes. However, variation appears to increase when higher trophic levels are considered. In addition to taxonomical bias, the literature is strongly biased toward short-term laboratory and greenhouse experiments rather than field conditions. Thus, current literature is insufficient to capture the breadth of variability inherent in the wild grass-endophyte populations and communities, and the general importance of defensive mutualism remains to be solved in future studies.

Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review

Reactive oxygen species are in all types of organisms from microbes to higher plants and animals. They are by-products of normal metabolism, such as photosynthesis and respiration, and are responsive to abiotic and biotic stress. Accumulating evidence suggests reactive oxygen species play a vital role in programmed cell death, stress responses, plant defense against pathogens and systemic stress signaling in conjunction with antioxidant production. Here, we propose that reactive oxygen species and antioxidants, as both universal and evolutionarily conserved, are likely to play important role(s) in symbiotic interactions. To support this hypothesis we review the root and foliar fungal endophyte literature specific to fungal-plant symbiotum production of reactive oxygen species and antioxidants in response to stress. These asymptomatic fungi can produce antioxidants in response to both biotic and abiotic stress when grown in culture as well as in planta. In addition, there is a growing but nascent literature reporting a significant impact of endophyte colonization on the antioxidant activity of colonized (E+) hosts when compared to uncolonized (E-) hosts, especially when exposed to stress. Here we summarize general patterns emerging from the growing literature specific to antioxidant activity of endophytes in colonized hosts and bring up possible future research questions and approaches. The consequences of changes in reactive oxygen species production and increased antioxidant activity in the symbiotum appear to be beneficial in many instances; but costs are also indicated. Unexplored questions are: 1) to what extent do antioxidants originating from the fungal endophyte mediate host metabolism, and thereby control host responses to endophyte colonization; (2) what role do fungal, plant, or symbiotum produced reactive oxygen species and antioxidants have in determining symbiotic outcome between extremes of pathogenicity and mutualism; and (3) what role if any, do the production of reactive oxygen species and their antioxidant counterparts play in the symbiotum’s ability to respond to changing selection pressures? If as the literature suggests, such endophyte imposed mediation can be utilized to foster increases in plant production in resource limited habitats then the utilization of fungal endophytes may prove useful in agronomic and conservation settings.

Chemical Ecology Mediated by Fungal Endophytes in Grasses

Defensive mutualism is widely accepted as providing the best framework for understanding how seed-transmitted, alkaloid producing fungal endophytes of grasses are maintained in many host populations. Here, we first briefly review current knowledge of bioactive alkaloids produced by systemic grass-endophytes. New findings suggest that chemotypic diversity of the endophyte-grass symbiotum is far more complex, involving multifaceted signaling and chemical cross-talk between endophyte and host cells (e.g., reactive oxygen species and antioxidants) or between plants, herbivores, and their natural enemies (e.g., volatile organic compounds, and salicylic acid and jasmonic acid pathways). Accumulating evidence also suggests that the tight relationship between the systemic endophyte and the host grass can lead to the loss of grass traits when the lost functions, such as plant defense to herbivores, are compensated for by an interactive endophytic fungal partner. Furthermore, chemotypic diversity of a symbiotum appears to depend on the endophyte and the host plant life histories, as well as on fungal and plant genotypes, abiotic and biotic environmental conditions, and their interactions. Thus, joint approaches of (bio)chemists, molecular biologists, plant physiologists, evolutionary biologists, and ecologists are urgently needed to fully understand the endophyte-grass symbiosis, its coevolutionary history, and ecological importance. We propose that endophyte-grass symbiosis provides an excellent model to study microbially mediated multirophic interactions from molecular mechanisms to ecology.

SEVERE DEFOLIATION OF SCOTS PINE REDUCES REPRODUCTIVE INVESTMENT BY ECTOMYCORRHIZAL SYMBIONTS

Reduction in the photosynthetic capacity of plants is presumed to negatively affect their fungal symbionts. To test this hypothesis under natural conditions, we artificially removed 100% of previous year needles in two successive years on Scots pine trees (Pinus sylvestris L.) to simulate pine sawfly attack. Despite a decline in the shoot growth of defoliated trees, root biomass did not differ from control trees. The ergosterol (fungal biomass) and starch concentration of fine roots, however, slightly declined in defoliated trees. Percent ectomycorrhizal colonization of fine root tips remained high in both defoliated and control trees. The dominant tubercle morphotypes were slightly more abundant in the control than in defoliated trees. In contrast to the relatively weak effects on vegetative ectomycorrhizae, reproduction declined near the defoliated pines. Average sporocarp numbers and, consequently, the relative fungal investment to reproduction of the estimated total fungal biomass were more than three times higher near controls than defoliated trees in the first treatment year. Defoliation also reduced the diversity of ectomycorrhizal species producing sporocarps. Mutualistic fungal symbionts may thus alter their reproductive investment in response to restrictions on host resources. Because fungal biomass in the roots as well as colonization percentage remained unchanged, Scots pine evidently continues to invest in the maintenance of the symbiosis despite the reduced photosynthetic capacity due to defoliation.

Are endophyte-mediated effects on herbivores conditional on soil nutrients?

Neotyphodium endophytes are assumed to have mutualistic relationship with their grass hosts, mainly resulting from mycotoxin production increasing plant resistance to herbivores by the fungus that subsists on the plant. To study importance of often ignored environmental effects on these associations, we performed a greenhouse experiment to examine the significance of endophyte infection and nutrient availability for bird-cherry aphid (Rhopalosiphum padi) performance on meadow fescue (Lolium pratense). Naturally endophyte-infected (E+), uninfected (E–), or manipulatively endophyte-free (ME–) half-sib families of meadow fescue were grown on two soil nutrient levels. Endophyte infection reduced aphid performance in general. However, to our knowledge, this is the first study to demonstrate experimentally that herbivore performance decreases on E+ host plants with increasing availability of nutrients in soils. Potential improvement in herbivore performance in high nutrient soils and decreased plant performance in low nutrient soils in ME– plants, compared to E– and E+ plants, suggests that loss of endophyte infection after long coevolutionary relationship may be critical to plant fitness.

Glyphosate in northern ecosystems

Glyphosate is the main nonselective, systemic herbicide used against a wide range of weeds. Its worldwide use has expanded because of extensive use of certain agricultural practices such as no-till cropping, and widespread application of glyphosate-resistant genetically modified crops. Glyphosate has a reputation of being nontoxic to animals and rapidly inactivated in soils. However, recent evidence has cast doubts on its safety. Glyphosate may be retained and transported in soils, and there may be cascading effects on nontarget organisms. These processes may be especially detrimental in northern ecosystems because they are characterized by long biologically inactive winters and short growing seasons. In this opinion article, we discuss the potential ecological, environmental and agricultural risks of intensive glyphosate use in boreal regions.

Components of male fitness in relation to body size in Epirrita autumnata (Lepidoptera, Geometridae)

Abstract. 1. The effect of body size on different components of male fitness was studied for Epirrita autumnata, a geometrid known for its eruptive population dynamics. Body size is the main determinant of female fecundity in this species.

ENVIRONMENTAL CONDITIONS AND HOST GENOTYPE DIRECT GENETIC DIVERSITY OF VENTURIA DITRICHA, A FUNGAL ENDOPHYTE OF BIRCH TREES

Abstract We investigated whether genetic variation of a common foliar endophyte of birch trees, Venturia ditricha, is affected by environmental conditions or host genotype. Fungal samples were collected from 10 half‐sibling families of mountain birch (Betula pubescens ssp. czerepanovii) grown in two environmental conditions with different daily average temperatures: a forested river valley and an adjacent open tundra (altitudinal difference 180 m). Genetic analysis of V. ditricha isolates was done using random amplified microsatellite polymerase chain reaction. We found that host genotypes, along with prevailing environmental conditions, influence the probability of infection by particular endophyte genotypes. The most susceptible host genotypes were highly infected with genetically similar endophyte genotypes, whereas the most resistant trees were poorly infected and they were infected by genetically dissimilar endophytes. Our results also showed environment–host genotype interactions, suggesting that the susceptibility of the host to a particular endophyte genotype may change in natural environments when environmental conditions are changed. It appears that a particular endophyte genotype needs to find the right host genotype for a successful infection. There are many host genotypes in natural stands; this means, from the point of view of the fungus, the environment is heterogeneous. Thus, under the influence of birch tree genotypes, genetically differentiated subgroups of the en‐dophytic fungus may be formed in different environments.

Genetic Compatibility Determines Endophyte-Grass Combinations

Even highly mutually beneficial microbial-plant interactions, such as mycorrhizal- and rhizobial-plant exchanges, involve selfishness, cheating and power-struggles between the partners, which depending on prevailing selective pressures, lead to a continuum of interactions from antagonistic to mutualistic. Using manipulated grass-endophyte combinations in a five year common garden experiment, we show that grass genotypes and genetic mismatches constrain genetic combinations between the vertically (via host seeds) transmitted endophytes and the out-crossing host, thereby reducing infections in established grass populations. Infections were lost in both grass tillers and seedlings in F1 and F2 generations, respectively. Experimental plants were collected as seeds from two different environments, i.e., meadows and nearby riverbanks. Endophyte-related benefits to the host included an increased number of inflorescences, but only in meadow plants and not until the last growing season of the experiment. Our results illustrate the importance of genetic host specificity and trans-generational maternal effects on the genetic structure of a host population, which act as destabilizing forces in endophyte-grass symbioses. We propose that (1) genetic mismatches may act as a buffering mechanism against highly competitive endophyte-grass genotype combinations threatening the biodiversity of grassland communities and (2) these mismatches should be acknowledged, particularly in breeding programmes aimed at harnessing systemic and heritable endophytes to improve the agriculturally valuable characteristics of cultivars.

Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar micro-fungi?

Previous studies on the mechanisms of birch resistance to herbivores and foliar micro-fungi (both pathogenic and endophytic) have focused mainly on the role of internal leaf chemistry. In the present study, we examined genetic correlations between leaf surface traits (glandular trichome density and total concentrations of surface flavonoid aglycones) and occurrence of three species of foliar micro-fungi, one pathogenic rust (Melampsoridium betulinum) and two endophytic fungi (Fusicladium sp. and Melanconium sp.), and performance of autumnal moth larvae (Epirrita autumnata) in two birch species, Betula pubescens ssp. czerepanovii and B. pendula. The performance of autumnal moth larvae on B. pubescens ssp. czerepanovii was negatively correlated with density of glandular trichomes (RGR: r=−0.855; pupal mass: r=−0.709). In addition, rust infection was negatively correlated with trichome density in B. pendula (r=−0.675) and with epicuticular flavonoid aglycones in B. pubescens ssp. czerepanovii (r=−0.855). The frequency of the endophytic fungus Fusicladium sp., was related to epicuticular flavonoid aglycones (r=−0.782), while another endophytic fungus, Melanconium sp., showed no associations with any of the studied variables in B. pubescens ssp. czerepanovii. Our results indicate that leaf surface traits may be at least as important determinants of herbivore performance and micro-fungi abundance in birch as leaf internal chemistry.