Can seed-borne endophytes promote grass invasion by reducing host dependence on mycorrhizas?

Symbiotic interactions between plants and microorganisms have recently become the focus of research on biological invasions. However, the interaction between different symbionts and their consequences in host-plant invasion have been seldom explored. Here, we propose that vertically transmitted fungal endophytes could reduce the dependency of invasive grasses on mycorrhizal fungi allowing host establishment in those environments where the specific mutualist may be not present. Through analyzing published studies on nine grass species, we evaluated the effect of seed-borne Epichloë endophytes on the relationship of invasive and non-invasive grasses with arbuscular mycorrhizal fungi (AMF), a symbiosis known to be fundamental for plant fitness and invasion success. The endophyte effect on AMF colonization differed between invasive and non-invasive grasses, reducing mycorrhization only on invasive species but with no impact on their biomass. These results allowed us to propose that Epichloë endophytes could reduce the dependency of host plants on the mutualism with AMF, promoting host grass establishment and subsequent invasion. Simultaneous interactions with different types of mutualists may have profound effects on the host-plant fitness facilitating its range expansion. Our findings suggest that some specific mutualistic fungi such as epichloid endophytes facilitate host invasion by reducing the requirements of the benefits derived from other mutualisms.     

Mutualistic asexual endophytes in a native grass are usually parasitic

Asexual systemic fungi that live symbiotically within grasses are viewed as strong mutualists on the basis of theory and empirical studies of introduced agronomic grasses. Evolutionary theory predicts that microbial symbionts that lose sexuality and rely on propagules of their hosts for transmission should evolve to benefit their hosts. Fungal endophytes of some cultivated turf and pasture grasses are well known for increasing plant performance and competitive abilities, especially under stress, and increasing resistance to herbivores, pathogens, and root-feeders by virtue of fungal alkaloids. The assumption of mutualism, however, has rarely been tested in native grasses, which often harbor high but variable frequencies of systemic asexual endophytes. We tested the effect of Neotyphodium infections for the native grass Arizona fescue in a 3-yr field experiment. We strictly controlled host genotype and manipulated soil moisture and nutrients. Infection generally decreased host growth in terms of plant volume, number of tillers, and dry mass of shoots and roots. Infected plants also showed decreased reproduction in terms of number and mass of seeds, and the seeds produced by infected plants had lower germination success than plants without their endophytes, suggesting that the negative effects of the symbiont are transferred to the next generation. Plant genotype strongly influenced host's growth and reproduction and interacted with the presence of the endophyte, but the interaction was usually in the direction of negative effects. Our results challenge the notion that systemic asexual endophytes must be plant mutualists for infections to persist in nature. We propose other hypotheses to explain the variable but usually high endophyte frequencies in natural populations of grasses.     

Epichloë fungal endophytes and the formation of synthetic symbioses in Hordeeae (=Triticeae) grasses

This review examines two classes of organism that live in symbiosis; grasses, and fungi. Specifically it deals with grasses of the tribe Hordeeae (formerly Triticeae) of the subfamily Poöideae and the Epichloë fungi of family Clavicipitaceae. Epichloë endophytes, particularly asexual forms, have important roles in pastoral agricultural systems in the Americas, Australia, and New Zealand. Selected strains add value to some grass-based forage systems by providing both biotic and abiotic stress resistance. The importance of cereal grasses such as wheat, barley, rye, and oats to human and animal nutrition and indeed to the foundation and maintenance of human civilization is well documented. Both organism classes, Epichloë endophytes and cereal grasses, are of great importance in their own contexts. Here, we seek to review these two classes of organism and examine the possibility of bringing them together in symbiosis with the ultimate goal of improving cereal production systems.     

Endophytic fungus-vascular plant-insect interactions

Insect association with fungi has a long history. Theories dealing with the evolution of insect herbivory indicate that insects used microbes including fungi as their principal food materials before flowering plants evolved. Subtlety and the level of intricacy in the interactions between insects and fungi indicate symbiosis as the predominant ecological pattern. The nature of the symbiotic interaction that occurs between two organisms (the insect and the fungus), may be either mutualistic or parasitic, or between these two extremes. However, the triangular relationship involving three organisms, viz., an insect, a fungus, and a vascular plant is a relationship that is more complicated than what can be described as either mutualism or parasitism, and may represent facets of both. Recent research has revealed such a complex relationship in the vertically transmitted type-I endophytes living within agriculturally important grasses and the pestiferous insects that attack them. The intricacy of the association depends on the endophytic fungus-grass association and the insect present. Secondary compounds produced in the endophytic fungus-grass association can provide grasses with resistance to herbivores resulting in mutualistic relationship between the fungus and the plant that has negative consequences for herbivorous insects. The horizontally transmitted nongrass type-II endophytes are far less well studied and as such their ecological roles are not fully understood. This forum article explores the intricacy of dependence in such complex triangular relationships drawing from well-established examples from the fungi that live as endophytes in vascular plants and how they impact on the biology and evolution of free-living as well as concealed (e.g., gall-inducing, gall-inhabiting) insects. Recent developments with the inoculation of strains of type-I fungal endophytes into grasses and their commercialization are discussed, along with the possible roles the endophytic fungi play in the galls induced by the Cecidomyiidae (Diptera).     

禾草内生真菌的遗传多样性及其共生关系

 近百年的禾草内生真菌研究历经了由浅入深的过程,从最初的家畜中毒事件认识到是一种共生内生真菌存在的缘故,到如今利用分子生物学技术揭示其共生机制,人类发现这类植物内生真菌并非想象中的对生态系统无足轻重。Epichloë及其无性型Neotyphodium与禾本科植物是系统发生的互利共生关系,尤其是Neotyphodium可提高宿主抵抗环境胁迫的能力和抵御动物的取食,增强植物的竞争力。禾草内生真菌有3种生活史：有性生活史、无性生活史和兼性生活史,后者表明真菌在不同的宿主及环境下既能营有性生殖也可营无性繁殖,是一种更灵活而有效的生活史对策。对内生真菌分子系统学、生活史以及与宿主禾草协同进化的研究发现,Neotyphodium起源于禾草致病真菌Epichloë的某些种,或是Epichloë与Neotyphodium的种间杂交后代。植物和内生真菌各异的生活史策略,真菌的种间杂交,两者的协同进化亦或种群间基因流的差异,都促成了共生体多样化的基因组合（Genetic combination ）,也是其共生关系多样化的根源。内生真菌对宿主的有益作用只在特定基因型真菌、宿主和一定环境条件下才起作用,自然生态系统的共生关系要比农业系统复杂得多,是一个从互利共生至寄生关系的连续系统。未来对于更多共生体的遗传背景和基因与环境相互作用的阐明将有助于对禾草内生真菌共生关系本质更加深入的认识。     

Evolutionary origins and ecological consequences of endophyte symbiosis with grasses

Over the past 20 yr much has been learned about a unique symbiotic interaction between fungal endophytes and grasses. The fungi (Clavicipitaceae, Ascomycota) grow intercellularly and systemically in aboveground plant parts. Vertically transmitted asexual endophytes forming asymptomatic infections of cool-season grasses have been repeatedly derived from sexual species that abort host inflorescences. The phylogenetic distribution of seed-transmitted endophytes is strongly suggestive of cocladogenesis with their hosts. Molecular evidence indicates that many seed-transmitted endophytes are interspecific hybrids. Superinfection may result in hyphal fusion and parasexual recombination. Most endophytes produce one or more alkaloid classes that likely play some role in defending the host plant against pests. Hybridization may have led to the proliferation of alkaloid-production genes among asexual endophytes, favoring hybrids. The ergot alkaloid ergovaline, lolitrems, and lolines are produced by only a single sexual species, Epichlo? festucae, but they are common in seed-transmitted endophytes, suggesting that E. festucae contributed genes for their synthesis. Asexual hybrids may also be favored by the counteracting of the accumulation of deleterious mutations (Muller's rachet). Endophyte infection can provide other benefits, such as enhanced drought tolerance, photosynthetic rate, and growth. Estimates of infection frequency have revealed variable levels of infection with especially high prevalence in the subfamily Pooideae. Longitudinal studies suggest that the prevalence of seed-transmitted endophytes can increase rapidly over time. In field experiments, infected tall fescue suppressed other grasses and forbs relative to uninfected fescue and supported lower consumer populations. Unlike other widespread plant/microbial symbioses based on the acquisition of mineral resources, grass/endophyte associations are based primarily on protection of the host from biotic and abiotic stresses.     

Forest habitat characteristics affect balance between sexual reproduction and clonal propagation of the ectomycorrhizal mushroom Hebeloma cylindrosporum

Endophytic fungi, especially asexual, systemic endophytes in grasses, are generally viewed as plant mutualists, mainly through the action of mycotoxins, such as alkaloids in infected grasses, which protect the host plant from herbivores. Most of the evidence for the defensive mutualism concept is derived from studies of agronomic grass cultivars, which may be atypical of many endophyte-host interactions. I argue that endophytes in native plants, even asexual, seed-borne ones, rarely act as defensive mutualists. In contrast to domesticated grasses where infection frequencies of highly toxic plants often approach 100%, natural grass populations are usually mosaics of uninfected and infected plants. The latter, however, usually vary enormously in alkaloid levels, from none to levels that may affect herbivores. This variation may result from diverse endophyte and host genotypic combinations that are maintained by changing selective pressures, such as competition, herbivory and abiotic factors. Other processes, such as spatial structuring of host populations and endophytes that act as reproductive parasites of their hosts, may maintain infection levels of seed-borne endophytes in natural populations, without the endophyte acting as a mutualist.     

Fungal Symbionts Alter Plant Drought Response

Grassland productivity is often primarily limited by water availability, and therefore, grasslands may be especially sensitive to climate change. Fungal symbionts can mediate plant drought response by enhancing drought tolerance and avoidance, but these effects have not been quantified across grass species. We performed a factorial meta-analysis of previously published studies to determine how arbuscular mycorrhizal (AM) fungi and endophytic fungal symbionts affect growth of grasses under drought. We then examined how the effect of fungal symbionts on plant growth was influenced by biotic (plant photosynthetic pathway) and abiotic (level of drought) factors. We also measured the phylogenetic signal of fungal symbionts on grass growth under control and drought conditions. Under drought conditions, grasses colonized by AM fungi grew larger than those without mycorrhizal symbionts. The increased growth of grasses conferred from fungal symbionts was greatest at the lowest soil moisture levels. Furthermore, under both drought and control conditions, C3 grasses colonized by AM fungi grew larger than C3 grasses without symbionts, but the biomass of C4 grasses was not affected by AM fungi. Endophytes did not increase plant biomass overall under any treatment. However, there was a phylogenetically conserved increase in plant biomass in grasses colonized by endophytes. Grasses and their fungal symbionts seem to interact within a context-dependent symbiosis, varying with biotic and abiotic conditions. Because plant–fungal symbioses significantly alter plant drought response, including these responses could improve our ability to predict grassland functioning under global change.     

内生真菌与禾本科植物之间的关系及其生态学意义

1　前　言内生真菌是一类生长在植物体内的真菌 ,至今已在许多高等植物中发现了内生真菌的存在 ,但以禾本科植物中尤为常见。这些真菌包括子囊菌纲、麦角菌科 (Ｃｌａｖｉｃｉｐｉｔａｃｅａｅ)、瘤座菌族 (Ｂａｌａｎ ｓｉｅａｅ)的许多种类 ,也包括与瘤座菌族关系密切的一些半知菌类 ,如Ａｃｒｅｍｏｎｉｕｍ[1 5] 。与菌根真菌的一个显著不同是 ,它们仅存在于植物地上部分的组织内而不是根的组织中。至少有 80个属、几百种禾本科植物被确认含内生真菌[1 6] ,但到目前为止 ,大量的研究都集中在两个有重要经济意义的植物种 ,即高羊茅 (Ｆｅ…     

Potential analysis of grass endophytes Neotyphodium as biocontrol agents

Many grasses in the subfamily Pooideae develop symbioses with Neotyphodium fungal endophytes, which exist widely in nature. The stably symbiotic relationship not only ensures accessible nutrients required by Neotyphodium fungal endophytes, but also significantly increases the resistance of host grasses to biological stresses through the production of secondary metabolites. Previous studies show that infected grasses with endophytic fungi have prominently enhanced resistance to pests, plant diseases, companion plants and other biological stresses. Grass endophytic fungi show remarkable resistant to at least 79 species of pests from three classes; arachnida, nematode and insecta, and to at least 22 species of pathogenic fungi. Although the biotechnological application of endophytic fungi in grass breeding for variety selection and quality improvement has progressed well, opportunities remain for further exploring the use of fungal endophytes among different host grasses coupled with the examination of genetic stability of Neotyphodium in novel host grasses. In the future application of endophytic fungi as a bio-control method, researchers should not only consider specificities of host grasses, but also need to have comprehensive analysis and knowledge about the mutual relationships among grasses, endophytic fungi and ecological environments, which will help use endophytic fungi to better serve humanity.     

Systematics, distribution, and host specificity of grass endophytes.

Clavicipitaceous endophytes (Ascomycetes) are distributed worldwide in many grasses and sedges forming a perennial and often mutualistic association with their hosts. Most endophytes appear to produce alkaloid toxins in infected plants. The high frequency of infection in many grasses and in certain grassland communities may indicate a selective advantage of infected over non-infected host plants due to their toxic effects on grazing animals and insects. Field observations and artificial inoculations of seedlings have demonstrated a high degree of specificity of most endophytes to their host plant, particularly in asexual, seed-borne endophytes. Specific isozyme genotypes found on several host species suggest that host-specific physiological races may occur. Knowledge of host range and host specificity is vital for potential applications of endophytes in pest control.     

禾草内生真菌作为生防因子的潜力分析

早熟禾亚科多种禾草可与Neotyphodium内生真菌形成禾草-内生真菌共生体, 这种植物-微生物共生体性状较为稳定, 且在自然界中广泛存在。禾草-内生真菌共生体稳定的互利共生关系不但保证了内生真菌所需的全部营养物质, 而且共生体产生的次生代谢物又可显著提高宿主禾草对生物胁迫的抗逆性。众多研究表明, 内生真菌的侵染可显著提高宿主禾草对虫害、病害及伴生植物等多种生物胁迫的抗性。据不完全统计, 禾草内生真菌对蛛形纲、线虫纲、昆虫纲3个纲至少79个种的害虫表现出较明显的抗性, 对至少22个种的病原真菌表现出明显的抗性。尽管利用内生真菌进行禾草品种选育及其品质改良的技术日趋成熟, 但是内生真菌在不同宿主禾草之间高效的替代转化技术, 及其在宿主体内遗传的稳定性仍有待于进一步深入探索。研究者把禾草内生真菌作为生防手段, 在未来的应用过程中不应只考虑其与宿主禾草之间的共生特异性, 而应更全面地分析禾草-内生真菌-生态环境之间的相互关系, 让内生真菌更好地为人类服务。     

Endophytes of native grasses from South America: Biodiversity and ecology

We review and present preliminary results of studies on cool-season grass endophytes native to South America. These fungi have been studied only in Argentina, where they have been detected in 36 native grass species. The hybrid Neotyphodium tembladerae is present in an extremely wide host range found in diverse environmental conditions, but some other endophytes seem to be strictly associated with one host species in a particular environment. In host species that inhabit different environments, the incidence of endophytes is highly variable among populations and in most of the cases is clearly associated with environmental conditions. In these native grasses, Neotyphodium presents a mutualistic behaviour, conferring enhanced growth, promoting the symbiosis with arbuscular mycorrhizal fungi, and inhibiting growth of pathogenic fungi. In native forage grasses, preliminary analyses indicate that some Argentinian endophytes can produce lolines but are unlikely to produce lolitrem B or ergot alkaloids.     

丛枝菌根真菌对植物繁殖的影响研究进展

丛枝菌根真菌(arbuscular mycorrhizal fungi, AMF)与宿主植物所形成的互惠共生体系是生态系统中广泛分布的共生体系代表类型之一。AMF除能够促进宿主植物生长发育外,也可以对宿主植物的繁殖过程产生多方面影响。研究宿主植物在AMF共生状态下繁殖策略的变化规律,对于深入理解植物繁殖适合度的变化具有重要理论意义。该文综述了AMF对宿主植物繁殖影响的相关研究,包括AMF的侵染对宿主植物繁殖分配、花部特征、虫媒传粉和花期的影响。目前已有研究发现某些AMF能够促进宿主植物增加繁殖资源投入,提高花朵产生的数量或花冠直径,同时增加花粉数量和花蜜量来影响访花昆虫的行为,以及造成开花提前及花期延长,但其作用的具体机制尚不明确,且因宿主植物的差异,并未有完全统一的结论。然而,由于AMF与植物共生的普遍性,其在植物繁殖过程中发挥的重要作用不可忽略。今后除了在以上各方面开展更深入的研究外,还需在AMF对宿主植物繁殖性状的影响机制、AMF共生条件下植物有性繁殖过程中雌雄功能的资源分配,以及对无性繁殖和后代适应性的影响等方面进行更深入的研究。     

禾草-内生真菌共生体在草地农业系统中的作用

综述了国内外近年对禾草 -内生真菌 (N eotyphodium)的研究进展。全世界现已报道 14种禾草内生真菌 ,与 2 3个属的禾草形成共生体 ,我国已在 13属 2 5种天然草地禾草中发现内生真菌 ,其中发草属 (Descampsia)、大麦属 (H ord eum)和赖草属(L eymus)以往在国际文献中未曾报道。内生真菌在禾草体内产生的生物碱 ,致使采食带菌禾草的马、牛、羊、鹿等家畜产生中毒症状 ,每年给美国、新西兰等国造成的经济损失达 6.4亿美元之多 ,对其毒理研究取得了进展。已发现我国醉马草 (Achnatheruminebrians)对家畜的毒性与内生真菌的侵染有关。内生真菌侵染增加可使禾草对 42种害虫的抗性 ,并可增加对某些线虫和病害的抗性。与不带菌禾草相比 ,带菌禾草的另一特点是抗逆性强 ,牧草产量高。国际在该领域的研究主要集中在多年生黑麦草(L olium p erenne)和高羊茅 (Festuca arundinacea)。我国的研究发现 ,带菌布顿大麦草 (H ordeum bodg anii)和圆柱披碱草(Elymus cylind ricus)的牧草产量分别增加 3 3 .3 %和 2 78.8% ,分孽数分别增加 13 6.8%和 84.5%。目前 ,国际研究的重点包括大规模开展内生真菌生物学与生态学特性的研究 ,创造不含对家畜有害毒素的有益禾草 -内生真菌共生体 ,培育带内生真菌的草坪草品种 ,培育抗毒     

Endophytic fungi: resource for gibberellins and crop abiotic stress resistance

The beneficial effects of endophytes on plant growth are important for agricultural ecosystems because they reduce the need for fertilizers and decrease soil and water pollution while compensating for environmental perturbations. Endophytic fungi are a novel source of bioactive secondary metabolites; moreover, recently they have been found to produce physiologically active gibberellins as well. The symbiosis of gibberellins producing endophytic fungi with crops can be a promising strategy to overcome the adverse effects of abiotic stresses. The association of such endophytes has not only increased plant biomass but also ameliorated plant-growth during extreme environmental conditions. Endophytic fungi represent a trove of unexplored biodiversity and a frequently overlooked component of crop ecology. The present review describes the role of gibberellins producing endophytic fungi, suggests putative mechanisms involved in plant endophyte stress interactions and discusses future prospects in this field.     

Do the costs and benefits of fungal endophyte symbiosis vary with light availability?

? Here, we examined whether fungal endophytes modulated host plant responses to light availability. First, we conducted a literature review to evaluate whether natural frequencies of endophyte symbiosis in grasses from shaded habitats were higher than frequencies in grasses occupying more diverse light environments. Then, in a glasshouse experiment, we assessed how four levels of light and the presence of endophyte symbioses affected the growth of six grass species. ? In our literature survey, endophytes were more commonly present in grasses restricted to shaded habitats than in grasses from diverse light environments. ? In the glasshouse, endophyte symbioses did not mediate plant growth in response to light availability. However, in the host grass, Agrostis perennans, symbiotic plants produced 53% more inflorescences than nonsymbiotic plants at the highest level of shade. In addition, under high shade, symbiotic Poa autumnalis invested more in specific leaf area than symbiont-free plants. Finally, shade increased the density of the endophyte in leaf tissues across all six grass species. ? Our results highlight the potential for symbiosis to alter the plasticity of host physiological traits, demonstrate a novel benefit of endophyte symbiosis under shade stress for one host species, and show a positive association between shade-restricted grass species and fungal endophytes.     

Does a foliar endophyte improve plant fitness under flooding?

Although endophytic fungi are ubiquitous in plants, their full range of ecological effects has yet to be characterized, particularly in non-agronomic systems. In this study, we compared the responses of two congeneric bluegrass species to flooding. Both plant species co-occur in subalpine zones of the Rocky Mountains. Marsh bluegrass (Poa leptocoma) commonly hosts a vertically transmitted fungal endophyte (Epichloë sp.) and naturally grows in wetter conditions than does nodding bluegrass (Poa reflexa), which lacks an epichloid endophyte. We investigated the novel hypothesis that endophyte symbiosis promotes host fitness under flooded conditions, contributing to niche differentiation between the two bluegrass species. We used a factorial greenhouse experiment to test whether endophyte presence improved survival, growth, or reproduction of P. leptocoma under flooded versus non-flooded edaphic conditions by experimentally removing the endophyte from half of the plants. We compared P. leptocoma responses to those of the endophyte-free congener. In contrast to expectations generated from the natural distributions of the two plant species, endophyte presence was more beneficial to P. leptocoma under ambient soil moisture than under flooding. Increased benefits of symbiosis in drier soils are consistent with studies of other grass endophytes. Flooded soils also unexpectedly improved the growth of P. reflexa more than that of the wet habitat specialist, P. leptocoma. While our results demonstrate an overall benefit of fungal symbiosis in this system, ecological factors other than flooding per se likely underlie the observed geographical distributions of these congeneric grasses in nature.     

Direct and indirect effects of the fungal endophyte <Emphasis Type="Italic">Epichloë uncinatum</Emphasis> on litter decomposition of the host grass, <Emphasis Type="Italic">Schedonorus pratensis</Emphasis>

Microbial plant symbionts have been suggested to mediate plant-soil feedback and affect ecosystem functions. Systemic Epichloë fungal endophytes of grasses are found to mediate litter decomposition. These effects are often linked to alkaloids produced by Epichloë species, which are hypothesized to negatively affect decomposers. Although endophytes have been found to affect plant community and soil biota, direct (through litter quality) and indirect (through the environment) effects of fungal endophytes on litter decomposition have been scarcely scrutinized. We placed litterbags with endophyte-symbiotic (E+) and non-symbiotic (E?) Schedonorus pratensis plant litter in plots dominated by E+ or E? plants of the same species, and followed the dynamics of mass losses over time. We predicted the endophyte would hinder decomposition through changes in litter quality and that both types of litter would decompose faster in home environments. E+ litter decomposed faster in both environments. The mean difference between decomposition rate of E+ and E? litter tended to be higher in E? plots. Nitrogen and phosphorus, two elements usually associated with high decomposition rates, were significantly lower in E+ litter. We also detected a higher proportion of C in the cellulose form in E+ litter. Contrary to the general assumption, we found that symbiosis with Epichloë fungal endophytes can be associated with higher decomposition of plant litter. Since direct effects of Epichloë fungi were still stronger than indirect effects, it is suggested that besides the alkaloids, other changes in plant biomass would explain in a context-dependent manner, the endophyte effects on the litter decomposition.     

The interactive effects of plant microbial symbionts: a review and meta-analysis

In nature, plants often associate with multiple symbionts concurrently, yet the effects of tripartite symbioses are not well understood. We expected synergistic growth responses from plants associating with functionally distinct symbionts. In contrast, symbionts providing similar benefits to a host may reduce host plant growth. We reviewed studies investigating the effect of multiple interactions on host plant performance. Additionally, we conducted a meta-analysis on the studies that performed controlled manipulations of the presence of two microbial symbionts. Using response ratios, we investigated the effects on plants of pairs of symbionts (mycorrhizal fungi, fungal endophytes, and nitrogen-fixers). The results did not support the view that arbuscular mycorrhizal (AM) fungi and rhizobia should interact synergistically. In contrast, we found the joint effects of fungal endophytes and arbuscular mycorrhizal fungi to be greater than expected given their independent effects. This increase in plant performance only held for antagonistic endophytes, whose negative effects were alleviated when in association with AM fungi, while the impact of beneficial endophytes was not altered by infection with AM fungi. Generalizations from the meta-analysis were limited by the substantial variation within types of interactions and the data available, highlighting the need for more research on a range of plant systems.