Summary1. Foliar endophytic fungi in herbaceous plants are known to be diverse, yet studies characterizing the fungal communities in roots and shoots of plants across time are absent. These fungi are supposedly ubiquitous in nature, infecting plants through airborne spores. As many foliar endophytes can also exist in soil, we hypothesized that there would be a strong similarity between root and shoot endophytes in any given plant species and that differences between plant species would be greater than those between organs within a species. 2. Leaf and root fungal endophyte communities were assessed in field-collected plants of three co-occurring grassland forbs (Cirsium arvense, Plantago lanceolata and Rumex acetosa) in two contrasting seasons (winter and summer). The former two species are mycorrhizal, whilst the latter species is not so. 3. The highest fungal species richness was recorded from P. lanceolata with R. acetosa hosting the least endophyte diversity. Endophyte communities were more diverse in root than leaf tissues and in summer than in winter. Similarity of endophyte communities between different host plant species and organs within an individual host was very low. Negative correlations were found between mycorrhizal colonization and endophyte presence in the roots of C. arvense and P. lanceolata, suggesting some degree of antagonism or competition between the fungi. Consistent positive associations were found between the number of endophyte species in roots and shoots of plants. 4. Synthesis. In contrast to previous studies, the results show that many endophytes do not occur ubiquitously, but instead exhibit both plant and tissue specificity. There is a strong seasonal change in endophyte communities, but the differences between roots and shoots at any one time can be just as large. This dissimilarity suggests a lack of systemic growth by the fungi from one tissue to another. Mycorrhizas may interact negatively with other root endophytes, indicating that the latter should not be ignored in future mycorrhizal studies. We should begin to think of individual plants as ecosystems of interacting microbes, whose community is structured by plant genetics and environmental conditions, coupled with interactions between the microbes themselves.

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To date, it has been thought that endophytic fungi in forbs infect the leaves of their hosts most commonly by air-borne spores (termed “horizontal transmission”). Here, we show that vertical transmission from mother plant to offspring, via seeds, occurs in six forb species (Centaurea cyanus, C. nigra,Papaver rhoeas,Plantago lanceolata,Rumex acetosa, and Senecio vulgaris), suggesting that this may be a widespread phenomenon. Mature seeds were collected from field-grown plants and endophytes isolated from these, and from subsequent cotyledons and true leaves of seedlings, grown in sterile conditions. Most seeds contain one species of fungus, although the identity of the endophyte differs between plant species. Strong evidence for vertical transmission was found for two endophyte species, Alternaria alternata and Cladosporium sphaerospermum. These fungi were recovered from within seeds, cotyledons, and true leaves, although the plant species they were associated with differed. Vertical transmission appears to be an imperfect process, and germination seems to present a bottleneck for fungal growth. We also found that A. alternata and C. sphaerospermum occur on, and within pollen grains, showing that endophyte transmission can be both within and between plant generations. Fungal growth with the pollen tube is likely to be the way in which endophytes enter the developing seed. The fact that true vertical transmission seems common suggests a more mutualistic association between these fungi and their hosts than has previously been thought, and possession of endophytes by seedling plants could have far-reaching ecological consequences. Seedlings may have different growth rates and be better protected against herbivores and pathogens, dependent on the fungi that were present in the mother plant. This would represent a novel case of trans-generational resistance in plants.

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Summary1 Endophyte fungi exist within the living tissues of all plants, but compared with grasses and trees, remarkably little is known about their ecology in herbaceous species. These fungi produce an array of metabolites in culture and there is some evidence that they can increase the resistance of plants to herbivorous insects. 2 As herbaceous plant endophytes are thought to be unspecialized, ubiquitous taxa, we hypothesized that their occurrence within two closely related plant species would not vary between local plant communities. Furthermore, we expected to find negative relations between endophyte occurrence and that of a herbivorous insect. 3 We tested these hypotheses by isolating endophytes from Leucanthemum vulgare and Cirsium arvense (Asteraceae) plants growing together in five populations, each about 13 km apart. Damage by the leaf mining fly, Chromatomyia syngenesiae , was also measured on each plant. 4 C. arvense harboured more species of fungi per plant and the number of isolates recovered per leaf was also higher. Several fungi showed differences in occurrence within the two plants, but these differences were not consistent between sites. The similarity in the endophyte assemblage decreased with increasing intersite distance in C. arvense , but not in L. vulgare . We conclude that endophytes either colonize C. arvense more readily or have greater activity within this host (or both). 5 Leaf miner attack was positively related to total endophyte species number in L. vulgare , but not so in C. arvense , while occurrence of Chaetomium species was negatively associated with insect attack in both plants. In L. vulgare , only 5% of relations between occurrence of different endophyte species were significant, but in C. arvense this figure was 43% and all were negative. 6 This study has important implications for understanding the factors that influence plant resistance to insects. It is the first report of endophytic fungi affecting host plant choice by insects in herbaceous plants. The abundance of unspecialized endophytes in forbs means that they are a neglected, but important, aspect of plant-herbivore relations.