Dr. Iva Franic

Purpose of review: Because tree seeds have been considered a low-risk pathway for the spread of plant pathogenic fungi, their international movement is not subject to strict phytosanitary regulation. However, recent studies have provided scientific evidence that the biosecurity risk of seed trade may not be as negligible as assumed. This review summarises current knowledge about seed trade activity across the world and seed-borne plant pathogenic fungi and highlights knowledge gaps that need to be filled to mitigate the risk of spreading tree pathogens via seeds.
Recent findings: Several outbreaks of severe tree diseases in natural forests and plantations worldwide have been linked to fungal pathogens spread by seed trade. Indeed, recent studies based on modern sequencing technologies have shown that tree seeds harbour highly diverse fungal communities, including well-known pathogens and fungal taxa belonging to unknown species. While it has become clear that even apparently healthy seeds can carry potentially pathogenic fungi, the likelihood of seed-borne pathogens being introduced and becoming established, spreading and causing impact in the new environment is still unclear which challenges the assessment of the phytosanitary risk posed by seed trade.
Summary: Our analyses show that large amounts of tree seeds have been traded among countries and continents. Based on published literature, the risk of spreading pathogenic fungi via tree seed movement is high. However, the role of the taxonomically and functionally diverse fungal communities associated with seeds is still poorly understood. In particular, more research is needed to assess the likelihood of seed-borne fungi being transmitted to the seedlings and spreading and causing impact in the new environment.

Non-native pests, climate change, and their interactions are likely to alter relationships between trees and tree-associated organisms with consequences for forest health. To understand and predict such changes, factors structuring tree-associated communities need to be determined. Here, we analysed the data consisting of records of insects and fungi collected from dormant twigs from 155 tree species at 51 botanical gardens or arboreta in 32 countries. Generalized dissimilarity models revealed similar relative importance of studied climatic, host-related and geographic factors on differences in tree-associated communities. Mean annual temperature, phylogenetic distance between hosts and geographic distance between locations were the major drivers of dissimilarities. The increasing importance of high temperatures on differences in studied communities indicate that climate change could affect tree-associated organisms directly and indirectly through host range shifts. Insect and fungal communities were more similar between closely related vs. distant hosts suggesting that host range shifts may facilitate the emergence of new pests. Moreover, dissimilarities among tree-associated communities increased with geographic distance indicating that human-mediated transport may serve as a pathway of the introductions of new pests. The results of this study highlight the need to limit the establishment of tree pests and increase the resilience of forest ecosystems to changes in climate.

International trade in plants and climate change are two of the main factors causing damaging tree pests (i.e. fungi and insects) to spread into new areas. To mitigate these risks, a large-scale assessment of tree-associated fungi and insects is needed. We present records of endophytic fungi and insects in twigs of 17 angiosperm and gymnosperm genera, from 51 locations in 32 countries worldwide. Endophytic fungi were characterized by high-throughput sequencing of 352 samples from 145 tree species in 28 countries. Insects were reared from 227 samples of 109 tree species in 18 countries and sorted into taxonomic orders and feeding guilds. Herbivorous insects were grouped into morphospecies and were identified using molecular and morphological approaches. This dataset reveals the diversity of tree-associated taxa, as it contains 12,721 fungal Amplicon Sequence Variants and 208 herbivorous insect morphospecies, sampled across broad geographic and climatic gradients and for many tree species. This dataset will facilitate applied and fundamental studies on the distribution of fungal endophytes and insects in trees.

Recent studies revealed a high diversity of fungal endophytes in traded tree seeds, including potential plant pathogens. The factors determining richness and composition of seed mycobiomes are poorly understood, but might be an important determinant for tree health. We assessed the relative impact of host identity, site, several site-specific environmental factors, and whether the host was sampled in its native or non-native distribution range, on the richness and composition of fungal seed endophytes of nine tree species across 15 sites in Europe and North America. Our results show that fungal richness was affected by host identity, but not by environmental variables or host distribution range. Fungal community composition was primarily driven by host identity, and to a lesser extent by environment. Around 25% of the 2147 amplicon sequence variants (ASVs) were generalists appearing on both continents and in both gymnosperms and angiosperms. Around 63% of the ASVs appeared in only gymnosperms or angiosperms, and 33% of the ASVs were associated with a single host species, while none were found in all tree species. Our results suggest that although seed trade might facilitate movements of fungi, their establishment and spread in the new environment might be limited by host availability.

Seeds and dormant twigs carry a large diversity of potentially pathogenic fungi and insects - vigilance when importing or exchanging plant material is therefore highly recommended.

Aim: Early warning against potentially harmful organisms of woody plant species can be achieved by sampling sentinel plants in exporting countries. However, it is unclear where sentinel plants can best be located, and how many samples are required and when and how often sampling optimally should take place for the adequate assessment of the biodiversity associated with the target plant species. We aimed to review spatial and temporal factors affecting associate biodiversity of single woody plant species and to develop guidance for the design of global biodiversity sampling studies.
Location: Worldwide.
Taxon: Insects and Fungi.
Methods: Literature about factors affecting the diversity of insects and fungi in association with single plant species on global, regional, local and different temporal scales was reviewed. Case studies of insect and fungal diversity, primarily collected on single plant species, and the cost of collecting and analysing samples from locations around the world were analysed.
Results: The review of the literature illustrated various factors affecting diversity, and the case studies allowed quantification of the relative impact of some spatial, temporal and financial aspects on captured biodiversity and, thus, illustrate the need to consider all possible factors that may affect the result of the sampling when deciding on a sampling design.
Main conclusions: Our study illustrates the factors that should be considered when deciding on the location and timing of sampling for sentinel plants, which is important because of the trade‐off between the number of samples and sampling locations needed to detect many of the species which may be potential pests, and the cost of (repeated) sampling in many locations. Decisions about the sampling design must be based on the objective of the sampling, but our recommendations apply irrespective of the targeted plant species or country.

The international seed trade is considered relatively safe from a phytosanitary point of view and is therefore less regulated than trade in other plants for planting. However, the pests carried by traded seeds are not well known. We assessed insects and fungi in 58 traded seed lots of 11 gymnosperm and angiosperm tree species from North America, Europe, and Asia. Insects were detected by X‐raying and molecular methods. The fungal community was characterized using high‐throughput sequencing (HTS) and by growing fungi on non‐selective agar. About 30% of the seed lots contained insect larvae. Gymnosperms contained mostly hymenopteran (Megastigmus spp.) and dipteran (Cecidomyiidae) larvae, while angiosperms contained lepidopteran (Cydia latiferreana) and coleopteran (Curculio spp.) larvae. HTS indicated the presence of fungi in all seed lots and fungi grew on non‐selective agar from 96% of the seed lots. Fungal abundance and diversity were much higher than insect diversity and abundance, especially in angiosperm seeds. Almost 50% of all fungal exact sequence variants (ESVs) found in angiosperms were potential pathogens, in comparison with around 30% of potentially pathogenic ESVs found in gymnosperms. The results of this study indicate that seeds may pose a greater risk of pest introduction than previously believed or accounted for. A rapid risk assessment suggests that only a small number of species identified in this study is of phytosanitary concern. However, more research is needed to enable better risk assessment, especially to increase knowledge about the potential for transmission of fungi to seedlings and the host range and impact of identified species.