2025/01/29 by Elizabeth M. Lombardi, Hannah E. Marx · 1 voice
Agricultural and Biological Sciences · Biochemistry, Genetics and Molecular Biology · #Plant Pathogenic Bacteria Studies #Plant Virus Research Studies #Plant and Fungal Interactions Research
paper · pdf · doi:10.1002/ajb2.16463
openalex publication_date 2025/01/29 · openalex created_date 2025/10/10 · openalex updated_date 2026/07/28
In the wake of a virus-mediated global health crises, research has rightfully focused on monitoring zoonotic viruses, particularly those that are emerging or novel in human populations (Baker et al., 2022). Viruses that infect plants are also worthy candidates for research investment and, depending on host outcomes, epidemiological action (Anderson et al., 2004; Jones and Naidu, 2019; Jones et al., 2021). While not all viruses are pathogenic (Roossinck, 2011; Takahashi et al., 2019), crop diseases caused by viral symbionts undermine food and economic security worldwide (Bos, 1982; Sastry and Zitter, 2014; Trębicki and Finlay, 2018; Rao and Reddy, 2020), and the consequences of viruses on plant biodiversity and ecosystems are understudied (Kamitani et al., 2016; Jones and Naidu, 2019; Lefeuvre et al., 2019). Better data regarding spatiotemporal patterns in plant-virus distributions is a prerequisite for understanding how viruses move, change, and emerge as threats to food and ecosystem security. One way that temporal trends in virus biodiversity may be studied is through use of natural history collections (Cook et al., 2020; Thompson et al., 2021), which offer the opportunity to retrospectively characterize host–virus interactions, thus building a baseline to which contemporary analyses may be compared. Similarly, Cook et al. (2020) demonstrate the potential benefit of using historical host specimens to efficiently survey for virus diversity across taxa and environments. This work, like most specimen-based research into historical virus diversity, focused on animal hosts. Here we discuss opportunities that would arise from utilizing plant collections in a similar fashion; while the practical and technical details of isolating plant-associated viruses from historical tissue differ from methods for other taxonomic groups, the benefits to research and disease management would be similar and numerous. There are multiple possible virus isolate types that may be useful in studying historical plant virus communities, including agricultural isolates and “forgotten” frozen tissue specimens collected by academic and agricultural researchers (Jones et al., 2021). We discuss pros and cons of using different tissue sources and conclude that usefulness of whole-host data from herbarium specimens justifies investment in development and research. Our objectives in this commentary are to (1) review and compare current resources and approaches available for studying plant-associated virus diversity in the context of natural history and (2) outline steps to improve global plant-virus biodiversity monitoring and preservation going forward. One of the primary reasons that it is important to build virus biodiversity baselines across space and time is to monitor emergence of novel pathogenic viruses that may threaten native plant species and agricultural hosts. Most basically, monitoring efforts cannot detect changes in biotic interactions without iterative sampling that measures turnover of species interactions compared to previous measurements (Magurran et al., 2010). Beyond that, downstream models and analyses documenting the impacts of a change on plant–virus interactions (e.g., elevated atmospheric carbon dioxide; see Scandolera et al., 2024) are improved when historical data are available (Willis et al., 2010). Long-term plant–virus data sets that would be useful for detecting change in virus–host communities over time are rare. Most temporal data sets are assembled through experimental studies of manipulated infections in controlled conditions such as greenhouses (Pagán et al., 2010; Montes et al., 2020). These are helpful in studying specific interactions but may not be generalizable across host or virus taxa and do not provide any insight into natural virus communities in wild plant hosts. Novel analyses of preserved tissue from taxonomically diverse hosts is the only direct way to generate new information or biodiversity baselines up to this point. Multiple types of resources exist for studying plant–virus interactions in a historical context (Table 1). These fall under four broad categories—virus taxonomic resources, qualitative data resources, and two categories of host tissue repositories (partial- vs. whole-host resources)—which we expand upon below. Each of these resources have limitations, but together represent a chance at characterizing a poorly understood dimension of plant ecology, evolution, and biodiversity. Botanical specimens preserved in herbaria are considered a type of host tissue repository. We argue herbarium collections are the most accessible (Figure 1), scientifically informative, and a largely untapped source of historic host and virus information. Until relatively recently, nomenclature and organization of viruses depended on the identity of their known hosts, viral morphology and characteristics, but did not include quantitative studies of genomic similarity (Koonin et al., 2021). Viral genome sequencing has allowed for a more detailed understanding of evolutionary relatedness between viruses themselves, which in turn sheds light on how viruses differ across taxonomic groups and over time (Simmonds et al., 2017; Lefkowitz et al., 2018). Past and current iterations of virus taxonomic databases have been built to curate data on virioplanktonic (Xie et al., 2021), vertebrate-associated (Carlson et al., 2022), and plant-associated viruses (Brunt et al., 1996; Adams and Antoniw, 2006). A universal, virus-focused community of researchers has established working groups to describe and update virus taxonomic lists, thus providing an index of all known viruses (International Committee on the Taxonomy of Viruses [ICTV]) (Lefkowitz et al., 2018). Taxonomic lists generated and revised by these experts are important for tracking the number of accepted virus taxa, and through the ever-growing length of the virus species list. it is clear that there are many more species than documented. Virus taxonomic checklists, however, are a tool that depends on new research for detection and discovery of plant-associated symbionts, which relies on generating new data from taxonomically diverse hosts sampled across environments and time. Image- and text-based detection of virus infections that induce visible symptoms may be useful when the etiology of specific host–virus interactions is well defined, and previous research has used other historical resources (e.g., poetry, herbal guides, garden lists) to locate plant–virus interactions centuries before the first virus was isolated. For example, the earliest record of a plant–virus interaction is described in the Man'yoshu anthology of Japanese poetry from the year 752 (Saunders et al., 2003) in which Empress Kōken describes premature yellowing in the leaves of eupatorium plants in the summer. Contemporary virologists have demonstrated that the yellow streaking leaf phenotype is present in hosts only when infected by a geminivirus, eupatorium yellow-vein virus, and accompanying satellite component (Saunders et al., 2003). Similarly, the condition of leaf yellowing associated with common virus infections were described circa the year 1000 by Surapala in the Vrikshayurveda (Sadhale, 1996; Rishi, 2009), and there is abundant archival evidence of tulip break virus infections in paintings, texts, and ledgers from mid-17th century Holland (Lesnaw and Ghabrial, 2000). Each of these archival observations of virus infections in plants demonstrates a history of biotic interaction that predates modern molecular diagnostic methods. These historical observations should be considered as hypotheses rather than direct evidence of specific host–virus interactions that may be addressed with modern resources including machine learning (e.g., natural language learning) and other types of artificial intelligence, with the caveat that symptomology alone is insufficient for virus identification. Similarly, but in more modern fashion, image and genome databases present opportunistic data that may be useful in studying plant–virus interactions in space and recent history, but they lack physical material specimens that are necessary to validate and quantify the hypothetical host and virus taxa. Public data repositories such as iNaturalist (www.inaturalist.org) provide photographs and taxonomic identifications made by community members who may upload and identify possible virus occurrences based on induced host phenotypes. We acknowledge the potential of using image-based plant virus identification for documenting well-described pathosystems as a way to explore the temporal and spatial breadth of occurrences, but emphasize the need for caution and additional, molecular evidence to confirm the specific infection (see Lombardi, 2022). One of the largest global data resources that may provide a centralized structure for studying virus occurrence and diversity research is the Global Biodiversity Information Facility (GBIF; www.gbif.org). GBIF holds enormous amounts of data on diverse taxa and currently hosts global virus records from across hosts. One GBIF data set of virus occurrence data includes viral identifications from taxonomically diverse hosts and viruses and is based on genetic sequence similarity with known viral contigs that were detected and uploaded by the International Nucleotide Sequence Database Collaboration (INSDC) (DOI: 10.15468/e97kmy). Material specimens are by far the most common basis of virus records in this data set, though there are also some preserved whole hosts representing less than 1% of the full data set. Of the GBIF virus occurrence data set, approximately 95,000 records (~10%) match to plant-associated viruses based on genus-level classifications made by ICTV, and of these records only 9235 records have coordinate data (9.7%). Most of the plant-associated virus occurrences in this data set are identified through an API that trawls INSDC sequences and assemblies that are available in public data sets, and thus these records require further exploration, validation, and curation. Nonetheless and despite limitations, the GBIF and the INSDC-reliant virus occurrence data set is the largest global resource currently available for studying virus diversity across taxa and may represent physical specimens with institutional metadata that can be utilized for follow-up analyses and validation. Reproducibility and validation of virus occurrence records depends on adequate host and institution data, which are provided when Darwin Core data standards are met and digital integration of records is maintained. One way to generate new information about historical virus communities is through high-throughput sequencing of viral genomes from preserved host tissue. The different types of historical host material from which viral genomes may be isolated have strengths and weaknesses, but are all potentially useful depending on specific research questions (Table 1). Partial-host tissue specimens include leaf punches or samples, cultures, and seeds. Whole-host material specimens are either living specimens (curated in living collections or naturally occurring) or herbarium specimens (Figure 2). Small RNA sequencing is the gold standard for characterizing contemporary virus communities isolated from fresh host material because it allows researchers to capitalize on host-associated interference (RNAi) genes that respond to any viruses present and therefore allows for identification and genome assembly of both RNA and DNA viruses (Pooggin, 2018). Furthermore, small RNA sequencing may be more robust when material is degraded (Rieux et al., 2021) and is therefore a promising approach for detection of historical infections as well. Previous research has demonstrated the usefulness of sequencing for studying viruses in preserved tissue from various host taxa including wheat (Malmstrom et al., 2007, 2022), cassava (Rieux et al., 2021), and tobacco (Fraile et al., 1997). Thanks to the small size of partial-host specimens, tissues may be preserved in freezers or liquid nitrogen, which increases the likelihood of virus genome et al., et al., 2022). conditions are across research groups, however, with some of small RNA or sequencing of partial-host tissue has been used to isolate viruses from tissue despite in frozen et al., and leaves (Rieux et al., 2021) and is accepted as of the most sequencing methods for virus research because of the to that are or RNA or DNA viruses (Pooggin, 2018; et al., 2019). on the other has not been at RNA or DNA though preservation of from plants has a more common as collections are used for genomic The most and accessible source of whole plant host are though living plant collections (e.g., may also provide tissue material that would the of plant virus communities with data from the full host phenotype and in context of the and plant In to using leaf or the use of tissue from specimens allows virus biodiversity to be considered across and with In an and for would all plants would have associated tissue specimens that were for and there would be a centralized global or data that research across In however, plants with specimens have frozen or and there is for genetic information for viruses and plant hosts accessible et al., (Figure 1). Furthermore, while the global of collections herbaria more accessible resources than tissue repositories (Figure 1), of global and are and to biodiversity research et al., 2020; et al., of all herbaria and of all specimens collected are in that were the of with many of these records in of biodiversity that were considered and by et al., in the of resources, specimens to research from their and of as new is are necessary to improve global biodiversity regarding plants and their We acknowledge these and that specimens are currently the most accessible resources we have for studying plant viruses across time and Of the resources only specimens by herbaria offer the opportunity to information about plant–virus interactions across global environments (Figure et al., host taxa et al., 2018; et al., and temporal (Malmstrom et al., 2007, 2022). plants on herbarium provide data, host data, and genetic resources demonstrated by 2). to the usefulness of isolating viruses from host tissues or qualitative resources like and the benefits of studying historical plant-associated viruses in the context of whole host information data are and cannot be (see the are but in and thus worthy of investment and methods and for studying viruses preserved in herbarium specimens provide insight into biodiversity that is to Here we discuss opportunities provided by virus research as a way to further development and isolated from herbarium specimens can with of viral through (1) detecting temporal changes in virus (2) monitoring disease symptoms and, viral from collections that may be for the and of wild While novel discovery the identification of may not be using RNA or DNA from herbarium of wild native plant species for infections of known viruses would represent a useful in wild plant The and number of accepted viral taxa with accessible genomes it possible to many viruses that may have been present in plant communities of the particularly those that disease and have been to their impacts on In these sampling of pathogenic viruses from herbaria multiple time for studying viral across space and host taxa and may also the to which virus impacts the host visible and other In in which cannot be from collections of infected hosts specimens, further evidence for evolutionary impacts of infection may be by contemporary and host or preserved associated with herbarium In all host information available through specimens is for how virus interactions are and or not trends emergence in wild While many viral symbionts that may be detected through may not there are epidemiological of studying virus biodiversity and across host taxa. between wild and crop hosts is particularly in and 2004; et al., 2011; et al., and monitoring plant populations over time may improve While the most for crop is detection of infected plants in and wild to it is also useful to which viruses have been present in et al., et al., and which have herbarium specimens, particularly those collected from in which are may agricultural researchers and and crop to viruses and monitoring is also important for and preservation of native plant species et al., 2019; et al., 2022). is known about the diversity of plant-associated viruses, particularly in wild hosts, that it is currently not possible to the that pathogenic viruses have on native plants et al., 2019). important resources for the of plant–virus across native host taxa that viral diseases may be identified and to native plant the of virus for and wild hosts at (Roossinck, and on conditions by the In a time of change, to plant environments biotic interactions and may the and of virus disease symptoms in wild hosts et al., 2016; Trębicki et al., 2016; 2020; et al., 2021). virus communities from herbarium specimens collected across characterize viruses have been in the common plant that be and virus conditions (e.g., carbon or and provide information useful to researchers monitoring plant epidemiological under groups, from researchers to may to working with herbaria as community for the development of new that to plant-associated Similarly, the of collections such as herbaria depends on for new and We present but not possible that herbaria and benefit from between communities of researchers and and as the use of historical natural history collections can with detection of including monitoring of viral emergence in natural plant would need to include natural history and of viral on the of monitoring efforts to infected or other such efforts would also include from across and to with the public regarding the plant viruses in Collaboration between natural history collections agricultural and virologists would also monitoring and management of viral symbionts that as have in agricultural and have made collections to Collaboration between (e.g., and food may improve crop by Furthermore, efforts between and natural history researchers improve of crop taxa in which to be native and taxa and historical virus communities between and crop wild efforts to viral in of and across is necessary to and across which herbaria in may be well to as to between research and for plant-virus research that herbarium data is in the use of machine learning models to detect disease symptoms in specimens or In the the number of using some of machine learning has et al., and with a models to identify disease symptoms in of plants et al., there are known and symptoms of virus infection such as leaf (e.g., it is possible that approaches to models may be of virus infections from Similarly, or as a models that may associated with herbarium specimens and identify those with some of phenotype worthy of further et al., this we do not of any to use models to historical virus infections in plants using any of the historic data resources we discuss (Table we and between and with the to generate new data and build analyses based on While there are many potential benefits of using herbarium specimens to historical plant-virus communities, there are also that be and and useful herbarium specimens based on resource and research questions may be a for some researchers (Figure While herbaria are more accessible than tissue repositories (Figure 1), there are some with or collections that may not be for and it may not be possible or to for viral genomes et al., 2019). to information are in or have not for some which the and discovery of biodiversity 2017; et al., 2019). Furthermore, some herbaria may specific taxa with temporal or spatial than the first for researchers is to identify which specimens are to specific and and to from the most that may the usefulness of herbaria for studying plant–virus interactions is viral genome (Figure We need to quantify virus over time and in preserved tissue types (e.g., leaf vs. preservation and diverse plant host taxa. is that all herbarium specimens more virus genomes than fresh or frozen tissue et al., et al., 2022), and we a between the length of time host and the of genomic both of these hypotheses need to be further across taxonomic with modern sequencing and detection built on databases and 2024) and machine learning models and 2014; et al., 2017; et al., 2022), identification and validation of virus genome sequences from herbarium tissue is and of research objectives (Figure We that viral genomes the they are preserved to and which the of genome assembly high-throughput sequencing and the of such as experimental (Fraile et al., and of viral or sequences et al., 2022), or other methods to validate virus from degraded is is the and in virus genome over time. these of preserved viral or not or other viral diversity are in preserved We that the first for methods development is to virus genome in hosts over time to or not there are or for isolating DNA or RNA viruses from In the small RNA sequencing and includes sequences associated with host and is therefore of viruses based on diverse and is the for et al., 2017; 2018; et al., 2019), but further development and For studying historical plant–virus interactions across host taxa, it is to genomic sequencing using (e.g., or a (Figure For many virus small RNA of the diversity of viral though virus contigs downstream insight and more include and sequence assembly of virus host virus identification based on virus genome virus genome and, analyses and (Figure that on viral such as and or sequencing of specific may also be useful when experimental and questions but these approaches are for when the viral in is known and well validation of sequencing using these methods is a that researchers using herbarium specimens may in studies of historical plant–virus interactions (Figure In to and genome we also that made by in the to plant-associated and researchers who plant specimens are to as of a and are to infected plant to both with the of the but also the of the of the for plant focused most herbarium collections hosts infected with any type of Viral symbionts do not induce it is that infected plant hosts have been collected for an collections would that all specimens also have associated preserved leaf genetic samples, and other data we of whole plants to also and curate diverse specimens in to This is particularly important multiple hosts similar which relatively or a species or We acknowledge that collections the of and from a there are many and important to this in collections including specimens with that are as new specimens with or (e.g., or specimens collected in for like In to new collections that host-associated virus communities, there is also for of physical and digital to preservation and of these methods to or for when from specimens in herbaria should be a considered by researchers to historical communities (see et al. for further however, investment is into the development of new associated with of of virus improve of the of and diverse between research communities with For example, and data through the of at the of in has research into taxonomically diverse hosts et al., and zoonotic and (Cook et al., and has public health monitoring et al., Each material that is at the is associated with specimens with data, and This demonstrates though not the only to resources without or A for more like the at institutional and as well as a approach to digital data et al., a new of biodiversity research across and understanding of host-associated virus viruses are across host taxa and but is known regarding the history and of plant–virus interactions in wild plant are and whole-host resources that may provide insight into questions about the and consequences of plant–virus for and practical this the to use of these biodiversity collections is the development of adequate methods to how and virus communities are when isolated from we for new collections of plants and of specimens to tissue in or in and research working of herbaria can provide important insight for the of plant communities and across the with opportunities to improve of data and resources going forward. viruses are are their hosts and who may we an this understudied of plant biodiversity. to data and and to and We all of the who have collected and herbarium specimens all over the their and we would have for understanding historical impacts of plant associated viruses on We also for and the who provided helpful on this This was as of the of in