The pollen virome: A review of pollen-associated viruses and consequences for plants and their interactions with pollinators.

The movement of pollen grains from anthers to stigmas, often by insect pollinator vectors, is essential for plant reproduction. However, pollen is also a unique vehicle for viral spread. Pollen-associated plant viruses reside on the outside or inside of pollen grains, infect susceptible individuals through vertical or horizontal infection pathways, and can decrease plant fitness. These viruses are transferred with pollen between plants by pollinator vectors as they forage for floral resources; thus, pollen-associated viral spread is mediated by floral and pollen grain phenotypes and pollinator traits, much like pollination. Most of what is currently known about pollen-associated viruses was discovered through infection and transmission experiments in controlled settings, usually involving one virus and one plant species of agricultural or horticultural interest. In this review, we first provide an updated, comprehensive list of the recognized pollen-associated viruses. Then, we summarize virus, plant, pollinator vector, and landscape traits that can affect pollen-associated virus transmission, infection, and distribution. Next, we highlight the consequences of plant-pollinator-virus interactions that emerge in complex communities of co-flowering plants and pollinator vectors, such as pollen-associated virus spread between plant species and viral jumps from plant to pollinator hosts. We conclude by emphasizing the need for collaborative research that bridges pollen biology, virology, and pollination biology.

The pollen virome of wild plants and its association with variation in floral traits and land use.

Pollen is a unique vehicle for viral spread. Pollen-associated viruses hitchhike on or within pollen grains and are transported to other plants by pollinators. They are deposited on flowers and have a direct pathway into the plant and next generation via seeds. To discover the diversity of pollen-associated viruses and identify contributing landscape and floral features, we perform a species-level metagenomic survey of pollen from wild, visually asymptomatic plants, located in one of four regions in the United States of America varying in land use. We identify many known and novel pollen-associated viruses, half belonging to the Bromoviridae, Partitiviridae, and Secoviridae viral families, but many families are represented. Across the regions, species harbor more viruses when surrounded by less natural and more human-modified environments than the reverse, but we note that other region-level differences may also covary with this. When examining the novel connection between virus richness and floral traits, we find that species with multiple, bilaterally symmetric flowers and smaller, spikier pollen harbored more viruses than those with opposite traits. The association of viral diversity with floral traits highlights the need to incorporate plant-pollinator interactions as a driver of pollen-associated virus transport into the study of plant-viral interactions.

Pollinator effectiveness is affected by intraindividual behavioral variation.

Variation in pollinator quality is fundamental to the evolution of plant-pollinator mutualisms and such variation frequently results from differences in foraging behavior. Surprisingly, despite substantial intraindividual variation in pollinator foraging behavior, the consequences for pollen removal and deposition on flowers are largely unknown. We asked how two pollen foraging behaviors of a generalist pollinator (Bombus impatiens) affect removal and deposition of heterospecific and conspecific pollen, key aspects of pollinator quality, for multiple plant species. In addition, we examined how bee body size and pollen placement among body parts shaped pollen movement. We manipulated foraging behavior types using artificial flowers, which donated pollen that captive bees then deposited on three recipient plant species. While body size primarily affected donor pollen removal, foraging behavior primarily affected donor pollen deposition. How behavior affected donor pollen deposition depended on the plant species and the quantity of donor pollen on the bee's abdomen. Plant species with smaller stigmas received significantly less pollen and fewer bees successfully transferred pollen to them. For a single plant species, heterospecific pollen interfered with conspecific pollen deposition, such that more heterospecific pollen on the bee's abdomen resulted in less conspecific pollen deposition on the flower. Thus, intraindividual variation in foraging behavior and its interaction with the amount and placement of acquired pollen and with floral morphology can affect pollinator quality and may shape plant fitness via both conspecific and heterospecific pollen transfer.

Integrating microbes into pollination.

Microbes (fungi, bacteria and viruses) living within flowers are hypothesized to affect pollination. We evaluate current support for this idea at each stage of the pollination process. Evidence to date is convincing that microbes influence pollinator attraction, but data are heavily weighted toward bumblebees and the effects of nectar yeasts. Effects of microbes on the efficacy of pollinator visits is understudied and variable outcomes from field studies suggest quality of pollinator visits, not only quantity, are likely involved. The effect of microbes on pollen performance is underappreciated. Beyond the effect of pathogenic viruses, the impacts of pollen-transmitted endophytic microbes on pollen viability or tube growth are unknown but could affect the outcome of pollen receipt. Future research integrating microbes into pollination should broaden taxonomic diversity of microbes, pollinators and plants and the processes under study.

Coding-Complete Genome Sequence of a Pollen-Associated Virus Belonging to the Secoviridae Family Recovered from a Japanese Apricot (Prunus mume) Metagenome Data Set.

We report the coding-complete genome sequence of Japanese apricot pollen-associated secovirus 1 (JAPSV1), a virus belonging to the Secoviridae family, recovered from Japanese apricot (Prunus mume) pollen that is closely related to Peach leaf pitting-associated virus (PLPAV). This discovery adds to the number of known pollen-associated viruses.

Gazing into the anthosphere: considering how microbes influence floral evolution.

The flower is the hallmark of angiosperms and its evolution is key to their diversification. As knowledge of ecological interactions between flowers and their microbial communities (the anthosphere) expands, it becomes increasingly important to consider the evolutionary impacts of these associations and their potential eco-evolutionary dynamics. In this Viewpoint we synthesize current knowledge of the anthosphere within a multilevel selection framework and illustrate the potential for the extended floral phenotype (the phenotype expressed from the genes of the plant and its associated flower microbes) to evolve. We argue that flower microbes are an important, but understudied, axis of variation that shape floral trait evolution and angiosperm reproductive ecology. We highlight knowledge gaps and discuss approaches that are critical for gaining a deeper understanding of the role microbes play in mediating plant reproduction, ecology, and evolution.

Considering the unintentional consequences of pollinator gardens for urban native plants: is the road to extinction paved with good intentions?

Urban centers are important foci for plant biodiversity and yet widespread planting of wildflower gardens in cities to sustain pollinator biodiversity is on the rise, without full consideration of potential ecological consequences. The impact of intentional wildflower plantings on remnant native plant diversity in urban and peri-urban settings has not received attention, although shared pollinators are likely to mediate several types of biotic interactions between human-introduced plants and remnant native ones. Additionally, if wildflower species escape gardens these indirect effects may be compounded with direct ones. We review the potential positive and negative impacts of wildflower gardens on urban native flowering plants, and we reveal substantial gaps in our knowledge. We present a roadmap for research to address whether wildflower gardens, while benefiting pollinators, could also hasten the extinction of native remnant plants in urban settings, or whether they could have other effects that enrich urban biodiversity. Goals of future wildflower mixes should consider the totality of potential interactions.