From Plant Press, Vol. 24, No. 3, July 2021.
By Gary A. Krupnick
The 18th Smithsonian Botanical Symposium, co-hosted by the Smithsonian’s Department of Botany and the United States Botanic Garden, was held virtually over two days on May 13 and 14, 2021. The Symposium, “Plant symbiosis: The good, the bad, and the complicated,” was originally scheduled to take place in May 2020 at the National Museum of Natural History (NMNH) in Washington, DC, but the coronavirus global pandemic pushed the symposium to 2021. The digital event this year successfully brought together six engaging speakers in a Zoom webinar setting to explore current research in the diversity of plant symbioses, examining the relationships plants have with insects, fungi, bacteria, and even other plants. Invited speakers included botanists, ecologists, microbiologists, and geneticists whose research unravels the complicated relationships that plants have with their collaborators and competitors in the natural world.
Eric Schuettpelz, Chair of Botany at NMNH, welcomed the virtual audience to the symposium and Rebecca Johnson, Associate Director for Science and Chief Scientist at NMNH, provided opening remarks. Johnson spoke about our strong relationship with the U.S. Botanic Garden and talked about our shared mission to educate the public about plants and their importance to people and the environment. She celebrated the amazing progress that the Botany Department has made in fully digitizing the specimens in the U.S. National Herbarium and the benefits of those digitized specimens to the scientific community. Even though the museum’s doors have been closed, the research still goes on.
Kenneth Wurdack, NMNH Department of Botany, presented the annual José Cuatrecasas Medal for Excellence in Tropical Botany to Sebsebe Demissew from Gullele Botanic Garden and Addis Ababa University, Ethiopia. Demissew accepted the Cuatrecasas Medal from Africa. He expressed his gratitude and encouraged those viewing the symposium to initiate collaboration with Ethiopian botanists.
Naomi Pierce from Harvard University delivered the first presentation, “Context dependent evolution of the African ant acacia, Vachellia drepanolobium, and its multitude of symbionts.” She spoke about the classic mutualism of a plant exchanging house and food for patrolling ants. Vachellia drepanolobium with its swollen thorn ant domatia is a dominant tree found on black cotton soils in East Africa. Phytoecious ants (Crematogaster mimosae, C. nigriceps, and Tetraponera penzigi) occupy different trees with one colony per tree.
Pierce’s research shows that the classic two-species mutualism is not exactly accurate, and that these mutualisms consist of a multiparty, complex network of interactions. She spoke about her studies with myrmecophiles (insects that live in association with ants), fungi, and bacteria. Her field research shows that 25 species of lycaenid butterflies parasitize acacia-ant mutualisms. She described how trees occupied by the most aggressive ant species, C. mimosae, have more myrmecophiles than those inhabited by C. nigriceps or T. penzigi. Likewise, fungal communities and bacterial communities are distinctive in the trees occupied by different ants. What Pierce found most interesting is that the possible true mutualisms within the system could be between the plant and fungus, and the ants may simply be the vector to carry the fungal cocktail between trees.
Pierce wrapped up her presentation talking about an unexpected detour that yielded a very interesting result. Can plants respond to the smell of the ants? Different ant inhabitants influence host plant architecture, including domatia size and branching pattern. Pierce’s research shows that plants respond differently to the smells of different ant species. Plants exposed to symbiotic ant odor produced more branches, and plants exposed to the odor of T. penzigi produced fewer extrafloral nectaries. She summarized that mutualisms are complex networks and because of that one should be careful about assigning causality to observed effects because there may be multiple parties involved.
The second presentation of the symposium was delivered by Jay Bolin of Catawba College. His presentation, "Hydnora from fungus to foul flower: the natural history of the strangest plants in the world," took us on a journey through the history, ecology, and evolution of a grotesquely beautiful and bizarre plant parasite. Plants in the genus Hydnora are entirely subterranean, lack roots, leaves, and chlorophyll, and rely entirely on its host plant for its water and carbon needs. In a brief history lesson, Bolin talked about how Swedish botanist Carl Thunberg in 1775 first described Hydnora as a fungus. One year after the original description, Erik Acharius, Linneaus' last student and father of lichenology, redescribed Hydnora as a plant in the family Hydnorineae.
Bolin described how the protogynous flowers of Hyndora produce heat and emit the odor of rotting meat as a strategy to attract pollinators. Bolin said that pollinating beetles get imprisoned in the chamber flower structure during the female stage of the flower, and then as soon as pollen is shed, the flower walls turn from smooth to textured allowing the pollen-covered beetles to climb out. The fruit of Hydnora are large, fleshy, and edible. In germination trials, Bolin discovered that Hydnora triceps only germinates in response to the presence of root exudates of its host plant Euphorbia dregeana and not related Euphorbia species.
Bolin’s phylogenetic research of Hydnora shows major clades based on host use: a Euphobia-parasitizing clade and an early-diverging lineage that parasitizes Fabaceae and Commiphora. Over the last 10 years of research, Bolin has simplified the taxonomy, elevated one forgotten species, and described two new species. He spoke about the drivers of speciation including summer versus winter rainfall areas, host specificity and host range, geographic isolation, and clear differences in phenology.
The last presentation on the Symposium’s first day was presented by Posy Busby from Oregon State University who spoke about the “Assembly and function of the leaf microbiome.” Busby began her talk by explaining that all leaves are colonized by microbes, and her focus is on endophytic fungi that live cryptically in leaves. To understand the function of leaf endophytes, Busby described one experiment in which she found that five of seven fungal genera that she tested are capable of modifying disease severity, mostly decreasing, but in one case increasing the severity of the disease. She further examined how fungal communities assemble within leaves and the consequences of the community for ecological function. She described a common garden experiment and a controlled greenhouse experiment using Populus trichocarpa (black cotton) and over 30 different commonly occurring endophytes to address these questions.
Busby’s common garden study tested host genetic effects and environmental effects on mycobiome composition. The study looked at the natural infection process in contrasting environments: one garden was in the cool, wet environment in Corvallis, Oregon, and the other in a hot, dry environment in Boardman, Oregon. She found over 1,000 fungi across the gardens with differences in communities from early to late season and dissimilar communities in the two locations. Busby found interesting genotype by environment interactions and she found that spatial location within gardens was significant suggesting the importance of stochastic variation.
Busby also talked about her greenhouse experiment in which host genotype and the inoculate process can both be controlled. She found that seven of eight fungi species were sensitive to host genotype, confirming this relationship between genotype and community composition, and the fungi were sensitive to integration order, showing the importance of stochastic variation in organisms. She found that integration history is important for disease outcomes, but that this also varies by genotype. She concluded her talk by explaining that improving our understanding of plant-endophyte symbiosis not only improves our understanding of the ecology and evolution of these fascinating relationships, but it could also potentially improve crop health through microbiome management in agriculture.
The first day of the symposium ended with a panel discussion moderated by Susan Pell (U.S. Botanic Garden) with questions from the audience to the three speakers. Questions included: what was the most surprising thing discovered about plant interactions in the systems that the speakers have studied; how have these interactions indirectly impacted other organisms around the systems that they study; what are the evolutionary advantages of parasitism; and how much genetic material is exchanged between organisms that live in close contact?
The second day of the symposium began with opening remarks and a welcome from Eric Schuettpelz and Saharah Moon Chapotin, Executive Director of the USBG. Schuettpelz emphasized that the symposium is a fundamental collaboration between USBG and the Department of Botany at NMNH, and he thanked everyone on staff at these institutions who helped organize the symposium. Chapotin similarly celebrated the partnership between the two institutions. She highlighted the joint effort to advance native orchid conservation, the collection and preservation of material from endangered plants, and the preservation of wild plant relatives. She invited those viewing the online symposium to partner with USBG, emphasizing the Garden’s living collections of 50,000 plants, including over 500 accessions of plants considered vulnerable and key collections of U.S. native plants, carnivorous plants, economic plants, and aroids.
The first speaker on the second day of the symposium was Leonora Bittleston from Boise State University who spoke about, "Convergent interactions in carnivorous pitcher plant microcosms." Bittleston defined convergent interactions as the independent emergence of multispecies interactions with similar physiological or ecological functions. The focus of Bittleston’s research is to understand if convergent interactions occur in pitcher plant communities. Carnivory evolved multiple times across plants and Bittleston described three independent evolutionary events of true pitcher plants across different orders: Nepenthaceae in Southeast Asia, Cephalotaceae in Western Australia, and Sarraceniaceae in the Americas. Do these convergent hosts lead to convergent interactions with their associated communities?
Using metabarcoding of the bacteria and the eukaryotes and shotgun metagenomes, Bittleston found that similar organisms colonized both the Nepenthes and Sarracenia pitchers, even though they are found on opposite sides of the world. Pitcher plants are rich in degradation enzymes and likely have similar functional roles in the ecosystems in the pitchers. Bittleston conducted a common garden experiment with Sarracenia and Nepenthes pitchers growing together in the same habitat and found that their pitchers are colonized by very similar communities. For instance, Nepenthes hosts were effective alternative hosts for the pitcher plant mosquito, Wyeomyia smithii, which is normally only found in S. purpurea pitchers.
Bittleston wrapped up her presentation by briefly highlighting some of her continuing work. This research includes the effects of history on bacterial community assembly and function, community dynamics over evolutionary time scales, and how a functional trait-based approach can help us understand microbiomes across space and time.
Dong Wang of the University of Massachusetts Amherst spoke next about, “Indentured servitude: host control of intracellular bacteria in the nitrogen-fixing symbiosis". Plants engage microbes from the soil to help absorb minerals, ions, and water. One of the most important and often limiting elements required by plants is nitrogen, and plants and bacteria have a symbiosis in root nodules where bacteria fix nitrogen for the host plant. Wang described in detail the cell biology of nitrogen-fixation in legume plants.
Wang compared arbuscular mycorrhizal symbiosis (which emerged more than 450 million years ago) to rhizobial symbiosis (which emerged between 50 and 100 million years ago). He asked which functions between the two processes are conserved and which ones are novel. The plant’s initial recognition of the microbes is very similar whether it be bacteria or fungus. He explains that the arbuscules and the infection threads are homologous conduits for the microbes. The difference in the nitrogen-fixing process is that a dedicated symbiotic organ called a nodule is produced on the root. Legumes repurposed root developmental genes to construct the nodule.
Wang described why bacterial symbiosis requires a specialized organelle whereas fungal symbiosis does not. Wang explained that legumes developed a mechanism to internalize the bacteria which he described with fine detail. He then explained how legumes reuse directed protein secretion to control the fate of the intracellular bacteria. Wang summarized by saying that the bacteria are domesticated by the host in that the host cell goes to an environment, captures a wild bacterium, put it insides the cytoplasm, then raises it and uses it for its own advantage.
The final presentation of the two-day Symposium was given by Manuela Dal Forno from the Fort Worth Botanic Garden and Botanical Research Institute of Texas. She spoke about, "The lichen dilemma: unveiling diversity in multi-species symbioses." Dal Forno explained that the original concept of lichens has changed from being a dual organism of mycobiont (the fungal partner) and photobiont (the photosynthesizing partner) to a diverse community of microorganisms including bacteria. To evaluate who are truly the symbiotic partners in a complex symbiotic system, Dal Forno presented results of a study examining the subtribe Dictyonemateae, a group of basidolichens.
Dal Forno explained that this lichen group was for a long time thought to be composed of a single genus and five species. Many different forms with distinct ecological preferences historically were identified to just one name. To see the true diversity of this group, Dal Forno collected field samples and utilized herbarium specimens to gather ecological, taxonomical, and genetic information. Unsurprising to her, she uncovered an enormous amount of hidden biodiversity. For instance, based on phylogeny, ecology, anatomy, and morphology data, she found that one genus was actually five: Two filamentous genera (Cyphellostereum, Dictyonema), two foliose genera (Corella, Cora) and a microsquamulose genus (Acantholichen). Further, what was once just five or so species is now over 300 species. A high level of endemism has also been found from previously believed large geographical distributions.
The photobiont in this group is Rhizonema, a cyanobacteria. Dal Forno found three putative species: two monophyletic species (R. neotropicum, R. andinum) and a species complex with many haplotypes (R. interruptum). Looking at how these photobiont lineages are distributed across the different lichens in Dictyonemateae, Dal Forno found that many genera of lichens share the same optimal photobiont. Switching to bacterial communities of these same lichens, she discussed that there is a phylogenetic correlation with the diversity and structure of these microbial communities in addition to ecological preferences and growth types. Future research of hers will examine the roles that each symbiont plays in the functionality, stability, and survival of the lichens.
Just as the first day of the symposium, the second day ended with a panel discussion moderated again by Pell with questions from the audience to the three speakers. Some specific questions included: how do pitcher plants change when growing in nutrient-rich soils; how often has nitrogen-fixation evolved; and what adaptations allow lichens to grow in extreme environments? More general questions included: where do you think we are on the discovery curve of these symbiotic dynamics and where do you see your field heading; are there any common characteristics of obligate organisms where perhaps they have lost something in their genomes; and, for the non-obligate participants, what is the impact of being in a mutualistic or symbiotic relationship that changes their function rather than growing on their own?
Over the two-day period, over 220 people attended the symposium. Those who viewed the proceedings watched from 22 countries. All speaker presentations, opening remarks, the presentation of the José Cuatrecasas Medal, and the roundtable panel discussions were recorded and are available for viewing at NMNH’s Natural History for Scientists YouTube page.
The 19th Smithsonian Botanical Symposium is scheduled to take place at the National Museum of Natural History and the U.S. Botanic Garden on Friday, May 13, 2022. The topic is still to be determined. Check the Department of Botany’s website for updates.
Video playlist of the 18th Smithsonian Botanical Symposium:
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