From Plant Press, Vol. 22, No. 3, July 2019.
By Gary A. Krupnick
Smithsonian’s Department of Botany and the United States Botanic Garden convened the 2019 Smithsonian Botanical Symposium, “What Darwin Couldn't Know: Modern Perspectives on Crop Plant Origins,” at the National Museum of Natural History (NMNH) in Washington, D.C., on May 17, 2019. The unusual title for the symposium is acquired from the writings of Charles Darwin. In his 1868 book, The Variation of Animals and Plants under Domestication, Darwin’s dim view of progress in understanding domestication in the vegetable kingdom is evident when he wrote, “Botanists have generally neglected cultivated varieties, as beneath their notice.”
In today’s age, there is a resurgence of research focused on the plants most essential to human life. With seven engaging speakers, the 17th Smithsonian Botanical Symposium highlighted contemporary research into the domestication of crops and their wild relatives as well as ornamental plants. Invited speakers included archaeobotanists, botanists, geneticists, and paleoethnobotanists utilizing molecular and genomic tools unknown to Darwin.
Kirk Johnson, the Sant Director of NMNH, and Eric Schuettpelz, the Acting Chair of Botany at NMNH, both provided opening remarks and welcomed the audience to the Smithsonian Institution. Kenneth Wurdack, Department of Botany at NMNH, presented the annual José Cuatrecasas Medal for Excellence in Tropical Botany to Sandra D. Knapp from the Natural History Museum in London. Unfortunately, Knapp was unable to attend in person. Ian Owens, Deputy Director of NMNH, accepted the Cuatrecasas Medal on her behalf. Owens read prepared remarks written by Knapp in which she shared that Cuatrecasas was one of her botanical heroes. She noted, “His influence and inspiration reach far, and will for generations to come.” While she was sorry to have missed the ceremony, she requested that we live tweet the event (#SBS19).
Allison Miller from Saint Louis University and the Donald Danforth Plant Science Center delivered the opening keynote talk, “What Darwin couldn’t know: Modern perspectives on crop plant origins and why it matters for the future of food.” She spoke about Darwin’s written observations on variation in domesticated systems, using pigeons as an example. While Darwin wrote extensively about animals (dogs, cats, horses, pigs, and others), his writings about crop plants (cereals and fruit trees) were more limited. Miller reviewed Darwin’s contributions in understanding crop origins including steps in cultivation, geographic origins of crop plants, variation among cultivated varieties, and rapid evolutionary change in response to artificial selection.
Miller continued her talk by describing how traits among domesticated grapevine species (Vitis) vary under common conditions. She explained that when a scion is grafted to a rootstock, the rootstock system affects which genes are turned on. Thus, the rootstock influences the shoot system phenotypes. The future of food, the development of new crops, and food security were among other topics that Miller discussed. She argued that understanding crop plant origins is important for the conservation of crop genetic resources, improvement of contemporary crops, and the development of new crops to meet the needs of a growing population in a changing climate.
Natalie Mueller from Cornell University spoke about the past domestication of plants in her talk, “Lost crops and ancient landraces: Deep histories of communities and their crops.” She uses long history to understand how social and environmental circumstances both foster and reduce agrobiodiversity. Her research focuses on 2,500 years of cultivation of erect knotweed (Polygonum erectum). Her work has uncovered evidence of at least two domestication events, the existence of distinct landraces, and the preliminary evidence of feralization of erect knotweed. She explains that for extant crops, it is possible to work backwards from known landraces to the archaeological record. With lost crops that are no longer present, it is necessary to explore variability through experimentation.
Mueller then went into detail on a project of hers exploring five lost crops: sumpweed, goosefoot, erect knotweed, little barley, and maygrass. She documented and collected seeds from populations of eastern North American crop progenitors. By doing so, she was able to document variability. Because the crops she studied are no longer in cultivation, she reconstructed best practices for cultivating the lost crops. She explored the role of developmental plasticity in plant domestication by conducting both fieldwork and greenhouse experimentation. By exposing progenitors to different kinds of growth conditions, she was able to effect plant architecture, yield, and seed and fruit morphology. She hypothesizes that unlike other wild plants, crop progenitors are usually plastic, and that ancient people chose to cultivate the select plants because they responded rapidly in beneficial ways.
For the last talk of the morning session, Nyree Zerega from the Chicago Botanic Garden and Northwestern University presented, “Seeing the forest for the fruits: Cultivation, domestication, and wild fruit trees in Southeast Asia.” She began her talk by discussing a five-step biological process of domestication – wild, wild harvested, cultivated, semidomesticated, and domesticated. The domestication syndrome involves the selection of traits that are suited to the human rather than the wild environment. Forest tree crops, however, may not fit in this syndrome. Zerega asks if forest tree crops are a result of domestication or intensification. One challenge in domesticating fruit trees in a forest is that humans are not the only animal acting on selection. For example, elephants act on seed germination of jackfruits in Southeast Asia. Another challenge is that many fruit trees are clonally propagated instead of grown from seed since many tropical trees have recalcitrant seeds.
Zerega described in detail the domestication of four Southeast Asian tree species in the genus Artocarpus (Moraceae). Tarap (A. odoratissmus) has two genetically distinct forms – a wild form with hairy buds and a domesticated form with smooth buds. The local people of Sarawak, Indonesia, recognize these forms. In cempedak (A. integer) the putative wild progenitor has been identified, and molecular analysis shows distinct cultivars that have different colors, tastes, and sizes. Jackfruit (A. hetrophyllus) has a long history of human use going back 6,000 years. While the wild relative has not been identified yet, there is a high level of diversity in morphology. Jackfruit is harvested from forests, cultivated and managed in agroforests and homegardens, and grown in commercial orchards. Finally, Zerega shared a Hawaiian origin story for breadfruit (A. altilis), a species which has lost the ability to survive in the wild. Zerega concluded her talk by stressing that rather than focusing on improved control and increased production of individual species, tropical forest culture aims at the domesticating production processes of an entire ecosystem, encouraging diversity, and representing an alternative model of forest domestication.
The afternoon session began with John Burke from the University of Georgia presenting his talk, “Genetics and the evolution of crop plants: Insights from sunflower (and related species).” Using Helianthus annuus as a model system, Burke described how a domestication gradient exists, where high levels of genetic diversity is present in the wild progenitor but that diversity drops as landraces and then modern cultivars evolve. He then asked which traits drove the evolution of the domesticated sunflower. Selection on larger seed sizes was highly influential, but surprisingly some directional selection effects were often in unexpected directions. Burke explained that it was possible that selection on oil-related traits may have led to these surprising findings.
Burke then focused on the timing of selection. He examined if seed size was a selecting trait early in the process of domestication, and oil traits were selected later in the process. By crossing wild sunflower with a primitive landrace, he discovered that past breeding efforts may have had unintended consequences. He explained that a post-domestication selection process for high oil content led to maladaptive alleles being introduced into the modern sunflower gene pool.
Briana Gross from the University of Minnesota Duluth next spoke on, “Domesticated apple in a global and local context.” Apple (Malus x domestica) is a global temperate perennial crop with its wild progenitor from western China. Gross explained that perennials show much more mild genetic bottlenecks – while annuals retain an average of 60 percent of their genetic diversity, perennials retain an average of 91 percent. Using collections from USDA-ARS’ Plant Genetic Resources Unit in Geneva, New York, she sampled the genotypes from 45 countries of domesticate apple, and compared the genotypes to the main progenitor M. sieversii, and two species that may have contributed to the crop, M. orientalis and M. sylvestris. Gross found M. x domestica has retained 95 percent of the variation present in M. sieversii. Thus, domesticated apple has maintained its diversity for over thousands of years. She did not find an improvement bottleneck either—modern domesticated apple has as much variation today as was present in the 1600s.
Gross spoke about diversity in the local landscape. Domesticated apple has become naturalized in North America, surviving without care for many years. Unidentified apple trees are common on the landscape. She spoke about a project in northeastern Minnesota, examining microsatellite markers to identify unknown local trees. She was able to genetically match 76 unknown trees to 20 named cultivars, of which eight were developed by the University of Minnesota apple-breeding program in the late 1800s and early 1900s. Six other cultivars were Russian dating back to the 1700s and early 1800s. Gross concluded that local breeding programs have a strong influence on regional genetics.
After an afternoon coffee break, Logan Kistler from NMNH presented his talk, “Unraveling the evolution of domestication in maize with ancient genomes.” He spoke about how corn became a global success, primarily due to genomic plasticity. Kistler examines ancient DNA to understand the order of events into domestication. Maize evolved from teosinte, an inedible plant. Origins of domestication date back approximately 9,000 years ago in the Balsas River valley in Mexico where starch grains and phytolith evidence has been found. Maize then arrived in Central America about 7,500 years ago and spread into South America around 6,500 years ago. Kistler, however, has discovered evidence that shows the domestication process was still happening in Mexico after it spread.
Examining 40 maize landraces, 9 archaeogenomes, and 70 published datasets, Kistler uncovered a stratified domestication process, where semi-domesticated maize led to semi-domesticated sub-groups leading to the diverse landraces we see today. In other words, the diversity of modern maize is the result of multiple waves of human-mediated dispersal. Thus, maize domestication was not complete before people started moving maize around. Some lineages failed while others were successful.
To close out the presentations, Dolores Piperno from NMNH delivered the closing keynote talk, “Current perspectives on agricultural origins in the lowland Neotropics.” Archaeological evidence shows that the earliest sites of farming are often in caves and rock shelters, where grinding stones, Cucurbita phytoliths, popped teosinte grains, Phaseolus beans, chili pepper seeds, and avocado stems have been found. Piperno spoke about the importance of phenotypic and developmental plasticity, which gives plants the ability to adjust their phenotypes in response to environmental variability and change.
Piperno explained that CO2, temperature, and precipitation levels were quite different in agricultural societies 12,000 years ago. She spoke about a greenhouse experiment where she grew teosinte in CO2 and temperature conditions that resembled late-glacial and Early Holocene environments. Teosinte grown in growth chambers resembling modern conditions resulted in plants having the architecture and inflorescences we see today; but those that grew in the late-glacial and the Early Holocene growth chambers resulted in plants with an appearance that was more maize-like. She explained that gene expression might be the key that gives rise to phenotypic change. Piperno thus argues that foragers and early cultivators worked with teosinte phenotypes and gene expression levels considerably different—and already with some maize-like traits—than the modern teosinte presently used as the morphological and genetic baseline for the domestication process. In other words, we cannot assume ancestral plants were similar in morphology to today’s plants. Piperno plans to follow up this research by looking at other traits such as fruit bitterness in squashes and pod twisting in lima beans.
The Symposium’s evening events at the U.S. Botanic Garden’s Conservatory included a closing reception and a poster session. Poster topics ranged from the domestication of edible hibiscus, mushrooms, and Agave, to the conservation of crop wild relatives both in the wild and maintained in botanic gardens.
Left: Leslie Overstreet highlights special notations in a botanical book on commercially important plants on display at the Cullman Rare Book Library. (photo by Allie Alvis)
Right: American Botanist and Family Physician by John Monroe, 1824. (photo by Rose Gulledge)
An optional field trip allowed attendees the opportunity to partake in three behind-the-scenes tours of the Joseph F. Cullman 3rd Library of Natural History, an event hosted by Smithsonian Libraries. The library located at NMNH had on display a wide selection of stunning books highlighting Darwin’s publications, medical botany, Native American plant use, and more. Leslie Overstreet, Curator of Natural History Rare Books, spoke about the collection of James Smithson’s books housed in a temperature and humidity controlled vault within the library. Other books presented included John Hill’s The British Herbal (1756) and William Jowit Titford’s Sketches Towards a Hortus Botanicus Americanus (1811).
The 18th Smithsonian Botanical Symposium is scheduled to take place at the National Museum of Natural History and the U.S. Botanic Garden on Friday, May 15, 2020. The topic is still to be determined. Check the Department of Botany’s website for updates.
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