NC7: Conservation, Management, Enhancement and Utilization of Plant Genetic Resources
(Multistate Research Project)
NC7: Conservation, Management, Enhancement and Utilization of Plant Genetic Resources
Duration: 10/01/2022 to 09/30/2027
Statement of Issues and Justification
Need, as indicated by stakeholders
Available, diverse germplasm is crucial to our ability to continually refine cultivars, inputs, production systems, markets, end-use processes, and scientific discoveries to respond to production challenges and to support changing societal needs for food, feed, fiber, bioenergy, manufacturing (e.g., medicines, biologicals, construction, etc.), and aesthetic uses. The conservation, management, and well-targeted utilization of plant genetic resources, also known as germplasm, enable harnessing genetic diversity to create and sustain agricultural production systems, necessary for economic security, health, and nutrition.
Germplasm, both the genetic material (genes, groups of genes, chromosomes) that controls heredity and the tissues, organs and organisms that express the variation contained in that genetic material, provides the essential building blocks to ensure future improvements in production and quality, and for innovations in crop development and utilization. Genetic resources in combination with water, air, soil, minerals, and crop management practices, together with cultural and market forces define the agricultural production systems that sustain humanity. These resources comprise the essence of our environment and consequently, our quality of life by providing crucial ecological services and valued aesthetic qualities.
Plant genetic resources acquired throughout the world and conserved at the North Central Regional Plant Introduction Station (NCRPIS) in Ames, IA serve a crucial role in supporting and sustaining humanity. This project is part of the National Plant Germplasm System (NPGS) and its mission is the to conservation, characterization, evaluation, and distribution of germplasm and associated information to researchers, educators, and commercial producers. It addresses multiple priorities, including global food security, value-added genes in conventional breeding and molecular biology, new plant species for agricultural production, nutritional quality of plant and food products, and natural resource and ecosystem quality.
The Maize Crop Germplasm Committee, a stakeholder advisory group, noted in their 2016 update to the maize crop vulnerability statement that “Maize … is the most important crop in the United States and one of the top three cereals in world calorie production. The United States is the world’s leading exporter of maize. Because of the importance of the crop to the United States’ economy and the world food supply, it is essential that maize germplasm be protected, maintained, and enhanced.” Similar stakeholder input on other NCRPIS crops provides strong evidence of the need for this project.
Importance of work and extent of problem
As the major grain production area in the world, the vitality of the agricultural system of the USA and the North Central Region (NCR) in particular, is crucial to global food security due to production of corn, soy, and other non-native crop species. Nutritional quality is fundamental to food security, health, and well-being.
Historically, few of the region’s many crops were indigenous to the U.S. Diverse genetic sources of crops and their wild relatives are now seldom available from their source locations. Areas within the NCR utilize extensive plant diversity to different degrees in their agricultural production, yet abiotic, biotic, and market pressures threaten profitability and therefore the sustainability of existing crop production. New species must also be evaluated for their potential and appropriate risk assessments conducted to help guide their introduction into new geographic areas.
Increased diversification of crops that can be integrated into existing sustainable production systems without compromising acres devoted to food use, and that can extend the period of capture of solar energy are high priorities. Integrated cropping strategies that maximize use of targeted genetic resources will contribute to improved soil and water quality; successful innovations will enhance the economic viability of producers, provide new market alternatives, and will support national rural development and environmental quality objectives.
Expanded use of crops for ethanol, biodiesel, or ‘drop in’ fuels is considered fundamental to U.S. energy production security. Prior to the use of petroleum for energy production, society depended much more intimately on plant products for fuel and industrial feedstocks. Society is looking once again to agricultural-production solutions for its energy and industrial raw-material needs, and research and development related to potential utilization of alternative plant species for energy production and biomaterials for food, fuel, fiber, medicinal or nutraceutical, and biobased products are all increasing in priority. Demand for the oilseeds collections for biofuel and industrial product applications as well as for food production has dramatically increased. Developing an understanding of selectable traits and the underlying genetic variation that can contribute to these objectives is challenging.
Evolving production threats include climate change, expanded ranges of damaging pests and pathogens, degradation of soils, loss of arable land due to development and other factors, and natural and civil disasters. As climate extreme events increase, with unusual heat, drought, excessive rainfall, and wind events, damage to local biosystems as well as crop production, genetic sources that can contribute adaptation traits are in high demand. These preceding factors increase the need for expanded access to plant genetic resources that can contribute useful genes and traits. Without such resources to address production and ecosystem issues, the world becomes a hungrier, more desperate, and dangerous place. These needs are reflected in annual increased demand for genebank germplasm resources over the past two decades.
Characterization of our existing germplasm is an ongoing, critical need. Quality characterization information greatly facilitates use of the germplasm system’s resources. New molecular techniques and genome research efforts can greatly enhance the value of characterization information, in combination with traditional and high throughput screening methods. Coupled with advances in high throughput phenotyping technologies, capabilities to manage, assess and interpret massive quantities of data in conjunction with biochemical and other biological processes, scientists can better elucidate germplasms’ inherent properties, thus increasing the potential for germplasm resources to address production challenges.
Because water is a limiting factor for production in many areas of the globe as well as in the U.S., development of drought-tolerant varieties is an important objective. Climate change has resulted in increased variability in both rainfall and temperature; research on increased tolerance to both extreme heat and cold conditions during sensitive growth stages is crucial to identify phenotypes and associated genetic mechanisms to deal with these challenges. Nutritional needs also drive demand for plant genetic resources, especially for the vegetable collections. Crop production on marginally productive lands threatens ecosystem and production system sustainability, and positive impacts on rural development are needed. Understanding how to manage and produce new crops is a complex task, and important to minimize economic and environmental risks and maximize benefits to producers, end-users, and consumers. The Department of Energy actively engages NCR and researchers in plant breeding and genetics, biochemistry, germplasm curation, agronomy, and various technologies to understand the energy potential of new and established crops.
Technical feasibility and value of research
Diverse germplasm collections are developed and maintained at the NCRPIS in excellent cold storage facilities by experienced personnel capable of conducting the mission of acquitting, conserving, evaluating, documenting, and distributing genetic resources of agronomic and horticultural crops of interest of the North Central U.S. Well-developed building and land infrastructure is available. The NCRPIS has been partially funded by Regional (now Multi-State) Project NC-007 and by the USDA-ARS. Iowa State University serves as its host institution and provides excellent in-kind and administrative support. The NCRPIS was the first Regional Plant Introduction Station in the U.S., and it has served as a major component of the network of 20 NPGS sites for the last 74 years. The NCRPIS maintains and provides plant genetic resources, associated information, and a wide variety of technical and leadership services devoted to substantially improving agricultural technology in the U.S. and abroad. In 2003, it was designated by the USDA-ARS as a mission-critical site. Its staff led the collaboration to replace the legacy Germplasm Resource Information Network (GRIN) with the GRIN-Global System, designed to support any genebank’s information management needs.
Advantages of the multistate effort
Through use of the products of plant genome sequencing efforts, statistical and bioinformatics tools, development of biochemical pathways, researchers are integrating phenotypic, genomic, and metabolic information to expand the understanding of gene function and expression in ways never before possible. Diverse scientific expertise and partnerships are required to accomplish high priority research objectives. These efforts enable innovative uses of plant genetic resources and new impacts and benefits to society.
Crop collections important to the North Central Region have been supported since 1947 through the partnerships with Multi-State Project NC-007, the USDA-Agricultural Research Service, the State Agricultural Experiment Stations (SAES) of the NCR, and Iowa State University. For 74 years NC-007 has served as a major repository within the NPGS and supported the activities of NCR and global researchers, educators, and producers to improve crop production genetics and technologies. The Multi-State Participants use germplasm and information resources to improve crop genetics and production technologies and to enhance the health and nutrition of society.
Since 1954, the NCRPIS has coordinated a cooperative network involving the NCR’s State Agricultural Experiment Stations, the USDA Natural Resources Conservation Service, and public gardens and arboreta to conduct long-term evaluations of promising new trees and shrubs. This network collects and summarizes performance data that shed light on plant-environment interactions and provide practical advice to landscape professionals. The NCR is an especially challenging region for the cultivation of trees and shrubs, with its climatic extremes, grassland soils, and increasing urbanization. Furthermore, new biotic stresses caused by the rise of new pests and diseases, such as Emerald Ash Borer or the Asian Longhorned beetle, present special challenges that can only be addressed by ensuring the ongoing availability of a diverse array of well-adapted landscape plants.
Because of the diversity of environments and needs in the North Central Region, and the diversity of research interests and expertise available, it is only logical and fitting that a multi-disciplinary effort utilizing the talents of all interested researchers be rigorously applied to develop and test potential solutions to these many challenges.
Benefits and impacts of the research
Potential benefits expected include secure, successful germplasm conservation, management, enhancement, and utilization that can be measured in the introduction of viable new crops, improved cultivars and expanded uses for existing crops based on an expanded understanding of their traits and properties, including nutritional, chemical, pharmaceutical, industrial, and aesthetic applications. Genetic characterization and phenotypic evaluation information, coupled with bioinformatics applications, will enable users to select accessions more efficiently for breeding and research, thereby, enhancing our ability to understand and realize the value of plant genetic resources. Impacts will also result from development of a fundamental understanding of the nature and biology of genetic diversity, how it interacts with and is influenced by environment, and the resulting discoveries, inventions and applications which benefit society. The researchers of the NCR and curatorial staff of the NCRPIS will also provide training for the next generation of plant scientists and curators, providing opportunity to sustain societal needs through agricultural innovation.
Related, Current and Previous Work
Note: A list of abbreviations used in this document can be found in Appendix 1.
Conservation and access to PGR collections is essential to global food security. Genetic sources of resistance to biotic and biotic stress and novel traits can be identified and captured from crop wild relatives, landraces, farmer selections, and heirloom varieties, and from elite germplasm for varietal improvement. The NPGS plays a critical role in sustaining the future of plant breeding (Byrne et al., 2018).
Since 1947, the NC-007 Project has enabled state and federal cooperators to participate in coordinated efforts to acquire, maintain, characterize, evaluate, document, and distribute crop plant genetic resources, and to encourage their use in research and crop development for food, feed, energy, industrial, landscape, and medicinal or nutraceutical purposes. Establishment of the Plant Introduction Stations resulted from the recognition of the importance of genetic variability to efforts to ensure food and economic security and to ensure access to PGR collections. Facilitated access and exchange of plant genetic resources is dependent on complex policies and practices. Characterization of germplasm is essential to successful utilization of PGR and to knowledge development.
The North Central Regional Plant Introduction Station is one of 20 seed and clonal germplasm repositories in the NPGS, and a collaborative effort of Iowa State University, the Agricultural Experiment Stations of the 12 NCR States, and the USDA-ARS PIRU. Located near ISU in Ames, the ISU AES serves as the NCRPIS’ host institution, and the Experiment Station Director serves as Administrative Advisor for the NC-007 project.
Related, Current and Previous Work of NC-007 Participants
Our work identifies novel traits that provide host plant resistance of cultivated and wild plants to insect herbivores. We examine mechanisms and consequences of induced resistance following herbivore attack or following exposure to volatile cues from (attacked). Localized induced plant responses increase spatial and temporal host plant variability, a component of defense. We have explored several physical plant traits that provide resistance – sticky surfaces and trichomes, spines, and prickles. Sticky seeds reduce ant and rodent predation while sticky leaves, stems and reproductive organs deter herbivores and facilitate specialist predators of herbivores. Unidirectional hairs of many grasses, including economically important grains, appear to usher insects away from vulnerable basal meristems.
Work focuses on the genus Aronia Medik, known as chokeberry, deciduous shrubs with novel fruit type and biologically health-promoting compounds such as antioxidants. Consumption of berries has increased significantly, and producers and retailers experiment with new varieties and products (Hoke, Campbell and Hau, 2017).
Wild and domesticated Aronia species exhibit a range of ploidy levels; AFLP markers, ploidy analysis and plant phenotype were used to understand their genetic variability and occurrence of apomixis (Mahoney et al., 2019). Intergeneric hybridization between Aronia and Pyrus has been investigated for development of larger, sweeter fruits while maintaining high levels of desirable, biologically active compounds.
We have studied maize genomic resources to determine genetic and epigenetic variability at centromeres, frequency of centromere-proximal genetic recombination, identification of potential centromere-linked domestication genes, and their implications for germplasm collections of other domesticated crop species (Schneider et al., 2016; Presting, 2018).
Juvik has focused on breeding vegetables for improved flavor, insect and disease resistance, and enhanced levels of phytochemicals associated with health promotion. DNA marker-based linkage maps of tomatoes, sweet corn, broccoli, and the bioenergy crop, Miscanthus identified favorable QTLs for marker-assisted introgression of beneficial alleles for improved quality, yield, and other traits into elite germplasm for commercial release. Work focuses on the feasibility of using pigments from corn as natural colorants in processed foods and beverages.
Sacks’ research with Miscanthus, a paleo-allotetraploid, is devoted to determining native species distribution and relationships, and the productive potential of members of this genus. Ploidy levels, phenotypic traits, genetic relationships, and evolution were explored. Kling’s research on shrub willow biomass reveals variation in compositional traits such as lignin among species and interspecific hybrids. Yield is negatively correlated with lignin content and positively with cellulose content (Fabio et al., 2017).
Lübberstedt lab works to understand the basis of spontaneous doubling of the haploid maize genome; use of GWAS and double haploid breeding method with exotic maize revealed a major locus on chromosome five (Verzegnazzi et al., 2021). Collaborative research with a Chinese group using ISU’s IBM mapping population contributed to understanding the genetic architecture underlying salt tolerance (Ma et al., 2021), and quantitative trait loci for tolerance to lead and cadmium soil levels (Hou et al., 2021). Alleles associated with adaptive agronomic traits, such as flowering time and plant height were identified, and predictive models for adaptive agronomic traits and performance of diverse germplasm exhibiting phenotypic plasticity were developed (Li et al., 2021).
Maize centromere research reveals previously unknown variation in gene content, methylation, and structure of major cytological landmarks such as chromosome knobs (Hufford et al., 2021). Community efforts to sequence 26 important, exotic maize founders’ genomes provide an unprecedented resource to better understand gene expression and support development of resilient maize PGR.
The soil microbiome, integral to the crop production system, responds to crop management practices, plant genotype, environmental factors, and impacts / responds to pathogens and pest populations. Fungal endophytes can influence production and post-harvest challenges in carrot. Carrot genotype was found to affect endophyte abundance and the potential for individual soil mycobiota to affect seed germination, seedling growth and tolerance to an important carrot pathogen.
Rice research on the origins of the gibberellin biosynthesis gene, SD1, responsible for the ability of plant internodes to elongate while submerged in flooded conditions, indicate that the deepwater, rice-specific genetic haplotype derived from wild rice and was selected for deepwater cultivation in Bangladesh (Kuroha et al., 2018). The U.S. rice PGR collection was characterized for haplotype diversity at the SD1 locus; seven unique haplotypes were identified and validated, important for breeding efforts (Angira et al., 2019).
Diverse germplasm PGR allow for development of canola, sorghum, soybean, and wheat varieties adaptable to Great Plains environmental extremes. PGR and varieties of new crops such as winter canola (Stamm et al., 2015, 2019, 2021) are made possible through the conservation of and access to NPGS collections. In addition to traditional variety improvement, parental lines are being developed for hybrid winter canola production.
Screening diverse sorghum and wheat collections identified herbicide-tolerant traits. Mechanism and inheritance of herbicide tolerance were investigated in sorghum (Pandian et al., 2020, 2021) and more recently in wheat and will support transfer of herbicide-tolerant traits to agronomically acceptable germplasm.
Current wheat germplasm and interactions with environment and management are evaluated for yield-associated traits. Long-term variety trial data have been scrutinized for agronomic and disease resistance traits (Munaro et al., 2020). Experiments investigated physiological traits for increased yield (de Oliveira Silva et al., 2020), increased grain protein concentration (Lollato et al., 2021), and genetic gain in yield (Maeoka et al., 2020).
Wild relatives of wheat have been used to broaden the gene pool of T. aestivum. Patterns of introgression from Aegilops tauschii were explored (Nyine, et al, 2020; Moses et al., 2020). Wild materials, including Ae. tauschii (Cruppe et al., 2020), Ambylopyrum mutica (Fellers et al., 2020), T. dicoccoides and Ae. ventricosa continue to be evaluated and transferred to adapted backgrounds to address biotic and abiotic stresses and explore the potential for improving wheat quality and nutritional traits.
Grumet leads a multi-institutional project with 20 co-PIs developing genomic tools for watermelon, melon, cucumber, and squashes (Grumet et al., 2020). The Cucurbit Genomics Database (CuGenDB, http://cucurbitgenomics.org) has made all available cucurbit genome sequences, sequence annotation and transcriptome profiles publicly accessible (Zheng et al., 2019). NPGS collections for the six crop species (1000-2000 accessions/crop) were GBS characterized, data available on CuGenDB (Wang et al., 2018, 2021; Wu et al., 2019).
The Cichy, Douche, Edger, Hollender, and McGrath programs are devoted to dry beans, potato, blueberry and strawberry, cherry, apple and peach, and sugar beet breeding and genetics, respectively. Many dry bean seed traits related to genotypic variability, diversity, mapping, genomic regions, and genes influencing cooking time, seed composition, and end use quality are investigated and assessed. The potato breeding and genetics program optimizes conventional breeding for superior varietal selection and development for the Michigan industry. Studies focus on self-compatibility in diploid potato, chip-processing quality, and resistance to Colorado potato beetle, late blight, and scab; all PIs of S. microdontum were screened for late blight resistance. The assembled sugar beet genome was used to examine diversity in a wide range of beet. Late blight resistance screening included 606 publicly available wild (321) and sugar beet (285) accessions, other crop types (table, fodder, and leaf), and crop wild relatives.
The Thompson program studies how maize genotypes grow in different environments. Maize and sorghum diversity and association panels, GEM lines, and the Sorghum Conversion lines are used to find and introgress tar spot resistance in maize, and for quantitative genetics, phenomics, and predictive modeling.
The Soybean Breeding Program accesses wide genetic variation contained in soybean PGR in several ways, including phenotyping diverse PGR for shoot architecture (SA) features and others. Information is used to determine the range in genetic variation for SA properties, which influence canopy structure, and hence light capture and light-use efficiency. We find that soybean presents a continuous distribution in SA, and several combinations of SA features can achieve a high degree of light capture and transmittance. A panel of 400 diverse MGI accessions were phenotyped and the data were combined with high-density genotypic data in a GWAS. A strong marker-phenotype association was found between markers on the end of chromosome 19 and canopy coverage and branch angle, suggesting that the well-known chromosome 19 QTL influences canopy coverage through branch angle. A potentially new branch number QTL was found closely linked to Dt2.
Our breeding and genetic work focuses on proso millet, a well-adapted rotational crop for the semiarid central U.S. High Plains. Rich in minerals, fiber, vitamins, proteins, and gluten-free, it has multiple benefits as a human food as well as a bird seed crop. Collaborations among researchers of diverse disciplines is required to develop new varieties and markets (Das et al., 2019; Santra et al., 2019).
Characterization of inter- and intraspecific variation in the ca. 30 wild perennial relatives of soybean (Glycine), representing the tertiary germplasm pool for the cultivated soybean, continued using GBS (Sherman-Broyles et al. 2017), and on the origins of allopolyploidy (Doyle and Sherman-Broyles 2017). Allopolyploidy produces transgressive effects on symbiotic nitrogen fixation (nodulation) in Glycine allopolyploids (Powell and Doyle 2017).
Maize (dent and sweet corn) PGR have been used to identify genes controlling leaf photosynthesis and architecture traits (Gore et al., in preparation), the accumulation of elements in grain (Baseggio et al., 2021; Wu et al., 2021) and to support the study of vegetation indices associated with grain yield (Anche et al., 2020; Morales et al., 2020).
Work focuses on ecological restoration of urban woodlands, understanding the composition and functional differences between urban and non-urban habitats and the forces that shape them. The effects of urban conditions and stressors have on plant recruitment are often species-specific and can facilitate or limit plant establishment. Plant life-history analyses can be adapted to urban environments to aid in plant establishment and develop effective management strategies. This extends to understanding the challenges impacting global coastal landscapes, due to climate change ecologically, and by social activities. Adapting ecological concepts can help maintain biotic and economic processes in threatened coastal communities.
During 2017-2021, adaptation potential for Ethiopian mustard and open-pollinated white sorghum, with ongoing efforts for industrial hemp and perennial flax, were evaluated in North Dakota and west central Minnesota. Initial evaluations focused on identifying PGR with early maturity, good grain yield and quality, and agronomic deficiencies such as low seed/seedling vigor, seed shatter, height extremes and non-uniformity, small seed size, and seed maturity at harvest. Adapted genotypes/varieties were selected for evaluation of stand establishment and harvest management.
Sorghum is planted early due to lack of early maturing varieties for short, cool growing season areas. Yields of early maturity hemp varieties do not decline when planted later in June in eastern North Dakota. Timely hemp harvest is important; delays reduce yields from shattering more so than with sorghum. Hemp chemical and biological seed treatments show promise for reducing pure live seed mortality from 30-50% or more as compared to wheat, corn, and soybean, where mortality is commonly 10-15%. Stand establishment challenges were apparent for perennial flax where soil crusting, soil moisture limitations, and seeding depth occur. Delayed and extended emergence followed by slow growth reduce perennial flax competitiveness with weeds. Advantages of well-established perennial flax include higher grain value, potential for two harvests per season, stand duration potential for up to five years, and an available market.
Corn and soybean relay intercropping systems were evaluated using the winter annual oilseeds camelina and field pennycress; potential for improved net production and economic advantage was largely dependent on grain yield and price. The winter annuals reduced soybean yields in the second year in some locations such as North Dakota where the growing season is short and cool. In addition to the potential economic grain value from harvesting three grain crops in two growing seasons, several ecosystem benefits (early pollinator food source, soil protection, carbon fixation, and wildlife habitat) show enhancement with these types of cropping systems.
The wild ancestors of the cultivated strawberry include approximately 20 species with a wide range of ecological, ploidy, and breeding system diversity. Studies conducted over the past five years contributed to understanding their phylogenetic relationships (Kamneva et al. 2017, Wei et al. 2017, Dillenberger et al. 2018); the diploid ancestry of the cultivated octoploid strawberry (Liston et al. 2020, Liston and Ashman, 2021); evolution of sex chromosomes in the genus (Wei et al. 2017, Tennessen et al., 2018); and ecological genetics of polyploidy (Wei et al. 2019, 2020).
Our work on maize pollen development focuses on understanding mutations that reduce pollen transmission. We identified two genes, stk1 and stk2, that play a redundant role in pollen development. Expression of other maize genome genes can be impacted positively and negatively by stk1 mutations, particularly genes involved in translation (Huang et al., 2017).
Efforts focused on characterization of soybean, sunflower, wheat, wheatgrass, and oat PGR. New sources of resistance to biotic and abiotic stresses were identified for cultivar development. Examples include soybean PGR resistant to root rot (Okello et al., 2020), and sunflower PGR resistant to Phomopsis stem canker (Elverson et al. 2020). GWAS has been used to identify genomic regions associated with Bacterial Leaf Streak, Tan Spot, and Spot Blotch resistance in hard winter wheat (Ramakrishnan et al., 2019; Sidhu et al.., 2019; Ayana et al. 2018).
Texas researchers utilize PGR from crop-wild relatives and develop introgression programs for key traits of agronomic importance. Specifically, weedy forms of sorghum, sunflower, rice, and Italian ryegrass are being utilized at Texas A&M University. Research on the adaptive potential of weedy sorghum (johnsongrass, shattercane) and their hybrids with grain sorghum aid in the development of perennial sorghum germplasm that can be used for grain, biomass, and bioenergy production. Understanding hybridization potential between sorghum and its weedy relatives helps develop appropriate strategies for gene flow mitigation. PGR for weedy rice, sunflower, and ryegrass will aid in developing cultivars with improved adaptation to abiotic and biotic stresses. Herbicide resistance is an important agronomic trait being explored using these germplasm resources.
More than 25 Texas plant breeders develop improved cultivars with several species from the NCRPIS, across a broad spectrum of the collection, enabling us to educate producers, students, and colleagues on the value of the PGR collection through courses, extension meetings and research outreach, with more than 1,500 contact hours on such activities this year.
Sweet corn is an important vegetable used in both U.S. fresh market and processing industries. The shrunken2, or sh2 allele, is present in 75% of sweet corn germplasm used by the processing industry and nearly 100% of the fresh market industry. Use of a high-quality reference-genome assembly of sweet corn inbred line Ia453-sh2 provided evidence for evolutionary relationships between sweet and other types of maize, identified genome regions under selection, and candidate genes associated with sweet corn traits (Hu et al., 2021). GWAS studies were devoted to kernel carotenoids (Bassegio et al., 2020), and identification of a gene for resistance to maize common rust, a widespread, important disease that impacts sweet corn yields and quality (Olukolu et al., 2016). Roughly 50% of the inbreds in the GWAS panel were sourced from the maize collection housed at NC-7 in Ames. Numerous lines sourced from the NC-7 collection are being used in a breeding program to improve earworm (Helicoverpa zea) resistance in sweet corn for organic growers (Moore and Tracy, 2018, 2020).
A de novo genome assembly of an ‘Oh43-type’ inbred maize line, a different lineage, enabled differentiation of transcripts based on previous reference genome assemblies. GWAS results for SCMV resistance detected the physical location of a known resistance gene, demonstrating the value of comparative genome resources (Gage et al., 2019.)
Automated image-based phenotyping was successfully developed for maize ear, cob, and kernel attributes (Miller et al., 2017), and for maize tassels (Gage et al., 2017). Custom algorithms and their source code are publicly available.
Cooperate and participate as a key element in the NPGS, a coordinated national acquisition and management program of plant germplasm valued for agricultural, horticultural, environmental, medicinal, and industrial uses in the NCR and throughout the U.S. and the world.
Collect and maintain plant genetic resources of dedicated crops and their crop wild relatives, evaluate, and enhance this germplasm.
Characterize and evaluate plant germplasm using a combination of traditional, phenomic, and molecular techniques and utilize modern plant genetic techniques to help manage plant germplasm.
Conduct research, and develop an institutional infrastructure needed to attain the preceding objectives efficiently and effectively, including seed and plant health testing, viability monitoring, pollinator efficacy, and advancements in software applications development and computerized management systems to improve functionality and efficiency, to store and transfer knowledge, and to enhance our understanding of the interrelationships of germplasm with changing abiotic and biotic environments.
Within the NCR, throughout the U.S., and internationally, encourage the use of a broad diversity of germplasm to reduce crop genetic vulnerability. Provide viable plant genetic resources, information and expertise that foster cultivar improvement of established crops, the development of new crops, and new uses for existing crops, thus contributing to a sustainable, biobased economy.
Educate students, scientists, and the general public regarding plant germplasm issues.
Crop production has many challenges, but climate change is a primary threat as it impacts adaptation of crops, their pollinators, pests, pathogens, and productive capacity globally (Giannini et al., 2017). Studies show that while some geographic areas show no significant interference due to climate variability, in substantial food production areas more than 60% of yield variability can be explained by climate variability (Karki et al., 2020), to which 32-29% of global maize, rice, wheat and soybean annual production variability is attributed. Climate variation explains a third of global crop yield variability (Ray et al., 2015). An analysis of global crop production data from 1974-2013 for ten major crops indicates decreased consumable food calories for rice, maize, and wheat (Ray et al., 2019). In the U.S. Great Plains alone, one quarter of the variability in maize, sorghum and soybean yields from 1968-2013 is explained by climate variability (Kukal and Irmak, 2018). Climate variability impacts spatial differences in crop production in countries, which in turn may impact conflict in agriculturally dependent countries (Vesco et al., 2021). Farmers’ perceptions on the impacts of climate change and variability on crop production are changing. In developing countries citizen science is being encouraged to use independent on-farm observations to contribute variety evaluation data (van Etten et al., 2019).
The NCR and other NC-007 participants directly benefit from use of the NPGS germplasm collections to accomplish research objectives, and active collaborations with the NCRPIS staff. Genebank and Multi-State Project participants’ efforts are complementary, resulting in unique advancements in PGR utilization, providing solutions for agricultural challenges, and increased understanding of biological and genetic diversity. Annual reports of the NCRPIS activities and NC-007 collaboration are available through the NIMMS and NCRPIS homepage (https://www.nimss.org/) and (https://www.ars.usda.gov/midwest-area/ames/plant-introduction-research/), respectively.
Working in multi-disciplinary teams, the Program Manager, Plant Pathologist, Entomologist, Agronomist, and IT Specialist provide support and technical expertise for the five curatorial teams. Shown in Appendix Figure 1, crops curated at NCRPIS are organized by proportion of holdings and color-coded by curatorial team lead (curator). These include, from largest to smallest scale of holdings, (1) maize, (2) oilseeds, (3) amaranth, grasses, legumes, etc., (4) melon, carrot, cucumbers, etc., and (5) woody landscape plants, medicinals, and ornamentals. Shared activities and services include: viability testing; controlled pollinations and insect efficacy and management; detection, quantification and elimination of seed-borne pathogens and pests; digital imaging standards and automation; georeferencing; enhancement of the internal and external (public) aspects of the GRIN (GG) System; development of software applications to improve quality and efficiency of data capture and genebank workflows; and operational and equipment innovations contributing to the quality of the germplasm and associated information.
NCRPIS curators and collaborators participate with researchers in the NCR and beyond to address crop development and improvement goals, the impact of climate change on crop adaptation, conduct invasive-species risk assessments, pursue genetic enhancement and trait discovery, address phytosanitary health issues, investigate pollinator-biology questions, and many additional objectives. The activities of researchers who utilize PGR contribute genetic and phenotypic characterization information, new crops and varieties with improved performance for yield, pest or abiotic stress resistance, enhancement to human or animal health and nutrition, aesthetic value, biofuel, and industrial use, providing value to consumers, producers, and end users.
NC-007 personnel collaborate with NLGRP researchers in Ft. Collins, CO to develop strategies and technologies critical to the storage and maintenance of PGR collections. This NPGS site, utilized for long-term seed storage, stores safety duplicates of the PGR collections, and conducts research related to germplasm viability and preservation of genetic profiles. Safety duplication samples are generally held at -18°C or under liquid nitrogen (LN, vapor phase). At the NCRPIS, original seed samples are stored at -18°C, separate from distribution samples (active collection) which are held at 4°C and 28% relative humidity. Periodic viability testing ensures seed quality, and signals when an accession needs to be regenerated, or seed increased. Many species, especially crop wild relatives, lack standardized viability testing or germination protocols. A certified seed analyst provides support for research efforts to develop methods to break dormancy and optimize conditions that promote germination.
Curators address questions and unknowns in taxonomy through external collaborations and by utilizing genetic and genomic technologies and morphological traits to resolve concerns. Accurate taxonomic identification is fundamental to the relevance of PGR for specific research applications. A taxonomic research collaboration of the NCRPIS vegetable curator and the USDA-ARS in Madison, WI is designed to resolve the taxonomy of Daucus and allied Apiaceae species. Umbelliferae taxonomy presents unique challenges; crops of this family are important for food and culinary use.
The NC-007 Ornamental Trials are the longest running ornamental evaluation trials in the US, entering their 68th year in 2022. Focused on evaluating woody ornamental introductions for their adaptation to the NCR, aesthetic and productive qualities, NCR trial cooperators have identified important sources of ornamental germplasm for the horticultural industry (Widrlechner, 2004). Eight NCR states have CRIS projects connected to these trials. Because of the successes that PGR introductions have brought to the horticultural industry in the U.S., a genebank for herbaceous ornamentals, the Ornamental Plant Germplasm Center (OPGC) was established at The Ohio State University (Tay et al, 2004). NCRPIS personnel work closely with the OPGC to transfer germplasm, technology, training, and PGR management methodology.
Controlled pollination programs are used to maintain the genetic profile of accessions during seed increases, utilizing either insect pollinators in screened cages (field and greenhouse) or manual pollination methods. Six different pollinator insects are utilized, including honeybees (Apis mellifera), Mason bees (Osmia spp.), alfalfa leafcutter bees (Megachile rotundata), bumble bees (Bombus impatiens.), and two fly species (Calliphora vomitoria and Musca domestica). Choice of pollinator is determined in part by the insect’s ability to pollinate certain flower types, floral characteristics, pollinator biology and suitability during varying environmental conditions throughout the growing season, and past seed production results. Frequently, combinations of pollinators are more efficacious for seed production and ensuring maximum cross-fertilization of flowers within a cage.
Phenotypic and genotypic characterization and evaluation data greatly increase the research value of the collections, allowing researchers to discriminate between elements of the collection and devote their resources to those most likely to fulfill their objectives. Curatorial staff members exchange information and technological capacities with other NPGS personnel and a wide array of scientific contacts, including NC-007 participants focused on PGR exploration, regeneration, phenotypic evaluation, genomic characterization, and other shared goals. Advances in phenotyping and genomics technologies, coupled with the sequence information from five genomes (foxtail, finger, and proso millets, teff and Japanese barnyard millet) and exploration of available proso millet germplasm diversity support accelerated breeding and development of climate-resilient and nutrient-dense small millets (Vetriventhan et al., 2020). Intraspecific Miscanthus hybrids are being bred by Illinois researchers, based on phenotypic and genetic information, to develop cultivars with tolerance to chilling that can persist multiple seasons, important to success of this bioenergy crop. The short growing season and climate extremes of North Dakota and similar areas have fueled intense agronomic research efforts to adapt and develop new crops (such as hemp), and for new cropping systems in order to diversify crop production and increase profitability.
Genomic characterization is generally accomplished by research collaborators; the resulting information used by curators to better understand and manage their collections. The findings of Romay et al. (2013), following analysis of genotyping of the maize inbred collection continue to provide clarification regarding the diversity of the inbreds, their relationships, seed lots, and potential duplication or misidentification of lines provided by an originator. Some genomic information has been incorporated into the GRIN-Global database. Researchers in Hawaii are developing software to automatically map chromosomal recombination blocks based on repeat sequences, common in pericentromeric regions. Understanding structural diversity is important for the continued improvement of maize (Liu et al., 2020). A graphical user interface (GUI) to better support cataloging, display, discovery, and retrieval of plant molecular genetic datasets from diverse information providers is in development, guided by NPGS curators and programmers.
Genomic characterization of NPG collections has potential to enhance development of new cultivars and varieties. Examples follow: Enhancements to the CuGenDB database (http://cucurbitgenomics.org) will support faster upload of genomes and establish phenotypic databases for several major cucurbit species. Members of the Michigan State team are identifying, genetically characterizing, developing makers, and breeding for resistance for 18 top priority crop-disease combinations identified by the respective Cucurbit industries (Grumet et al., 2020). Genomically-informed core collections are in development for each crop and will be re-sequenced, enabling GWAS for important traits.
Use of genetic information associated with a major locus on maize chromosome five may enable DH line production in exotic populations without use of colchicine or other artificial doubling methods (Verzegnazzi et al., 2021). Research collaborations between institutions with different expertise and testing environments will contribute to development of salt-tolerant maize, and heavy metal tolerant varieties. Efforts to improve seed production in outcrossing grass species focus on identifying candidate genes responsible for self-incompatibility, particularly for perennial ryegrass.
Demand for quality NPGS PGR of known provenance has increased markedly over the past 20 years. We expect this trend to continue, especially requests from developing nations where increased food need is concentrated. While distributions from the NCRPIS have accounted for 20% of all NPGS distributions over the past five years (15% in the last five-year cycle), NCRPIS holdings make up only 9% of the NPGS total collection, reflecting the importance of these holdings to agricultural research (Appendix Table 3, Appendix Table 4). Within the U.S., demand for germplasm varies according to crop-specific, regionally based efforts; NCR researchers request the highest proportion of NCRPIS germplasm. Distributions to developing countries contribute to utilization in crop breeding programs, and secondary benefits through sharing PGR with other scientists (Smale et al., 2004). The impact of new technologies such as genome editing on the nature and use of PGR collections is growing. As methodologies are developed in conjunction with more complete characterization information, utilization of some germplasm may change, and new PGR will be developed and incorporated in genebank collections, increasing collection value.
The U.S. ratified the International Treaty for Plant Genetic Resources for Food and Agriculture in 2017, to the mutual benefit of the global agricultural community and U.S. agriculture. By joining the Treaty, access to PGR covered by the treaty’s multilateral system for access and benefit-sharing is facilitated. Germplasm exchange provides new genetic diversity to fuel U.S. agricultural research and breeding, supporting farmers and promoting food security.
Acquiring new PGR from both domestic and international sources is increasingly complex and challenging due to national, state, county, institutional and international laws, and phytosanitary concerns and restrictions. The NPGS facilitates the exchange of diverse PGR through both acquisition and distribution activities, as well as discovery of these resources via a public access database, GG. Consequently, the quantity of NPGS samples distributed annually expands steadily, free of charge or restrictions. International NPGS distributions will likely increase as research programs utilizing PGR grow. Additional changes in NPGS holdings may occur as the norms for international exchange of PGR evolve in concert with national and international trends in scientific research, and the evolution of access and benefit-sharing regimes (Bretting, 2007).
Development of collections that represent the genetic diversity of crops and their wild relatives is a primary curatorial responsibility. This requires a high level of scholarly research, logistical planning, a willingness to travel and explore diverse environments, and the ability to adapt to new challenges. Acquisition proposals are funded primarily by the USDA’s Plant Exchange Office, and reflect priorities developed in consultation with Crop Germplasm Committee (CGC) members, international scientific collaborators, stakeholder priorities, and urgency to collect if PGR or access is threatened. Recent analyses of the distribution and conservation status of NC7 crops and their wild relatives by crop curators and allied experts have identified vulnerabilities and helped redefine collection priorities (Grumet et al., 2021; Khoury et al., 2020) Access to genetic resources is threatened due to rare or endangered status, human development or farming activities, climate change, or natural or man-made sources of disaster.
Since 2016, about 3,200 new accessions were acquired by NCRPIS curators. Acquired germplasm was obtained primarily through curator-led explorations, but also by contributions from university partners and USDA-ARS researchers, transfers of PVP varieties to NCRPIS after their intellectual property protection expired, or when responsibility for distribution of CSR material was transferred to a curator.
Each state in the NCR conducts germplasm research in connection with Multi-State Research Project NC-007. A search of the Current Research Information System (CRIS), (https://cris.nifa.usda.gov/) for current projects (as of Nov 2, 2021) involving plant genetic resources (queried for plant genetic resources; plant breeding; plant pathology; genetic diversity; plant adaptation; crop; crop domestication; crop evolution; organic breeding; maize; sweet corn; vegetable; amaranth; Fraxinus; melon; carrot; phenomic; plant genomic) resulted in identification of more than 843 active NCR projects. The foci and applications of these research efforts are highly diverse, reflecting the complexity of needs, environments, challenges, and opportunities addressed.
See Methods Table 1 (Attachments).
Over the past 119 years, the NC-007 collection has obtained germplasm from over 164 countries. Growing from 332 (in 1948) to 54,490 accessions in 2021 it represents 374 genera, with 2,156 species (Appendix Figure 1 and Appendix Table 2). The NPGS collection maintains 601,425 accessions, about 9% of which are held at the NCRPIS (Appendix Table 3).
Measurement of Progress and Results
- A primary output of NC-007 participants will be the advancement of new crops, new varieties and cultivars, and new uses to address breeding needs and production challenges, as well as the conservation of these genetic resources to sustain agricultural productivity, resilience, and food security. Plant germplasm distributions will support the agricultural sustainability and success of U.S. and international researchers and novel research.
- Rapid acceleration of well-targeted germplasm utilization and breeding progress will be supported via use of rapidly advancing technologies in genomics, phenomics, bioinformatics, non-destructive trait information capture, and tools to integrate knowledge.
- Progress in understanding crop adaptation and providing recommendations for production challenges faced by growers will occur through implementation of findings from well-designed agronomic studies.
- Plant explorations and germplasm exchange will continue to address taxonomic gaps and expand the genetic and geographic diversity of crop collections and their wild relatives.
- Seed viability and health will be monitored to safeguard collection quality. Methods and protocols will be developed or adapted as needed.
- Seed regenerations will continue to increase and will focus on offering a diverse array of plant germplasm, while conserving the original genetic profile of the material. Many Crop Germplasm Committees cite availability as a primary limitation to evaluation and characterization efforts (Byrne et al., 2018).
- New software applications will increase the productivity and efficiency of genebank workflows at the NCRPIS and throughout the NPGS, improve the public user GRIN-Global interface experience, and enable interoperability with other information providers. Collaborations with international adopters provide opportunity to develop solutions that extend the utility and life cycle of GRIN-Global.
Outcomes or Projected Impacts
- Germplasm characterization and evaluations will provide new genomic data, new and improved genetic linkage maps, identification of QTL for important agronomic and quality traits useful for future genetic improvement of cultivars using both conventional and modern breeding approaches, further genetic analysis of important traits, map-based cloning of genes and to elucidate evolutionary relationships.
- Development of new markets for non-traditional crops provides values to growers and society. For example, improved fenugreek (Trigonella foenum-graecum L.) cultivars could support their use as a valuable medicinal crop, especially in production areas less suited for commodity crops. Introduction of a waxy proso millet (Panicum miliaceum L.) cultivar with novel end-use characteristics such as waxy starch (amylose-free) may open new opportunities for using proso millet in the food and beverage industry. Due to the impact of climate variability on production, canola cultivars adapted to the U.S. Southern Plains, new crops for northern growing areas, and new cropping systems could increase grower options. Improved disease resistant rootstocks of fruit trees, and improved tolerance to climatic extremes during flowering may reduce production and financial risks to growers. Use of wild relatives in breeding of grain, horticultural, ornamental, and other crops support introduction of valuable genes and traits.
- Training of undergraduate and graduate students, postdoctoral candidates and visiting scientists provides valuable experience with use of plant genetic resources for a wide range of objectives and provides for the next generation of scientific leadership in agricultural and allied sciences. Plant genetic resource use will continue to support a diversity of innovative research spanning agronomic, genetic, molecular biology, plant pathology, entomological, horticultural, ecological, biochemical, industrial, anthropological, medical, and pharmaceutical, animal nutrition, human nutrition and culinary use, and bioenergy disciplines.
- Germplasm use will continue to contribute to the aesthetics and sustainability of the world we live in, and the health, welfare, and security of the world’s population.
Milestones(2023):NCRPIS genebank personnel and NC-007 participants will cooperate as part of a coordinated effort between NPGS, university, and private sectors to utilize and capture valuable traits and genes from plant genetic resources. Coordination efforts will be a key focus each year of the plan (2023-2027).
(2023):With U.S. implementation of the ITPGRFA, access to international plant genetic resources should increase. Valuable native crop wild relatives will continue to be identified, with a strong focus on those located in threatened habitats. Addition of key genetic resources is an ongoing process with all steps in operation each year of the project plan (2023-2027).
(2026):More germplasm will be molecularly characterized, and this information will be used to help manage the collections by 2026. Phenotypic evaluations will provide information for analyses in conjunction with genetic marker and genomic information, which will facilitate identification of useful genes, alleles, and metabolic processes.
(2023):GRIN-Global will be enhanced to better enable loading of images and documentation to the database, and mobile applications developed. The public interface will be improved. Enhancements will be made each year (2023-2027) as a continuous process of improvement.
(2023):The NCRPIS will continue to provide a wide array of genetic resources to investigators. NC-007 participants will develop new crops and new uses, conduct agronomic management research, investigate the nature of biodiversity, and apply new genetic technologies. This ongoing process will continuously cycle each year (2023-2027).
(2023):The NCRPIS will provide learning and work experiences for undergraduate students and research assistance to graduate students and postdoctoral students. The investigators of the NCR will help mentor and train the next generation of agricultural scientists. Numerous opportunities will be available in each year (2023-2027) of the project plan.
Projected ParticipationView Appendix E: Participation
Plant genetic resources and associated information are publicly available worldwide on the GRIN-Global website, https://npgsweb.ars-grin.gov/gringlobal/search.aspx . Information on genetic resources, management procedures, characterizations, evaluations, and distributions will be published by PIRU and NCRPIS scientists and NC-007 participants. Information on the NC-007 project, including members, annual reports, and minutes, will be maintained on the NIMSS website (https://www.nimss.org/) . Presentations by NC-007 participants and NCRPIS/PIRU scientists on germplasm-associated research outcomes will be made at regional and national meetings. NC-007 staff will engage with local and regional groups such as garden clubs, master gardeners, commodity groups, nursery personnel, 4-H and other agricultural education programs, library programs, and other events to publicize the importance of valuable genetic resources. NCRPIS tours will be provided to federal and state legislators, university personnel, domestic and foreign scientists and government officials, germplasm users, producers, teachers and school classes, environmental groups, and other interested parties.
The NC-007 Regional Technical Advisory Committee (RTAC) and CGC members will publicize crop-specific germplasm resources within their institutions and companies, sharing research outcomes and impacts. RTAC members will devise effective, proactive ways to publicize the collections and their importance, and will seek to communicate the critical nature of this work to the public. The Germplasm Enhancement of Maize (GEM) project, also part of the Ames PIRU, holds annual field days and tours of the NCRPIS and genetic resource collections are provided. As NC-7 participants discuss their institution’s research and its impacts in their own field day and meeting events, they reach a wide segment of the public.
The NC-007 Regional Technical Advisory (RTAC) committee is comprised of representatives from each of the twelve AES’ of the NCR, and ex-officio members from USDA-ARS. The RTAC has a chair, secretary, and past chair. The secretary is elected to a one-year term and becomes the chair the following year. Each year the project reports results, assesses progress, and receives guidance from the RTAC and Administrative Advisor during the annual NC-007 committee meeting. This meeting is held every third year in Ames at the NCRPIS and rotates among the other locations of the NCR. Sharing of information between scientists at the host locations with the RTAC members is one of the most valuable contributions and enriches the breadth of knowledge of all participants. The perspectives contributed by the NC-007 RTAC members, with their diverse experiences and research interests, are invaluable to developing an understanding of germplasm’s potential and value throughout the NPGS as well as supporting the development of NCRPIS priorities and capacities.
The RTAC provides valuable direction in the following areas:
- Requesting and suggesting organizational structure of information needed to determine project impact and provide accountability. This includes advice on useful formats for analyzing and evaluating the nature of distributions, whom they benefit, and how benefits are realized, which are essential for determining the impact and value of the project.
- Identifying needed improvements to the public GRIN-Global interface.
- Providing input from their respective AES Directors to curators, genebank and other administrators.
- Providing guidance to increase the NCRPIS program’s relevance to NCR stakeholders.
- Providing technical expertise, particularly in the areas of diversity assessment and taxonomy.
- Providing added breadth in understanding issues at genebanks beyond the NCRPIS.
- Understanding the challenges faced by public researchers partnering with other public institutions’ researchers, both governmental and non-governmental. This has provided useful insights for ARS and NCR administrators to guide programmatic decision-making, as well as operational guidance; this function is key because of its direct impact on the public interest as well as the specific research interests of more directly involved stakeholders.
Anche MT, Kaczmar NS, Morales N, Clohessy JW, Ilut DC, Gore MA, Robbins KR. 2020. Temporal covariance structure of multi-spectral phenotypes and their predictive ability for end-of-season traits in maize. Theoretical and Applied Genetics 133:2853-2868. https://doi.org/10.1007/s00122-020-03637-6
Angira B, Addison CK, Cerioli T, Rebong DB, Wang DR, Pumplin N, Ham JH, Oard JH, Linscombe SD, Famoso AN. Haplotype characterization of the sd1 Semidwarf gene in United States Rice. 2019. The Plant Genome 12(3):190010. https://doi.org/10.3835/plantgenome2019.02.0010
Ayana GT, Ali S, Sidhu JS, Gonzalez Hernandez, J.L., Turnipseed, B., Sehgal, S.K. 2018. Genome-wide association study for Spot Blotch resistance in hard winter wheat. Front. Plant Sci. 9:926. https://doi.org/10.3389/fpls.2018.00926
Baseggio M, Murray M, Magallanes‐Lundback M, Kaczmar N, Chamness J, Buckler ES, Smith ME, DellaPenna D, Tracy WF, Gore MA. 2020. Natural variation for carotenoids in fresh kernels is controlled by uncommon variants in sweet corn. The Plant Genome 13(1):e20008. https://doi.org/10.1002/tpg2.20008
Baseggio, M., Murray, M., Wu, D., Ziegler, G., Kaczmar, N., Chamness, J., Hamilton, J.P., Buell, C.R., Vatamaniuk, O.K., Buckler, E.S., Smith, M.E., Baxter, I., Tracy, W.F., and Gore, M.A. 2021. Genome-wide association study suggests an independent genetic basis of zinc and cadmium concentrations in fresh sweet corn kernels. G3: Genes| Genomes| Genetics 11:jkab186. https://doi.org/10.1093/g3journal/jkab186
Bretting PK. 2007. The U.S. National Plant Germplasm System in an era of shifting international norms for germplasm exchange. Acta Hort. 760:55–60. https://doi.org/10.17660/ActaHortic.2007.760.5
Byrne PF, Gardner C, Gore MA, Simon PW, Smith, Volk GM. 2018. Sustaining the Future of Plant Breeding: The critical role of the USDA-ARS National Plant Germplasm System. Crop Science 58(2):451-468. https://doi.org/10.2135/cropsci2017.05.0303
Cruppe G, Cruz CD, Peterson G, Pedley K, Asif M, Fritz A, Calderon L, da Silva CL, Todd T, Kuhnem P, Singh PK, Singh RP, Braun HJ, Naresh C, Barma D, and Valent B. 2019. Novel sources of wheat head blast resistance in modern breeding lines and wheat wild relatives. Plant Disease. 104(1):35-43. https://doi.org/10.1094/PDIS-05-19-0985-RE.
Das S, Khound R, Santra M, Santra DK. 2019. Beyond bird feed: Proso millet for human health and environment. Agriculture 9(3):64. https://doi.org/10.3390/agriculture9030064
de Oliveira Silva A, Ciampitti IA, Slafer GA, Lollato RP. 2020. Nitrogen utilization efficiency in wheat: A global perspective. European Journal of Agronomy114:126008. https://doi.org/10.1016/j.eja.2020.126008
Dillenberger, M. S., N. Wei, J. A. Tennessen, T.-L. Ashman, and A. Liston. 2018. Plastid genomes reveal recurrent formation of allopolyploid Fragaria. American Journal of Botany 105:862–874. https://doi.org/10.1002/ajb2.1085
Doyle JJ, Sherman-Broyles S. 2017. Double trouble: taxonomy and definitions of polyploidy. New Phytologist 213(2):487-93. https://doi.org/10.1111/nph.14276
Elverson TR, Kontz BJ, Markell SG, Harveson RM, Mathew FM. 2020. Quantitative polymerase chain reaction assays developed for Diaporthe helianthi and D. gulyae for Phomopsis stem canker diagnosis and germplasm screening in sunflower (Helianthus annuus). Plant Dis. 104 (3): 793-800. https://doi.org/10.1094/PDIS-09-19-1827-RE
Fabio ES, Volk TA, Miller RO, Serapiglia MJ, Kemanian AR, Montes F, Kuzovkina YA, Kling GJ, and Smart LB. 2017. Contributions of environment and genotype to variation in shrub willow biomass composition. Industrial Crops and Products 108:149-61. https://doi.org/10.1016/j.indcrop.2017.06.030
Fellers JP, Matthews A, Fritz AK, Rouse MN, Grewal S, Hubbart-Edwards S, King IP, and King J. 2020. Resistance to wheat rusts identified in wheat/Amblyopyrum muticum chromosome introgressions. Crop Science. 60:1957-1964. https://doi.org/10.1002/csc2.20120.
Gage JL, Miller ND, Spalding EP, Kaeppler SM, de Leon N. 2017. TIPS: a system for automated image-based phenotyping of maize tassels. Plant Methods 13(1):1-2. https://doi.org/10.1186/s13007-017-0172-8
Gage JL, Vaillancourt B, Hamilton JP, Manrique-Carpintero NC, Gustafson TJ, Barry K, Lipzen A, Tracy WF, Mikel MA, Kaeppler SM, Buell CR, de Leon N. 2019. Multiple Maize Reference Genomes Impact the Identification of Variants by Genome-Wide Association Study in a Diverse Inbred Panel. United States: N. p., 2019. Web. https://doi.org/10.3835/plantgenome2018.09.0069
Giannini TC, Costa WF, Cordeiro GD, Imperatriz-Fonseca VL, Saraiva AM, Biesmeijer J, Garibaldi LA. 2017. Projected climate change threatens pollinators and crop production in Brazil. PLoS One. 12(8):e0182274. https://doi.org/10.1890/15-1696.1
Grumet R*, Fei Z, Levi A, Mazourek M, McCreight JD, Schultheis J, Weng Y, Hausbeck M, Kousik S, Ling KS, Linares-Ramirez A, McGregor C, Quesada-Ocampo L, Reddy U, Smart C, Wechter P, Wehner T, Wessel-Beaver L, Wintermantel WM. 2020. The CucCAP project: leveraging applied genomics to improve disease resistance in cucurbit crops. Acta Hortic. 1294, 91-104. https://doi.org/10.17660/ActaHortic.2020.1294.12
Grumet R, McCreight JD, McGregor C, Weng Y, Mazourek M, Reitsma K, Labate J, Davis A, and Fei Z. 2021. Genetic resources and vulnerabilities of major cucurbit crops. Genes 12:1222. https://doi.org/10.3390/genes12081222
Hoke O, Campbell B, Brand M, Hau T. 2017. Impact of information on northeastern US consumer willingness to pay for aronia berries. HortScience 52(3):395-400. https://doi.org/10.21273/HORTSCI11376-16
Hou F, Zhou X, Liu P, Yuan G, Zou C, Lübberstedt T, Pan G, Ma L, Shen Y. 2021. Genetic dissection of maize seedling traits in an IBM Syn10 DH population under the combined stress of lead and cadmium. Mol Genet Genomics 296, 1057–1070 https://doi.org/10.1007/s00438-021-01800-2
Hu Y, Colantonio V, Müller BS, Leach KA, Nanni A, Finegan C, Wang B, Baseggio M, Newton CJ, Juhl EM, Hislop L, Gonzalez JM, Rios EF, Hannah LC, Swarts K, Gore MA, Hennen-Bierwagen TA, Myers AM, Settles AM, Tracy WF, Resende MFR. 2021. Genome assembly and population genomic analysis provide insights into the evolution of modern sweet corn. Nature communications 12(1):1-3. https://doi.org/10.1038/s41467-021-21380-4
Huang JT, Wang Q, Park W, Feng Y, Kumar D, Meeley R, Dooner HK. 2017. Competitive ability of maize pollen grains requires paralogous serine threonine protein kinases STK1 and STK2. Genetics 207(4):1361-70. https://doi.org/10.1534/genetics.117.300358
Hufford MB, Seetharam AS, Woodhouse MR, Chougule KM, Ou S, Liu J, Ricci WA, Guo T, Olson A, Qiu Y, Della Coletta R, Tittes S, Hudwon AI, Marant AP, Wei S, Lu Z, Wang B, Tello-Ruiz MK, Piri RD, Wang N, Kim Dw, Zeng Y, O’Connor CH, Li X, Gilbert AM, Baggs E, Krasileva KV, Portwood JL, Cannon EKS, Andorf CM, Manchanda N, Snodgrass SJ, Hufnagel DE, Jiang Q, Pedersen S, Syring ML, Kudrna DA, Llaca V, Fengler K, Schmitz RJ, Ross-Ibarra J, Yu J, Gent JI, Hirsch CN, Ware D, Dawe RK. 2021. De novo assembly, annotation, and comparative analysis of 26 diverse maize genomes. Science. 373:655-662. https://doi.org/10.1126/science.abg5289
Kamneva OK, Syring J, Liston A, Rosenberg NA. 2017. Evaluating allopolyploid origins in strawberries (Fragaria) using haplotypes generated from target capture sequencing. BMC Evolutionary Biology 17: 180. https://doi.org/10.1186/s12862-017-1019-7
Karki S, Burton P, Mackey B. 2020. The experiences and perceptions of farmers about the impacts of climate change and variability on crop production: a review. Climate and development. 12(1):80-95. https://doi.org/10.1080/17565529.2019.1603096
Khoury CK, Carver D, Greene SL, Williams KA, Achicanoy HA, Schori M, Leon B, Wiersema JH, Frances A. 2020. Crop wild relatives of the United States require urgent conservation action. PNAS 117:33351-33357. https://doi.org/10.1073/pnas.2007029117
Kukal MS, Irmak S. 2018. Climate-Driven Crop Yield and Yield Variability and Climate Change Impacts on the U.S. Great Plains Agricultural Production. Sci Rep 8, 3450. https://doi.org/10.1038/s41598-018-21848-2
Kuroha T, Nagai K, Gamuyao R, Wang DR, Furuta T, Nakamori M, Kitaoka T, Adachi K, Minami A, Mori Y, Mashiguchi K. 2018. Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding. Science 361(6398):181-6. https://doi.org/10.1126/science.aat1577
Li X, Guo T, Wang J, Bekele WA, Sukumaran S, Vanous AE, McNellie JP, Cortes LT, Lopes MS, Lamkey KR, Westgate ME. 2021. An integrated framework reinstating the environmental dimension for GWAS and genomic selection in crops. Molecular Plant. 7;14(6):874-87. https://doi.org/10.1016/j.molp.2021.03.010
Liston A, Ashman T-L. 2021. The origin and subgenome dynamics of the octoploid strawberries. Acta Horticulturae 1309: 107–118. https://doi.org/10.17660/ActaHortic.2021.1309.17
Liston A., Wei N, Tennessen JA, Li J, Dong M, Ashman T-L. 2020. Revisiting the origin of octoploid strawberry. Nature Genetics 52: 2–4. https://doi.org/10.1038/s41588-019-0543-3
Lollato RP, Jaenisch BR, Silva, SR. 2021. Genotype-specific nitrogen uptake dynamics and fertilizer management explain contrasting wheat protein concentration. Crop Sci. 61:2048-2066. https://doi.org/10.1002/csc2.20442
Ma L, Zhang M, Chen J, Qing C, He S, Zou C, Yuan G, Yang C, Peng H, Pan G, Lübberstedt T. 2021. GWAS and WGCNA uncover hub genes controlling salt tolerance in maize (Zea mays L.) seedlings. Theoretical and Applied Genetics 134(10):3305-18. https://doi.org/10.1007/s00122-021-03897-w
Maeoka RE, Sadras VO, Ciampitti IA, Diaz DR, Fritz AK, Lollato RP. 2020. Changes in the phenotype of winter wheat varieties released between 1920 and 2016 in response to in-furrow fertilizer: Biomass allocation, yield, and grain protein concentration. Frontiers in plant science. 10:1786. https://doi.org/10.3389/fpls.2019.01786
Mahoney JD, Hau TM, Connolly BA, Brand MH. 2019. Sexual and apomictic seed reproduction in Aronia species with different ploidy levels. HortScience 54(4):642-6. https://doi.org/10.21273/HORTSCI13772-18
Miller ND, Haase NJ, Lee J, Kaeppler SM, de Leon N, Spalding EP. 2017. A robust, high‐throughput method for computing maize ear, cob, and kernel attributes automatically from images. The Plant Journal 89(1):169-78. https://doi.org/10.1111/tpj.13320
Moore VM, Tracy WF. 2019. Recurrent full-sib family selection for husk extension in sweet corn. Journal of the American Society for Horticultural Science 144(1):63-9. https://doi.org/10.21273/JASHS04559-18
Moore VM, Tracy WF. 2020. Survey of organic sweet corn growers identifies corn earworm prevalence, management and opportunities for plant breeding. Renewable Agriculture and Food Systems 36:126-129. https://doi.org/10.1017/S1742170520000204
Morales N, Kaczmar NS, Santantonio N, Gore MA, Mueller LA, Robbins KR. 2020. ImageBreed: Open-access plant breeding web–database for image-based phenotyping. The Plant Phenome Journal 3:e20004. https://doi.org/10.1002/ppj2.20004
Moses N, Adhikari E, Clinesmith M, Jordan KW, Fritz AK, Akhunov E. 2020. Genomic patterns of introgression in interspecific populations created by crossing wheat with its wild relative. G3: Genes, Genomes, Genetics. 10:3651-3661. https://doi.org/10.1534/g3.120.401479.
Munaro LB, Hefley TJ, DeWolf E, Haley S, Fritz AK, Zhang G, Haag LA, Schlegel AJ, Edwards JT, Marburger D, Alderman P. 2020. Exploring long-term variety performance trials to improve environment-specific genotype× management recommendations: A case-study for winter wheat. Field Crops Research 255:107848. https://doi.org/10.1016/j.fcr.2020.107848
Nyine M, Adhikari E, Clinesmith M, Jordan KW, Fritz AK, Akhunov E. 2020. Genomic patterns of introgression in interspecific populations created by crossing wheat with its wild relative. G3: Genes, Genomes, Genetics. 10(10):3651-61. https://doi.org/10.1534/g3.120.401479
Okello PN, Petrović K, Singh A K, Kontz B, Mathew FM. 2020. Characterization of species of Fusarium cause root rot of soybean (Glycine max L.) in South Dakota, USA. Can. J. Plant Pathol. 42(4):560-571. https://doi.org/10.1080/07060661.2020.1746695
Olukolu BA, Tracy WF, Wisser R, De Vries B, Balint-Kurti PJ. 2016. A genome-wide association study for partial resistance to maize common rust. Phytopathology 106(7):745-51. https://doi.org/10.1094/PHYTO-11-15-0305-R
Pandian BA, Sathishraj R, Djanaguiraman M, Prasad PV, Jugulam M. 2020. Role of cytochrome P450 enzymes in plant stress response. Antioxidants 9(5):454. https://doi.org/10.3390/antiox9050454
Pandian BA, Varanasi A, Vennapusa AR, Sathishraj R, Lin G, Zhao M, Tunnell M, Tesso T, Liu S, Prasad PVV, Jugulam M. 2020. Characterization, genetic analyses, and identification of QTLs conferring metabolic resistance to a 4-hydroxyphenylpyruvate dioxygenase-inhibitor in sorghum (Sorghum bicolor). Front. Plant Sci. 11:596581. https://doi.org/10.3389/fpls.2020.596581
Presting GG. 2018. Centromeric retrotransposons and centromere function. Current opinion in genetics & development 49:79-84. https://doi.org/10.1016/j.gde.2018.03.004
Powell AF, Doyle JJ. 2017. Non-additive transcriptomic responses to inoculation with rhizobia in a young allopolyploid compared with its diploid progenitors. Genes 8:357. doi:10.3390/genes8120357 http://www.mdpi.com/2073-4425/8/12/357/htm
Ramakrishnan SM, Sidhu JS, Ali S, Kaur N, Wu J, Sehgal SK. 2019. Molecular characterization of bacterial leaf streak resistance in hard winter wheat. PeerJ 7:e7276 https://doi.org/10.7717/peerj.7276
Ray D, Gerber J, MacDonald GK, West PC. 2015. Climate variation explains a third of global crop yield variability. Nat Commun 6, 5989. https://doi.org/10.1038/ncomms6989
Ray DK, West PC, Clark M, Gerber JS, Prishchepov AV, Chatterjee S. Climate change has likely already affected global food production. PLoS ONE. 2019, 14(5): e0217148. https://doi.org/10.1371/journal.pone.0217148
Romay MC, Millard MJ, Glaubitz JC, Peiffer J, Swarts KL, Casstevens TM, Elshire RJ, Acharya CB, Mitchell SE, Flint-Garcia SA, McMullen MD, Holland JB, Buckler ES, Gardner CA. 2013. Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biology 14:R55. https://doi.org/10.1186/gb-2013-14-6-r55.
Santra DK, Khound R, Das S. 2019. Proso Millet (Panicum miliaceum L.) breeding: progress, challenges and opportunities. In: Al-Khayri J., Jain S., Johnson D. (eds) Advances in Plant Breeding Strategies: Cereals. Springer, Cham. https://doi.org/10.1007/978-3-030-23108-8_6
Sherman-Broyles, S., A. Bombarely, and J. J. Doyle. 2017. Characterizing the allopolyploid species among the wild relatives of soybean: Utility of reduced representation genotyping methodologies. Journal of Systematics and Evolution 55:365-376. https://doi.org/10.1111/jse.12268
Sidhu JS, Ramakrishnan SM, Ali S, Bernardo A, Bai G, Abdullah S, Ayana G, Sehgal SK. 2019. Assessing the genetic diversity and characterizing genomic regions conferring Tan Spot resistance in cultivated rye. PLoS ONE 14(3): e0214519. https://doi.org/10.1371/journal.pone.0214519
Smith S, Nickson TE, Challender M. Germplasm exchange is critical to conservation of biodiversity and global food security. 2021. Agronomy Journal. 113(4):2969-2979. https://doi.org/10.1002/agj2.20761
Smale M., Bellon MR, Jarvis D, and Sthapit B. 2004. Economic concepts for designing policies to conserve crop genetic resources on farms. Genetic Resources and Crop Evolution, 51:121-135. https://doi.org/10.1023/B:GRES.0000020678.82581.76
Schneider KL, Xie Z, Wolfgruber TK, Presting GG. 2016. Inbreeding drives maize centromere evolution. Proceedings of the National Academy of Sciences 113(8):E987-96. https://doi.org/10.1073/pnas.1522008113
Stamm M, Cramer G, Dooley SJ, Holman J, Phillips D, Rife C, Santra DK. 2015. Registration of ‘Griffin’ winter canola. J. Plant Reg. 9:144-148. doi:10.3198/jpr2014.05.0037crc.
Stamm M, Damicone J, Dooley S, Holman J, Johnson J, Lofton J, Santra D. 2019. Registration of ‘Surefire’ winter canola. J. Plant Reg. 13(3):316-319. doi:10.3198/jpr2019.02.0007crc.
Stamm M, Aiken R, Angadi S, Damicone J, Dooley S, Holman J, Johnson J, Kimura E, Larson K, Lofton J, Santra D. 2021. Registration of ‘KS4719’ winter canola. J. Plant Reg. https://doi.org/10.1002/plr2.20177
Tay D, Widrlechner MP, and J.L Corfield. 2004. Establishment of a new genebank for herbaceous ornamental plants. Plant Genetic Resources Newsletter 137:36. https://lib.dr.iastate.edu/ncrpis_pubs/45
Tennessen JA, Wei N, Straub SC, Govindarajulu R, Liston A, Ashman TL. 2018. Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries. PLoS biology 16(8):e2006062. https://doi.org/10.1371/journal.pbio.2006062
Van Etten J, de Sousa K, Aguilar A, Barrios M, Coto A, Dell’Acqua M, Fadda D, Gebrehawaryat Y, van de Gevel J, Gupta A, Kiros AY, Madriz B, Mathur P, Mengistu DK, Mercado L, Mohammed JN, Paliwal A, Pè ME, Quirós CF, Rosas JC, Sharma N, Singh SS, Solanki IS, Steinke J.2019. Crop variety management for climate adaptation supported by citizen science. Proceedings of the National Academy of Sciences 116 (10) 4194-4199; https://doi.org/10.1073/pnas.1813720116
Verzegnazzi, AL, dos Santos IG, Krause MD, Hufford M, Frei UK, Campbell J, Almeida VC, Zuffo LT, Boerman N, Lübberstedt. 2021. Major locus for spontaneous haploid genome doubling detected by a case–control GWAS in exotic maize germplasm. Theor Appl Genet 134: 1423–1434. https://doi.org/10.1007/s00122-021-03780-8
Vesco P, Kovacic M, Mistry M, Croicu M. Climate variability, crop and conflict: 2021. Exploring the impacts of spatial concentration in agricultural production. J of Peace Research. 58(1) 98-113. https://doi.org/10.1177/0022343320971020
Vetriventhan M, Azevedo VC, Upadhyaya HD, Nirmalakumari A, Kane-Potaka J, Anitha S, Ceasar SA, Muthamilarasan M, Bhat BV, Hariprasanna K, Bellundagi A. 2020. Genetic and genomic resources, and breeding for accelerating improvement of small millets: current status and future interventions. The Nucleus 4:1-23. https://doi.org/10.1007/s13237-020-00322-3
Wang X, Bao K, Reddy UK, Bai Y, Hammar SA, Jio C, Wehner TC, Madera AR, Weng X, Grumet R*, Fei Z*. 2018. The USDA cucumber (Cucumis sativus L.) collection: genetic diversity, population structure, genome-wide association studies and core collection development. Horticulture Research. 5:64. https://doi.org/10.1038/s41438-018-0080-8
Wang X, Ando K, Wu S, Reddy UK, Tamang P, Bao K, Hammar SA, Grumet R, McCreight JD, Fei Z. 2021. Genetic characterization of melon accessions in the US National Plant Germplasm System and construction of a melon core collection. Molecular Horticulture 1(1):1-3. https://doi.org/10.1186/s43897-021-00014-9
Widrlechner, MP. 2004. Insights into woody plant adaptation and practical applications. NCRPIS Conference Papers, Posters and Presentations. 5. http://lib.dr.iastate.edu/ncrpis_conf/5/
Wei N, Cronn R, Liston A, Ashman TL. 2019. Functional trait divergence and trait plasticity confer polyploid advantage in heterogeneous environments. New Phytologist 221(4):2286-97. https://doi.org/10.1111/nph.15508
Wei N, Du Z, Liston A, Ashman T-L. 2020. Genome duplication effects on functional traits and fitness are genetic context and species dependent: studies of synthetic polyploid Fragaria. American Journal of Botany 107: 262–272. https://doi.org/10.1002/ajb2.1377
Wei N, Govindarajulu R, Tennessen JA, Liston A, Ashman T-L. 2017. Genetic mapping and phylogenetic analysis reveal intraspecific variation in sex chromosomes of the Virginian strawberry. Journal of Heredity 108: 731–739. https://doi.org/10.1093/jhered/esx077
Wu D., Tanaka, R., Li, X., Ramstein, G.P., Cu, S., Hamilton, J.P., Buell, C.R., Stangoulis, J., Rocheford, T., and Gore, M.A. 2021. High-resolution genome-wide association study pinpoints metal transporter and chelator genes involved in the genetic control of element levels in maize grain. G3: Genes| Genomes| Genetics 11:jkab059. https://doi.org/10.1093/g3journal/jkab059
Wu S, Wang X, Reddy U, Sun H, Bao K, Gao L, Mao L, Patel T, Ortiz C, Abburi VL, Nimmakayala P, Branham S, Wechter P, Massey L, Ling K-S, Kousik C, Hammar SA, Tadmor Y, Portnoy V, Gur A, Katzir N, Guner N, Davis A, Hernandez AG, Wright CL, McGregor C, Jarret R, Zhnag X, Xu Y, Wehner TC, Grumet R, Levi A, Fei Z. 2019. Genome of ‘Charleston Gray’, the principal American watermelon cultivar, and genetic characterization of 1,365 accessions in the U.S. National Plant Germplasm System watermelon collection. Plant Biotechnology Journal. https://doi.org/10.1111/pbi.13136
Zheng Y, Wu S, Bai Y, Sun H, Jioa C, Blanca J, Zhang Z, Huang S, Xu Y, Weng Y, Mazourek M, Reddy U, Ando K, McCreight J, Tadmor Y, Katzir N, Giavannoni J, Ling K-S, Wechter WP, Levi A, Garcia-Mas J, Grumet R, Fei Z. 2019. Cucurbit genomics database (CuGenDB): a central portal for comparative and functional genomics of cucurbit crops. Nucleic Acids Res. https://doi.org/10.1093/nar/gky944
NC7 Participant References
Avolio ML, Forrestel EJ, Chang CC, La Pierre KJ, Burghardt KT, Smith MD. 2019. Demystifying dominant species. New Phytol, 223: 1106-1126. https://doi.org/10.1111/nph.15789
Karban, R. 2015. Plant Sensing and Communication. University of Chicago Press, Chicago. https://doi.org/10.7208/9780226264844
Karban, R. 2019. The ecology and evolution of induced responses to herbivory and how plants perceive risk. Ecol Entomol, 45: 1-9. https://doi.org/10.1111/een.12771
Karban R. Plant Communication. 2021. Ann Rev of Ecology, Evolution, and Systematics. 52:1-24. https://doi.org/10.1146/annurev-ecolsys-010421-020045
Karban R, LoPresti E, Vermeij GJ, and Latta R. 2019. Unidirectional grass hairs usher insects away from meristems. Oecologia 189:711-718. https://doi.org/10.1007/s00442-019-04355-7
Karban R, Orrock JL. 2018. A judgment and decision-making model for plant behavior. Ecology, 99: 1909-1919. https://doi.org/10.1002/ecy.2418
Karban R, Takabayashi J. 2019. Chewing and other cues induce grass spines that protect meristems. Arthropod-Plant Interactions 13:541-550. https://doi.org/10.1007/s11829-018-9666-1
Koerner SE, Smith MD, Burkepile DE, Hanan NP, Meghan LA, Collins SL, Knapp AK, Lemoine NP, Forrestel EJ, Eby S, Thompson DI, Aguado-Santacruz GA, Anderson JP, Anderson TM, Angassa A, Bagchi S, Bakker ES, Bastin G, Baur LE, Beard KH, Beever EA, Bohlen PJ, Boughton EH, Canestro D, Cesa A, Chaneton E, Cheng J, D’Antonio CM, Deleglise C, Dembélé F, Dorrough J, Eldredge DJ, Fernandez-Going B, Fernández-Lugo S, Fraser LH, Freedman B, García-Salgado G, Goheen JR, Guo L, Husheer S, Karembé M, Knops JMH, Kraaij T, Kulmatiski A, Kytöviita M, Lezama F, Loucougaray G, Loydi A, Milchunas DG, Milton SJ, Morgan JW, Moxham C, Nehring KC, Olff H, Palmer TM, Rebollo S, Riginos C, Risch AC, Rueda M, Sankaran M, Sasaki T, Schoenecker KA, Schultz NL, Schütz M, Schwabe A, Siebert F, Smit C, Stahlheber KA, Storm C, Strong DJ, Su J, Tiruvaimozhi YV, Tyler C, Val J, Vandegeheuchte ML, Veblen KE, Vermeire LT, Ward D, Wu J, Young T), Yu Q, Zelikova TJ. 2018. Change in dominance determines herbivore effects on plant biodiversity. Nat Ecol Evol 2, 1925–1932. https://doi.org/10.1038/s41559-018-0696-y
LoPresti E, Karban R. 2016. Chewing sandpaper: grit, plant apparency and plant defense in sand-entrapping plants. Ecology 97:826-833. https://doi.org/0.1890/15-1696.1
LoPresti E, EF, Pan V, Goidell J, Weber M, Karban R. 2019. Mucilage-bound sand reduces seed predation by ants but not by reducing apparency: a field test of 53 plant species. Ecology 100:e02809. https://doi.org/10.1002/ecy.2809
Pan VS, McMunn M, Karban R, Goidell J, Weber MG, LoPresti EF. 2021. Mucilage binding to ground protects seeds of many plants from harvester ants: A functional investigation. Functional Ecology. 35, 2448– 2460. https://doi.org/10.1111/1365-2435.13881
Parker LE, McElrone AJ, Ostoja SM, Forrestel EJ. 2020. Extreme heat effects on perennial crops and strategies for sustaining future production. Plant Science 295:110397 https://doi.org/10.1016/j.plantsci.2019.110397
Wetzel, W., Kharouba, H., Robinson, M, Holyoak M, Karban R. 2016. Variability in plant nutrients reduces insect herbivore performance. Nature 539:425–427. https://doi.org/10.1038/nature20140