Award Abstract # 1545553
PIRE: U.S.-East Africa Research and Education Partnership: Cassava mosaic disease - A paradigm for the evolution of insect-transmitted plant virus pathosystems

NSF Org: OISE
Office of International Science and Engineering
Recipient: NORTH CAROLINA STATE UNIVERSITY
Initial Amendment Date: September 23, 2015
Latest Amendment Date: March 28, 2023
Award Number: 1545553
Award Instrument: Continuing Grant
Program Manager: Paul Raterron
praterro@nsf.gov
 (703)292-8565
OISE
 Office of International Science and Engineering
O/D
 Office Of The Director
Start Date: October 1, 2015
End Date: September 30, 2024 (Estimated)
Total Intended Award Amount: $5,000,000.00
Total Awarded Amount to Date: $5,000,000.00
Funds Obligated to Date: FY 2015 = $1,029,266.00
FY 2016 = $1,188,239.00

FY 2018 = $1,184,677.00

FY 2020 = $225,228.00
History of Investigator:
  • Linda Hanley-Bowdoin (Principal Investigator)
    linda_hanley-bowdoin@ncsu.edu
  • Siobain Duffy (Co-Principal Investigator)
  • George Kennedy (Co-Principal Investigator)
Recipient Sponsored Research Office: North Carolina State University
2601 WOLF VILLAGE WAY
RALEIGH
NC  US  27695-0001
(919)515-2444
Sponsor Congressional District: 02
Primary Place of Performance: North Carolina State University
Raleigh
NC  US  27695-7622
Primary Place of Performance
Congressional District:
02
Unique Entity Identifier (UEI): U3NVH931QJJ3
Parent UEI: U3NVH931QJJ3
NSF Program(s): PIRE- Prtnrshps Inter Res & Ed
Primary Program Source: 01001516DB NSF RESEARCH & RELATED ACTIVIT
01001617DB NSF RESEARCH & RELATED ACTIVIT

01001718DB NSF RESEARCH & RELATED ACTIVIT

01001819DB NSF RESEARCH & RELATED ACTIVIT

01002021DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 5976, 5991, 7338, 7742
Program Element Code(s): 774200
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.079

ABSTRACT

This PIRE project establishes a research and training partnership between scientists and students in the United States and East Africa to study how plant DNA viruses change over time. Plant DNA viruses have emerged as leading pathogens that threaten crops worldwide. These studies will focus on Cassava mosaic disease, which is endemic to Africa and severely limits the production of cassava, a major food crop across the continent. Because Africa is one of the fastest growing regions in the world, with a population projected to double to 2.4 billion people by 2050, producing sufficient quantities of high quality, nutritious food is a challenge there. Agriculture is increasingly a global enterprise and finding solutions to food security problems will depend on research partnerships such as this one that explores the basic science of how plant DNA viruses evolve and what limits their ability to adapt over time. Such fundamental knowledge can then be used by others to develop rational, durable strategies to control these important plant pathogens. The project, which relies on the combined expertise and resources of U.S. and African participants, provides an excellent framework for training U.S. students to develop their scientific skills and to work in a global community to help ensure the future security of the developing and developed world.

Molecular evolution of plant viruses occurs through mutation, recombination and reassortment of viral genome components, resulting in a high degree of variation. In complex pathogen-host systems, the evolutionary outcomes are influenced by many ecological factors including agricultural practices, insect vector populations, interactions between crops and reservoir plants, and climate. Most of our knowledge of viral evolution is based on field-collected samples, which only provide snapshots of viral diversity at specific times and locations. To examine the full evolutionary potential of plant DNA viruses and the bottlenecks that constrain their evolution, we propose a comprehensive analysis of the drivers of viral genetic diversity, emergence, persistence and spread under tightly controlled experimental conditions. We will focus on the DNA viruses that cause Cassava mosaic disease using NexGen sequencing to compare their diversity during vegetative and whitefly transmission, in mixed infections, and in wild plants that serve as reservoir hosts. We will ask if movement through the host plant and/or transmission by insect vectors serve as bottlenecks that limit viral diversity. Our study of the evolutionary potential and factors that contribute to Cassava mosaic disease is transformative in that it will provide a comprehensive framework for examining viral evolution in relationship to the host, the insect vector and the environment using a crop and inoculation methods that accurately reflect real world conditions. Our integrated approach will also serve as a model for examining viral evolution and will inform the development of control strategies for other insect-transmitted viruses that negatively impact plant, animal and human health. Postdoctoral researchers, graduate students and undergraduates will be mentored by a strong international research team, which includes experts on viral population genetics, insect vector transmission and population dynamics, virus/vector/plant interactions, and STEM education. The multidisciplinary nature of the research will provide trainees experience in laboratory and field-based research as well as bioinformatics. This will prepare them to become globally engaged, independent scientists with a solid foundation in a range of research methodologies and environments and first-hand experience in international and multidisciplinary collaborations.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 24)
A. Crespo-Bellido, J. S. Hoyer, Y. Burgos-Amengual, S. Duffy "Phylogeographic analysis of Begomovirus coat and replication-associated proteins" J. Gen. Virol. , v.105 , 2024 , p.002037 10.1099/jgv.0.002037
Aimone, C.D., Hoyer, J.S., Dye, A.E., Deppong, D.O., Duffy, S., Carbone, I., Hanley-Bowdoin "An improved experimental strategy for preparing circular ssDNA virus genomes for next-generation sequencing" Journal of Virological Methods , v.300 , 2022 , p.114405 10.1016/j.jviromet.2021.114405
Aimone C.D., Lavington, E., Hoyer, J.S., Deppong, D.O., Mickelson-Young, L., Jacobson, A., Kennedy, G.G., Carbone, I., Hanley-Bowdoin, L., Duffy, S "Population diversity of cassava mosaic begomoviruses increases over the course of serial vegetative propagation" Journal of General Virology , v.102 , 2021 10.1099/jgv.0.001622
A. Jacobson, P. Sseruwagi, S. Duffy "Whiteflies making mosaics and streaking cassava: vectors of viruses that threaten food security" Current Opinions in Virology , v.33 , 2018 , p.167
Burley, S., Y. Bromberg, P. Craig, S. Duffy, S. Dutta, B. Hall, B. Hudson, J. Jiang, S. Khare, J. Koeppe, J. Lubin, S. Mills, M. Pikaart, R. Roberts, V. Sarma, J. Singh, J. Tischfield, L. Xie, C. Zardecki "Virtual boot camp: COVID-19 evolution and structural biology" Biochemistry and Molecular Biology Education , v.48 , 2020 , p.511 10.1002/bmb.21428
Crespo-Bellido, A., and Duffy, S. "The how of counter-defense: viral evolution to combat host immunity" Current Opinion in Microbiology , v.74 , 2023 , p.102320 10.1016/j.mib.2023.102320
Crespo-Bellido, A., Duffy, S. "Strand-Specific Patterns of Codon Usage Bias Across Cressdnaviricota" Frontiers in Virology , v.2 , 2022 , p.899608 10.3389/fviro.2022.899608
Crespo-Bellido, A., Hoyer, J.S., Dubey, D., Jeannot, R.B., Duffy, S. "Interspecies recombination has driven the macroevolution of cassava mosaic begomoviruses" Journal of Virology , v.95 , 2021 , p.e0054121 10.1128/JVI.00541-21
Dubey, D., Hoyer, J.S., and Duffy, S. "Limited role of recombination in the global diversification of begomovirus DNA-B protein" Virus Research , v.323 , 2023 , p.198959 10.1016/j.virusres.2022.198959
Dye, A. E., Muga, B., Mwangi, J., Hoyer, J.S., Ly, V., Rosado, Y., Sharpee, W., Mware, B., Wambugu, M., Labadie, P., Deppong, D., Jackai, L., Jacobson, A., Kennedy, G., Ateka, E., Duffy, S., Hanley-Bowdoin, L., Carbone, I. and J. T. Ascencio-Ibáñez "Cassava begomovirus species diversity changes during plant vegetative cycles" Front. Microbiol. , v.14 , 2023 , p.1163566 10.3389/fmicb.2023.1163566
Hoyer, J.S., Fondong, V.N., Dallas, M.M. Aimone, C.D., Deppong, D.O. Duffy, S., Hanley-Bowdoin, L. "Deeply sequenced infectious clones of key cassava begomovirus isolates from Cameroon. Microbial Resource AnnouncementsNCBI Bioproject PRJNA649777" Microbiology Resource Announcements , 2020 10.1128/MRA.00802-20
(Showing: 1 - 10 of 24)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

The project established a research and training partnership between scientists and trainees in the United States and East Africa to study how plant viruses change over time. It was highly multidisciplinary, bringing together experts in virology, entomology, evolutionary biology, and and STEM education from 4 U.S. universities and 3 institutions in Kenya and Tanzania. 

The research goal was to understand the molecular evolution of plant viruses using deep sequencing and controlled experiments that mimic field conditions. Studies focused on two important viral pathosystems – one in cassava, the other tomato. Cassava, a vegetatively propagated, staple food crop in Sub-Saharan Africa, is critically important to the food security of ca. one billion people. Tomato, a valuable source of nutrients, is grown worldwide. Both crops are threatened by diseases caused by whitefly-transmitted, single-stranded DNA viruses in the Begomovirus genus. Research examined aspects of the cassava and tomato pathosystems that potentially contribute to the rapid evolution and capacities of begomoviruses to adapt over time and cause severe disease and yield losses. Because begomoviruses are frequent and emergent pathogens of nearly all tropical and subtropical crops, project results are directly translatable to plant pathosystems worldwide and to insect-transmitted viruses of many hosts. 

Within this framework, we provided junior faculty, postdoctoral researchers, and graduate and undergraduate students with multidisciplinary, multicultural research experiences and training to prepare them to become independent scientists able to work globally to ensure availability of plentiful and nutritious food. Forty-one undergraduate students, 9 graduate students, 5 postdoctoral researchers, and 3 junior faculty received research training. The large number of students in the project reflected a strong interest in working on “real-world” problems. Many trainees gained first-hand international experience at meetings, in the laboratory, and in the field. Participants produced 4 graduate theses, 2 book chapters, 5 reviews, and 20 journal articles. Most of these publications were led by graduate students and postdoctoral researchers; several included undergraduate authors. Subsequently, many trainees went on to postgraduate or professional training in plant sciences or human health programs. Two students were selected for the BASF Ph.D. Leadership Development Program, which is designed to propel Ph.D. graduates into positions of leadership in industry. Junior faculty involved in the project were promoted and are engaged international research and education.

Our research uncovered several important aspects of begomovirus evolution and pathosystems.

  • Nine begomovirus species are associated with cassava disease in Sub-Saharan Africa. They can be transmitted by whiteflies and by vegetative propagation of infected stems. Our results showed that some viral species are preferentially maintained during vegetative regrowth, while the maintenance of others depends on whitefly transmission. Viruses that persist during vegetative transmission pose a greater threat to “clean seed” systems used to produce healthy cassava materials for African farmers. 
  • During vegetative propagation of cassava begomoviruses, we observed selective pressure in specific nucleotide sequences required for viral replication but not in protein coding sequences. This difference likely reflects the ability of viral proteins to act in trans, while replication sequences must act in cis. We also found that spontaneous mutational diversity during vegetative propagation differed between cassava begomoviruses, suggesting that vegetative propagation differentially affects the evolution of cassava begomovirus species.
  • Many begomoviruses occur as coinfections that can increase disease severity. Phylogenetic analyses of begomovirus genomes revealed that recombination during coinfection plays a larger role in the generation of new viral species than mutations, although mutations occur more frequently. There is a strong geographical bias with respect to which viruses undergo recombination, likely reflecting the historical separation of plant viruses geographically. With increased international trade, this bias may disappear and lead to the emergence of new viruses and diseases in agronomically important plant species. 
  • Monopartite begomoviruses have one genome segment while bipartite viruses have two -– DNA-A and DNA-B. We found a novel type of coinfection in tomato involving a monopartite virus and the whitefly-transmissible DNA-A segment of a bipartite virus, in which the monopartite virus supported movement of the DNA-A segment in the absence of DNA-B. Similar infections likely occur in the field and impact the spread and severity of begomovirus diseases.
  • The DNA-A to DNA-B ratio varies in infected plants, while the ratio transmitted by whiteflies is 1:1. Because both genome segments are required to establish a systemic infection, this interaction between virus and vector fosters transmission and spread of bipartite begomoviruses.

Agriculture is increasingly a global enterprise. Solutions to food security problems will depend on research partnerships such as this one that explored the basic science of how plant DNA viruses evolve and what limits their adaptability over time. Such fundamental knowledge informs the development of rational, durable strategies to control these important plant pathogens. U.S. and African scientists who engaged in the project are well positioned to work as independent scientists in the global community to help ensure future security during these rapidly changing times. 


Last Modified: 01/18/2025
Modified by: Linda K Hanley-Bowdoin

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