Genomic Science Program
U.S. Department of Energy | Office of Science | Biological and Environmental Research Program

Advancing Towards Synthetic Biology that Can Detect and Control Plant-Fungal Interactions

Authors:

Jared LeBoldus1* (jared.leboldus@oregonstate.edu), Breeanna Urbanowicz2, Parastoo Azadi2, Joanna Tannous3, Daniel Jacobson3, Paul E. Abraham3

Institutions:

1Department of Botany and Plant Pathology, College of Agricultural Sciences, Oregon State University–Corvallis; 2Complex Carbohydrate Research Center, University of Georgia; 3Biosciences Division, Oak Ridge National Laboratory

URLs:

Goals

The Secure Ecosystem Engineering and Design (SEED) Science Focus Area (SFA) led by Oak Ridge National Laboratory combines unique resources and expertise in the biochemistry, genetics, and ecology of plant-microbe interactions with new approaches for analysis and manipulation of complex biological systems. The long-term objective is to develop a foundational understanding of how non-native microorganisms establish, spread, and impact ecosystems critical to DOE missions. This knowledge will guide biosystems design for ecosystem engineering while providing the baseline understanding needed for risk assessment and decision-making.

Abstract

The introduction of microorganisms into new environments can have profound effects on resident communities (e.g., plants, associated microbiome) and local ecosystem services (e.g., soil stabilization, carbon sequestration). Depending on the organism and environmental context, these impacts can be positive, negative, or neutral. Over the last decade, the commercialization of several unique strains of beneficial fungi have begun improving agricultural yields at a lower cost-in-comparison to chemical fertilizers, while mitigating negative environmental impacts from agrochemicals. However, there are natural barriers limiting the use and reliability of beneficial fungi beyond the existing range of applications (i.e., host-specific benefits). Understanding these barriers will not only improve the ability to safely and reliably engineer ecosystems using fungi to reach specific goals (e.g., sustainable biofeedstocks) but also help predict and prevent economically and ecologically costly disease outbreaks. Evolutionary and ecological principles hindering targeted beneficial microbial inoculants frequently overlap with those overcome by invasive pathogens, thus learning about the first will enable better understanding of pathogen-mediated invasions.

Historically, there has been more research on the anthropogenic introduction and movement of fungal pathogens. In fact, recent population genomics analyses show human translocation of Populus across North America resulted in the spread of Sphaerulina musiva (formerly Septoria musiva) that now threatens natural forests and managed plantations. This pathogen has recently expanded to a new host, Populus balsamifera, and causes fatal stem cankers in the DOE-flagship species Populus trichocarpa.

Knowing the causal genetic factors associated with establishment and functional impact of S. musiva in the genus Populus will contribute to innovations in biodesign tools for early detection or altered outcomes of plant–fungal interactions. For the invader-centric research, researchers have assembled a pangenome from 146 S. musiva isolates collected from regions across North America spanning the range of several Populus species. This population genomics resource is being used to characterize the gene space of S. musiva and has identified more than 6-million single nucleotide polymorphisms, of which 50% were not found in the reference genome. Researchers have performed genome-wide association studies for rapid genotype-phenotype discovery. Using the recently developed protoplast-mediated transformation system with CRISPR-Cas9, the team tested several useful biodesign targets for manipulating S. musiva virulence.

Understanding the establishment and spread of S. musiva must also consider the host genes that regulate plant-fungal symbiosis. In several instances, the team has demonstrated the role of G-type receptor-like kinases (LecRLKs) in the susceptibility of a plant host to fungal colonization in both beneficial and pathogenic fungi. Building on this work, researchers hypothesized that advancing the understanding of G-type lecRLKs will inform biodesign strategies to detect and control plant- fungal interactions. To this end, researchers are working to determine how structural features of fungal cell walls are selectively recognized by G-type lecRLKs and this information is being used to design synthetic protein receptors systems that selectively detect fungal-derived ligands to report (biosensor) or permit (biocontrol) plant-fungal interactions.

Collectively, these studies will provide knowledge and tools to detect and control fungal invasions.

Funding Information

The Secure Ecosystem and Engineering Design Science Focus Area is sponsored by the Genomic Science Program, DOE, Office of Science, BER program, under FWP ERKPA17. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the DOE under contract no. DE-AC05-00OR45678.