Source: VIRGINIA POLYTECHNIC INSTITUTE submitted to
UNDERSTANDING PLANT NATURAL PRODUCT BIOSYNTHESIS IN BLUEBERRY THROUGH CORE GENE DISCOVERY
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1031807
Grant No.
2022-67013-41879
Cumulative Award Amt.
$135,063.15
Proposal No.
2023-11869
Multistate No.
(N/A)
Project Start Date
Dec 15, 2023
Project End Date
Jan 14, 2026
Grant Year
2024
Program Code
[A1103]- Foundational Knowledge of Plant Products
Recipient Organization
VIRGINIA POLYTECHNIC INSTITUTE
(N/A)
BLACKSBURG,VA 24061
Performing Department
(N/A)
Non Technical Summary
Food crops provide the essential micronutrients needed in the human diet through production of minerals and vitamins. Additionally, plants produce thousands of specialized metabolites, many of which have human health benefits. The Ericaceae family contains several economically important fruit crops that produce diverse natural products, including blueberry and cranberry. Cultivated blueberry has seen an annual increase in market size since 2000, with rising popularity due to the overall sweet fruit flavor and consumer perceived levels of known health-promoting compounds. Blueberries also produce iridoid compounds, which are potent natural products with human health benefits. Despite these known properties, little work has been done to fully understand the genetic basis of iridoid biosynthesis in cultivated blueberry. This New Investigator Seed Grant aims to obtain data to identify core iridoid biosynthetic genes in blueberry. A multi-faceted approach incorporating transcriptomic, genomic and metabolomic data will be used to elucidate genes involved in the biosynthesis of the iridoid glycoside monotropein in blueberry. The objectives of the proposal are: 1) Identify iridoid biosynthetic pathway genes in blueberry using transcriptomic, orthology, co-expression and genome sequencing analysis, and 2) Validate the computationally predicted gene targets through functional enzyme characterization. This work leverages the within-species genotypic and phenotypic diversity in blueberry iridoid production to understand the genetic basis of natural product biosynthesis in this economically important crop. Outcomes from this proposal will serve as a platform to more fully understand iridoid production in blueberry and can translate into the development of new blueberry varieties with enhanced human health benefits.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2011120108050%
2061120100025%
2061120104025%
Goals / Objectives
The research in this proposal addresses the genetic basis of the synthesis of plant-derived, high-value chemicals in blueberries. As part of the balanced human diet blueberries can provide essential micronutrients, vitamins, and thousands of specialized metabolites with additional health benefits. The Ericaceae plant family contains several economically important fruit crops including blueberry and cranberry. Cultivated blueberry (Vacciniumspecies) has seen an annual increase in U.S. market size since 2000. The popularity of this crop is based on their overall sweet flavor of the fruit and the consumer perceived levels of known health-promoting compounds, including vitamin C, folate, phenolic and flavonoid compounds. Blueberries also produce iridoid compounds, which are potent natural products with human health benefits. Several iridoid compounds have been identified in a subset of species within the Ericaceae, with significant inter-species diversity observed in production of the iridoid glycoside monotropein in blueberry.Despite the relevant human health properties, little work has been done to fully understand the iridoid biosynthetic pathway in cultivated blueberry.This New Investigator Seed Grant aims to address this knowledge gap by obtaining data to identify core iridoid biosynthetic genes in blueberry.Themajor hypothesisof this work is that the genes involved in iridoid biosynthesis in blueberry can be identified by comparative genomics and orthology analysis using specific blueberry varieties known to have presence/absence of this class of secondary metabolites.A multi-faceted approach incorporating transcriptomic, genomic and metabolomic data will be used to elucidate genes involved in the biosynthesis of the iridoid glycoside monotropein in cultivated blueberry. This work leverages the within-species genotypic and phenotypic diversity in blueberry iridoid production to understand the genetic basis of natural product biosynthesis in this economically important crop.The two objectives of the proposed project are:1)Identify iridoid biosynthetic pathway genes in blueberryusing transcriptomic, orthology, co-expression and genome sequence analysis; and2)Validate the computationally predicted gene targets through functional enzyme characterization.
Project Methods
Objective 1:Identify iridoid biosynthetic pathway genes in blueberryHypothesis: The combination of analyses using transcriptomics, orthology, co-expression and genome sequence analysis will reveal the candidate iridoid biosynthesis genesObjective 1, Task 1.A new cultivar and tissue panel will be generated for select cultivars to expand the genetic and phenotypic diversity needed for identification of monotropein biosynthetic genes. Both Ornablue and Concord cultivars have been previously analyzed for monotropein content in several tissues. We already havede novotranscriptome assemblies completed for tissues from Ornablue (+) and Concord (-) which can be used for candidate gene identification using orthology analysis to previously characterized iridoid biosynthetic genes inC. roseus. Three additional cultivars 1) Summit, a previously identified monotropein-positive cultivar that is a southern highbush ecotype (Leisner et al., 2017) 2) Cara's choice (monotropein-negative), a half-sibling of Summit (Ehlenfeldt & Stretch, 2005) and northern highbush ecotype, and 3) Tifblue, a rabbiteye cultivar (V. virgatum)have been selected for analysis to expand the panel diversity. Tifblue is a late season blueberry variety that is one of the most important cultivars in rabbiteye breeding (Hancock et al., 2008).Rabbiteye blueberries are native to the southeastern U.S. and a major ecotype grown in Alabama and southern Georgia (Coneva, 2013). In this new expanded panel, root tissue will be analyzed for all cultivars as other plant species has shown significant production of iridoids in plant roots (e.g., Kellner et al., 2015). As the origin and/or transport of monotropein production in blueberry are unknown, analysis of root tissue is invaluable. This panel will also include young leaves sprayed with methyl jasmonate (MeJa).Previous work has demonstrated that application of MeJa can increase the level of monoterpenes in cranberry (Rodriguez-Saona et al., 2013),C. roseus(Liscombe et al., 2011), and other species (Wang et al., 2010; Nagatoshi et al., 2011; Góngora-Castillo et al., 2012; Semiz et al., 2012). It is hypothesized that increasing monotropein production will increase expression and/or abundance of genes related to iridoid biosynthesis and be a valuable asset in gene discovery and co-expression analysis.All samples for the blueberry tissue diversity panel will be collected from verified cultivars.Monotropein content of ground tissues will be analyzed and quantified by targeted LC-MS using an authentic standard as described in Leisner et al. (2017). For transcriptomic analysis, RNA will be isolated and cDNA libraries will be constructed and sequenced with the Illumina HiSeq4000 sequencer. In addition to short-read sequencing,transcriptome assemblies for all cultivars will be reconstructed using isoform sequencing (Iso-Seq) from Pacific Biosciences (PacBio). Short-read Illumina data generated from the HiSeq4000 will be used to error correct the reconstructed transcriptomes and generate gene expression data.From the Iso-Seq analysis a high-quality, full-length transcripts will be generated with no assembly required. Gene expression analysis will be completed by mapping each RNA-Seq library to the transcriptome for each cultivar followed by determination of transcript abundance values.Objective 1, Task 2.Enzymes in threekey steps in the early iridoid biochemical pathway will be selected for targeted orthology analysis - GES, G8H and GOR. These genes represent the first committed steps in iridoid biosynthesis (Miettinen et al., 2014) and should share sufficient homology withC. roseusto utilize comparative genomic and orthology analysis. We will also use the new data to validate our previous work with ISY.Orthology analysis will be completed and potential orthologs will be analyzed for presence/absence variants and transcript abundance by mapping the transcript sequences to theV. corymbosumgenome (cv. Draper, Colle et al., 2019) and to the transcriptome assembly for each cultivar.Co-expression analyses, including hierarchical clustering, principal component analyses, mutual rank, and self-organizing maps will be used to identify the candidate genes involved in the early iridoid biosynthetic pathway (Obayashi & Kinoshita, 2009; Saeed et al., 2003; Wehrens & Buydens, 2007).Objective 2: Validate the computationally predicted gene targets through functional enzyme characterizationHypothesis:The functionality of the gene products can be confirmed by biochemical analysis.Objective 2, Task 1.In order to validate the computationally predicted gene targets, cloning of genes encoding three key enzymes (GES, G8H, GOR) will be completed for two blueberry genotypes, with the long-term goal of confirming enzyme sequences for all cultivars (outside the scope of this grant). The entire coding sequence will be amplified and cloned into pOPINF expression vector using In-Fusion cloning (Takara Bio). Plasmids containing the cloned gene will be transformed into competentE. colior yeast expression strain cells to produce protein in quantities suitable for enzymatic analysis. After lysing the cells by sonication, the soluble portion will be loaded onto Ni-NTA agarose resin (Qiagen), and the recombinant His-tagged protein eluted. The purified recombinant protein will then be used in Task 2.Objective 2, Task 2.To validate enzyme function, end-point enzyme assays for the enzymes of interest will be done according to Lichman et al., 2020. This is key to confirming the cloned gene sequence produces a protein that has the assigned function in the iridoid biosynthetic pathway. To obtain anin vitroprofile of reaction products for the enzyme of interest GC-MS will be performed(Yang et al., 2009; Geu-Flores et al., 2012). The early biosynthetic intermediates, such as geranyl diphosphate, geraniol, and 8-hydroxygeraniol required as a substrate for these enzymes are commercially available. Completion of this objective will be done in collaboration with Dr. Sarah O'Connor, Director at the Max Planck Institute for Chemical Ecology.

Progress 12/15/23 to 12/14/24

Outputs
Target Audience:There are several target audiences that are the focus of effort for the duration of this USDA NIFA Project. They include: Early Career Researchers: This includes early career researchers through both teaching and research mentoring. Graduate students have been served by this project through direct and indirect involvement in research projects, data analysis and presentation of their research findings. Students will also be directly involved in outreach opportunities that will serve the local community. For example, the graduate student was involved in the annual outreach event Kid's Tech University hosted by the Fralin Life Sciences Institute at Virginia Tech. During this event they interacted with middle school students and exposed them to plant science by interacting with fruits and vegetables through microscopy and DNA extractions. We have also mentored a high school student during the summer and into the winter (2024) to learn about molecular cloning and functionally characterize a gene in the iridoid biosynthetic pathway in blueberry. Breeders: We have continued our collaboration with the small fruit breeder at Auburn University in the Department of Horticulture. We work with them to translate the research findings in a way that will facilitate future breeding efforts focused on natural product biosynthesis in blueberry. I have also established a collaboration with the berry fruit extension specialist at Virginia Tech to establish blueberry plots at their field site, and establish new connections with blueberry farmers in the Hampton Roads region of Virginia. Broader scientific community: The findings from this work will be disseminated through conference presentations and open-access peer-reviewed publications. Additionally, data will be deposited in public repositories (NCBI and Github). This will allow the larger scientific community access to our research findings and increase understanding and awareness of natural product biosynthesis in blueberry. Changes/Problems:PI Leisner has moved her research group from Auburn University to Virginia Tech (VT) in August 2023. The graduate student working with Dr. Leisner also moved with the lab. This has ensured a smooth transition of the project, however there was a pause in data collection and analysis while the lab was transitioning during summer 2023. The wet lab is now set-up for PI Leisner at VT. PI Leisner also now has a research technician with significant experience in molecular cloning. This has allowed us to successfully produce GES protein (which we were unable to at Auburn University). This will facilitate completion of Objective 2 for more genes now that the system is established. What opportunities for training and professional development has the project provided?Dr. Leisner has provided teaching and mentoring to the graduate students involved in the project. Dr. Leisner has provided them with the skills and learning environment to further their own curiosity and research endeavors in natural product biosynthesis in blueberry. Dr. Leisner has also taught a course focused on plant physiology and genomics which provides further training for students. Additionally, Dr. Leisner meets weekly with the graduate student on the project to discuss project goals, recent progress, project hurdles and next steps. This gives the graduate student an opportunity to discuss their own scientific questions and practice their scientific communication skills. The graduate student also meets regularly with the research technician involved in the project to gain insights into the molecular cloning work and aid in troubleshooting. How have the results been disseminated to communities of interest?All data produced from this proposal will be publicly available through use of data servers after publication, data repositories (i.e., GitHub) and federal data repositories (NCBI and SRA). Funds from this project will also be used to provide open access to all future publications to make them freely available to the public. The research conducted under this project (completed by the PI, graduate student and technician) was presented at three meetings and one on-campus seminar during the current reporting period. The asterisks (*) indicates the graduate student working on the project. Leisner CP (2024) Invited Keynote speaker, Plant and Microbial Sciences Graduate Symposium, Washington University in St. Louis. Leisner CP (2024) Invited Seminar, "Comparative genomics to understand natural product biosynthesis in blueberries." Genetics, Bioinformatics, & Computational Biology (GBCB) Program, Virginia Tech. Kaur I*, Leisner CP (2024) "Small Molecules Shaping Big Interactions: Interdisciplinary Perspectives from Early Career Botanists Bridging Biochemistry, Physiology, Animal Behavior, Ecology, and Evolution." Botanical Society of America, Grand Rapids, Michigan. Kaur I*, Leisner CP (2024) "Elucidation of the biosynthetic pathway involved in the production of monotropein in blueberry using transcriptomic approaches." The New Phytologist Next Generation Scientists Conference, Durham, North Carolina What do you plan to do during the next reporting period to accomplish the goals?We have several plans for the next reporting period. First, we will continue to screen cultivars of blueberry for the presence of monotropein (Objective 1) in collaboration with Dr. Dennis Cladis. Additionally, we will continue to analyze the short-read and long-read (Iso-Seq) RNA-Sequencing data for gene discovery (Objective 1). We will continue work to clone and functionally characterize key genes in the monotropein biosynthetic pathway in blueberry (Objective 2), with a current priority of GES.Finally, we are exploring the impact of monotropein production on blueberry flavor and will continue this work in collaboration with faculty at Virginia Tech.

Impacts
What was accomplished under these goals? Several experiments have been completed in during the reporting period. First, we have completed cloning and functional characterization of the ISY gene in blueberry (Lawas et al., 2023). Subsequently, we performed mutual rank and other co-expression analysis to determine the role of transcript expression on the production of monotropein blueberry (Lawas et al., 2023). We are now working on cloning another gene in the pathway, GES, which is a key step differentiation the production of monoterpenes and iridoid compounds (Objective 2). This work is being continued by the graduate student in the laboratory with support from a research technician. The graduate student provided updated sequences from GES to the research technician. The research technician successfully expressed GES in tobacco and purified the protein. The research technician is now working to purify more protein for functional characterization of GES and to express a truncated version of GES in tobacco to see if the pro-peptide region is required for function of GES. The functional characterization will be carried out by the graduate student. The graduate student helped prepare samples for short-read RNA-sequencing and long-read Iso-sequencing. The graduate student has analyzed all long-read Isoseq data and identified all candidate genes in the early iridoid biosynthetic pathway, and candidates for all genes in the late monotropein-biosynthetic pathway except the final tailoring enzymes (oxidases). The graduate student is now working to analyze the short-read RNA-sequencing data for differential expression analysis and co-expression analysis to validate the candidate genes and determine the mechanism by which some cultivars of blueberry produce iridoids and others do not. The graduate student has also worked with a faculty in the Department of Food Science and Technology at Virginia Tech (Dr. Dennis Cladis) to establish LC-MS methodology to effectively measure monotropein in blueberry fruits. They are finalizing this work and will screen an additional 33 cultivars of blueberry for the presence and quantity of monotropein. Finally, the graduate student has worked with a faculty in the School of Plant and Environmental Sciences at Virginia Tech to screen cultivars with and without monotropein for the content of sugars, amino acids and sugar acids using GC-MS to determine the impact of monotropein production on flavor. Prior to this reporting period the graduate student also obtained untargeted LC-MS data and will work with a faculty in the Department of Animal and Poultry Sciences at Virginia Tech to use machine learning to identify metabolites significantly associated with cultivars that produce monotropein. This work will build on our understanding of how monotropein affects blueberry flavor. This work was tangential to the grant objectives but served to increase our understanding of how biosynthesis of metabolites in blueberries may impact market quality traits.

Publications

  • Type: Peer Reviewed Journal Articles Status: Published Year Published: 2023 Citation: Lawas LMF, Kamileen MO, Buell CR, OConnor SE, Leisner CP (2023) Transcriptome-based identification of genes involved in monotropein biosynthesis and functional characterization of iridoid synthase in blueberry. Plant Direct. 2023;7:e512.