Source: WEST VIRGINIA UNIVERSITY submitted to
DECIPHERING THE CYTOSOLIC CONTRIBUTION TO SHIKIMATE/QUINATE DERIVED METABOLITES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1029732
Grant No.
2023-67013-39021
Cumulative Award Amt.
$650,000.00
Proposal No.
2022-08445
Multistate No.
(N/A)
Project Start Date
Feb 1, 2023
Project End Date
Jan 31, 2026
Grant Year
2023
Program Code
[A1103]- Foundational Knowledge of Plant Products
Recipient Organization
WEST VIRGINIA UNIVERSITY
886 CHESTNUT RIDGE RD RM 202
MORGANTOWN,WV 26505-2742
Performing Department
(N/A)
Non Technical Summary
The intermediates and immediate end-products of the shikimate pathway serve in plants as precursors to thousands of compounds with agronomic, nutritional, and industrial relevance. A complete set of enzymes necessary for the shikimate pathway is known to be located in the subcellular compartment known as the plastid. Whilethis compartment is generally accepted as the sole site of synthesis of shikimate pathway products, it is necessary for plant cells to maintain pools of the key intermediate shikimate and the closely related compound quinate outside of the plastids for the production of several major metabolites. This apparent contradiction in our current understanding of plant metabolism prevents effective targeting of enhanced production of valuable shikimate pathway-derived phytochemicals via either traditional breeding or bioengineering strategies.We have identified a DHDSDHenzymewith apparent extra-plastidial localization that may help resolve this apparent contradiction in our current understanding of plant metabolism. We willusea combination of in vitro biochemistry, reverse genetics, and metabolic analysis to explore the link between different DHDSDH isoforms and downstream phytochemicals that influence food quality and/or have agronomic and industrial relevance. Using tomato and beet as our experimental systems, we will determine the biochemical properties and verify the subcellular localization of DHDSDH enzymes, including those presumed to be cytosolic, thereby determining the metabolic potential of these enzymes. This will be complemented by examining the real in planta impact of alternative DHDSDH isoforms in tomatoand beet, including determining whether the metabolic roles of these isozymes may be integrated with a more complete cytosolic shikimate pathway, as posited nearly four decades ago. This will involve the creation of genetically modified plants in which the levels of these enzymes have been altered and measuring the impact of these alterations on shikimate pathway intermediates and products, including several chemicals that confer desirable characteristics on crop species.Results generated from this work will impact our fundamental understanding of phytochemical metabolism, providing targets for future development of enhanced crop varieties. This is expected to ultimately facilitate develop of crops with better resistance to pests and abiotic stresses, improved nutritional value, and flavors and colors that are more desireable to consumers. Due to the industrial potential of many shikimate pathway-derived compounds as lubricants, plastic alternatives, and fuels, this research will also build on existing groundwork intended to develop plant-based platforms for sustainable production of petrochemical replacements as society moves towards the goal ofpost-petroleum lifestyles.
Animal Health Component
0%
Research Effort Categories
Basic
100%
Applied
0%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2061460100070%
2061499100030%
Goals / Objectives
Goal 1:Fully biochemically characterize the DHDSDH isoforms from Arabidopsis, tomato, and beetObjective 1.1:Determine the full sequence of all transcripts of beet BvDHDSDH2Objective 1.2:Biochemically characterize DHDSDH isoformsObjective 1.3:Determine subcellular localization of DHDSDH isoformsGoal 2: Determine the in planta metabolic role of cytosolic DHDSDH isoforms using reverse genetic strategiesObjective 2.1: Determing metabolic impact of SlDHDSDH2 loss of functionObjective 2.2: Determine contribution of SlDHDSDH2 to plant herbivory resistanceObjective 2.3: Assess gain of function in a type-b-negative species3) Assess the non-canonical beet DHDSDH contribution to betalain metabolismObjective 3.1:Analyze DHDSDH gene expression in beetObjective 3.2: Test loss of function of BvDHDSDH isoforms
Project Methods
Objective 1To determine the full-length protein coding sequence(s) of any and all BvDHDSDH2 transcripts, we will perform 5'- and 3'-RNA Ligase Mediated-Rapid Amplification of cDNA Ends (RLM-RACE) on the encoding gene using the standard protocols developed for the GeneRacer kit (Invitrogen). Briefly, total RNA will be extracted from beet seedlings and an RNA oligonucleotide will be selectively ligated to the 5'-ends of uncapped mRNAs. Subsequent, the full-length mRNAs, including the ligated oligonucleotide, will be reverse transcribed, and the resulting cDNA will be subject to PCR amplification of the 5'- and 3'- ends of the BvDHDSDH2 cDNA using gene-specific primers in conjunction with the GeneRacer 5' (homologous to the RNA oligonucleotide) and 3' (homologous to the oligo dT reverse transcription primer) primers, respectively, and a proofreading DNA polymerase. Amplicons will be gel purified and cloned using the Zero Blunt TOPO cloning kit.The coding sequences of AtDHDSDH and all transcript variants of BvDHDSDH2 will be cloned into the E coli expression vector pET32a, as has already been done for all tomato DHDSDHs. The constructs will be used for recombinant expression of all proteins using Rosetta 2 (DE3) E coli. Proteins will be purified by IMAC chromatography and the fusion tag will be cleaved by enterokinase digestion to leave the native protein. All purified recombinant proteins will be assayed for DHD, QDT, SDH, and QDH activities. Conditions will be optimized (i.e. buffer composition, ionic strength, metal cofactors) to maximize activity within the constraints of maintaining physiological relevance.The open reading frames of all DHDSDH genes characterized above will be cloned into pK7WGF2 and pK7FWG2 with and without, respectively, the genes' native stop codons, toallow for strong plant expression of the proteins with green fluorescence protein fused to the N- or C- terminus, respectively. The expression constructs will be agro-infiltrated into Nicotiana benthamiana leaves following an standard protocols. Subcellular distribution of GFP fluorescence will be observed by confocal microscopy using chlorophyll autofluorescence as a plastidial marker.Objective 2SlDHDSDH2 and SlCM2 null mutants will be created by transforming tomato cotyledons using a standard protocol for agrobacterium-mediated transformation.Plantlets will be regenerated under kanamycin selection. Regenerated shoots that are successfully rooted will be screened for CRISPR/Cas9-induced mutations by PCR amplification of the respective genes from genomic DNA and subsequent Sanger sequencing. A SlDHDSDH2/CM2 double mutant will subsequently be generated by crossing a confirmed null mutant for each of the two genes.We will conduct targeted metabolic analysis in both fruits and vegetative tissues of all transgenic lines.To directly test for a roll of SlDHDSDH2 in sustaining synthesis of aromatic amino acids in the cytosol, we will measure total Phe, Tyr, and Trp levels. We will directly measure shikimate, quinate, and chlorogenic acid in mutants using established HPLC based methods. We will use a previously described LC-MS/MS method to simultaneously measure the organic acids, aldehydes, and alcohols of the phenylpropanoid network, as well as the coumaroyl and caffeoyl shikimate esters.Additionally, we will measure anthocyanin and condensed tannin levels.To assess herbivory impacts, we will perform no-choice feeding assays using the wildtype and mutant tomato lines.Briefly, tobacco hornworm larvae will be allowed to feed on the plants, and hornworm mass gain and development speed will be monitored.To assess gain-of-function,we have already used a construct that overexpresses SlDHDSDH2 under the control of the CMV 35s promoter to transform two genetic backgrounds of Arabidopsis: wild-type Columbia and a CM2 null mutant.The BASTA-resistance phenotype will be used to ensure segregation consistent with single-copy insertion and ultimately for selection of homozygous transformants in the T3 generation. Expression will be assessed qRT-PCRwith biological replication in the homozygous T3 plants. Homozygous lines will be used toanalyze shikimate, quinate, and the three AAAs, as well as intermediates and products of the general phenylpropanoid pathway, including monolignols, anthocyanins, and tannins, as described above.Objective 3We will collect root peel, root flesh, hypocotyls, leaf petioles, and leaf lamina from greenhouse-grown beet plants (inbred line W357B), with a minimum of five biological replicates per tissue. Each tissue will be analyzed by qRT-PCR for expression of both BvDHDSDH1 and BvDHDSDH2. If 5'-RLM-RACE experimentsreveal the presence of multiple transcripts of BvDHDSDH2, we will utilize separate primer pairs specific to each transcript in order to determine expression of each transcript variant individually.As a positive control, we will also measure expression of genes known to be involved in betalain production, including ADHα, ADHβ, MYB1, DODAα, and BvCYPAD1α (36). Finally, expression of the single beet CM2 homolog (BvCM2, XP_019102621), shown in other species to be involved in a cytosolic post-chorismate pathway for production of AAAs, will also be measured to further examine the possibility of a cytosolic contribution to synthesis of the betalain precursor Tyr. All tissues will also be analyzed for content of betalain pigments by a spectrophotometric method, and for Tyr via an HPLC-based method.If the unique biochemistry of BvDHDSDH2 enables high production of betalains, we expect expression to correlated with betalain content and with genes previously shown to facilitate betalain production in beet roots.We will pursue an RNAi strategy to downregulate expression of BvDHDSDH2 in beets. We will create an RNAi hairpin constructs in the Gateway destination vector pH7GWIWG2(II). The hairpin will target nucleotides 480-780 and the corresponding nucleotides (528-828) of the predicted full lengther BvDHDSDH1 and BvDHDSDH2, respectively, full-length coding sequences.The final RNAi constructs will used to transform beet via an established agrobacterium-mediated protocol shown to be efficient across multiple beet cultivars. For each construct, the three lines showing the greatest, specific repression of the target gene's expression will be propagated by seed and used in downstream analyses.Roots and leaves of transgenic plants and non-transformed controls will be used in metabolic analyses. Betalain pigments will be measured spectrophotometrically as described above. Tyr, as well as Phe, Trp, and shikimate, will be measured by HPLC as described above.If a metabolic effect is observed upon RNAi suppression of either DHDSDH isoform, we will perform genetic complementation experiments in that background. Synthetic, recoded sequences of the open reading frames of all DHDSDH isoforms, including any alternative transcripts identified for BvDHDSDH2, will produced by Twist Bioscience. The synthetic genes will be subcloned into pB2GW7 to drive expression of the proteins under the control of the strong constitutive CMV p35s promoter. Intact leaves from RNAi beet lines will be transiently infiltrated with agrobacterium strains carrying the pB2GW7 constructs or a control empty vector , and change in betalain levels will be monitored as described above.

Progress 02/01/23 to 07/22/24

Outputs
Target Audience:Plant scientists, especially those working in the field of amino acid metabolism, plant secondary metabolism, and crop production. Plant breeders, whether working in an academic or industrial capacity. Synthetic biologists, who may wish to incorporate the newfound knowledge into strategies for production of value-added phytochemicals Changes/Problems:In response to budget shortfalls, West Virginia University opted to terminate the position of PD Lynch as part of a large-scale layoff. Downstream impacts of this decision include the university opting to rescind the employment offer of the postdoctoral researcher intended to work on this project, and a PhD student mentored by the PD opting to transfer to another institution. Undergraduate students participating in the research all graduated by May 2024 or transferred to other labs. No students or postdoctoral researchers were replaced due to a lack of supervisor positions associated with this project. Thus, all personnel associated with this project have left the university. What opportunities for training and professional development has the project provided?The project provided four undergraduate students with the opportunity to participate in an active research lab. This has not only given them hands-on research experience with direct mentorship, their training also involved science communication, as students were able to present their work through poster presentations at institutional and regional conferences. This training and professional development has enabled two undergraduate students to enter graduate programs, and another to enter the STEM workforce.The project has also provided one PhD student with the opportunity to participate in an active research lab. In addition to provding hands on research experience and making progress towards their degree, this student has been provided theopportunity to mentor undergraduate students How have the results been disseminated to communities of interest?Results from research performed were presented at the 2023 Gordon Conference on Enzymes, Coenzymes, and Metabolic Pathways, the 2023 and 2024 ASPB Midwest Section Annual meeting, multiple WVU research symposia, and at six invited seminar talks at research institutions What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Objective 1.1 - As proposed, the full-length sequences of the beet BvDHDSDH2 isoforms was determined at both the nucleotide and the protein level. This work for the first time demonstrates experimentally that the BvDHDSDH2 enzyme exists in two differnt forms with two different lengths. Unexpectedly, the shorter isoform is truncated relative to model predictions, leading to a protein with domains for only one enzymatic activity rather than two. This provides the basis for better understanding the underlying mechanisms by which beets are are to sustain pigment production. This subobjective is fully completed. Objective 1.2 - Biochemical characterization requires recombinant expression and purification of the target enzymes, followed by in vitro enzyme assays under carefully controlled condition. During the project, the genes were cloned and the proteins expressed and purified. These enzymes are now ready to be assayed. Objective 1.3 - The genes encoding the beet DHDSDH isoforms were subcloned into the appropriate vectors for fusion with fluorescent tags to enable live-cell imaging. Imaging was performed and the subcellular localizations determined. Objective 2.1 - The determination of the metabolic impact requires generation of stable transgenic lines with the target genes knocked out and/or expression knocked down. We have initiated generation of these transgenic lines. Existing protocols for generation of transgenic tomato resulted in poor rates of shoot and root re-generation from callus under the conditions present at WVU facilities. We have sucessfully optimized this process to increase re-generation rates and have confirmedsuccessful gene modification of the target genes. Generated transgenic lines are available for analysis of the metabolic and physiological impact Objective 2.2 - Nothing to report under this subobjective. Objective 2.3 - Preliminary metabolic analyses were performed on the generated transgenic plant lines for this objective. These preliminary analyses provide the basis for more comprehensive analyses in the future. Objective 3.1 - As proposed, we determined gene expression for the beet DHDSDH isoforms across multiple beet tissues and assessed the correlation with abundance of betalain pigments, as well as genes known to be involved in betalain pigment biosynthesis and cytosolic aromatic amino acid production. This work provides information about fundamental plant function that can be leveraged for enhanced production of phytochemicals generally speaking, and more specifically in modulating production of betalain pigments in beets, an important US crop species. This subobjective is fully complete. Objective 3.2 - As proposed, the determination of the metabolic impact requires generation of stable transgenic lines with the target genes knocked out and/or expression knocked down. We have initiated generation of these transgenic lines following established protocols. Our initial efforts have demonstrated successful tissue regeneration.

Publications

  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2024 Citation: Smith, Taylor, and Joseph H Lynch. "Testing of a metabolic engineering strategy to increase phenylalanine in plants." Oral presentation at Davis College Student Research and Creative Scholars Day, Morgantown, WV. (1st place, Undergraduate Oral Presentation)
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2024 Citation: Smith, Taylor, and Joseph H Lynch. "Testing of a metabolic engineering strategy to increase phenylalanine in plants." Poster presentation at ASPB Plant Biology 2024 meeting, Honolulu, HI.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2024 Citation: Smith, Taylor, and Joseph H Lynch. "Testing of a metabolic engineering strategy to increase phenylalanine in plants." Poster presentation at ASPB Midwest Section 2024 meeting, West Lafayette, IN.
  • Type: Other Status: Accepted Year Published: 2024 Citation: Lynch, Joseph H. "New Horizons in Plant Shikimate Metabolism." Seminar presentation at Clemson University Department of Genetics and Biochemistry.
  • Type: Other Status: Accepted Year Published: 2024 Citation: Lynch, Joseph H. "New Horizons in Plant Shikimate Metabolism." Seminar presentation at Northern Arizona University Department of Chemistry and Biochemistry.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2024 Citation: Choudhary, Monika, and Joseph H Lynch. "Study of the in planta metabolic role of putative cytosolic ncADH in tomato." Poster presentation at ASPB Midwest Secion 2024 Meeting, West Lafayette, IN.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2024 Citation: Choudhary, Monika, and Joseph H Lynch. "Study of the in planta metabolic role of putative cytosolic ncADH in tomato." Poster presentation at Davis College Student Research and Creative Scholars Day, Morgantown, WV.
  • Type: Other Status: Accepted Year Published: 2024 Citation: Lynch, Joseph H. "New Horizons in Plant Shikimate Metabolism." MizzouForward Keynote address and University of Missouri, Columbia, MO.
  • Type: Other Status: Accepted Year Published: 2024 Citation: Lynch, Joseph H. "New Horizons in Plant Shikimate Metabolism." Seminar presentation at Oklahoma State University Department of Plant Biology, Ecology, and Evolution.


Progress 02/01/23 to 01/31/24

Outputs
Target Audience:Plant Scientists- Results from research performed were presented at the 2023 Gordon Conference on Enzymes, Coenzymes, and Metabolic Pathways, the ASPB Midwest Section Annual meeting, two WVU research symposia, and at two invited seminar talks at research institutions. Changes/Problems:PROBLEMS FACED Delays in Institutional Processing- Due to staffing shortages in the WVU Office of Sponsored Programs, institutional setup of the grant was delayed and this resulted in a delay in the availability of funds to the investigators. This resulted in delays in initiating the work as well as in hiring activities, creating delays relative to the proposed timeline. This is not expected to impact the overall accomplishments of work performed under this project Delays due to staffing challenges- During 2023, WVU undertook an institutional transformation. This process and the associated institutional instability inhibitted the ability to recruit a graduate student to assist in performing the proposed work. In addition, while a postdoctoral researcher was hired to work on this project, his offer was retracted by WVU prior to his start date due the impacts of the institutional transformation process. This has resulted in delays in performing work relative to the proposed timeline. These staffing shortages are anticipated to be addressed in the coming year, and therefore this is not expect to impact the overall accomplishments of the work performed under this project. What opportunities for training and professional development has the project provided?The project has provided two undergraduate students with the opportunity to participate in an active research lab. This has not only given them hands-on research experience with direct mentorship, their training also involved science communication, as both students were able to present their work through poster presentations at institutional and regional conferences. This training and professional development has enabled one student to get a The project has also provided one PhD student with the opportunity to participate in an active research lab. In addition to provding hands on research experience and making progress towards their degree, this student has been provided the opportunity to mentor undergraduate students. How have the results been disseminated to communities of interest?Results from research performed were presented at the 2023 Gordon Conference on Enzymes, Coenzymes, and Metabolic Pathways, the ASPB Midwest Section Annual meeting, two WVU research symposia, and at two invited seminar talks at research institutions. What do you plan to do during the next reporting period to accomplish the goals?Objective 1.2- We will continue to perform in vitro enzyme assays to establish the kinetic properties of all the enzymes of interest. Objective 1.3- We will extend the work already performed on beet enzymes to the enzymes in other species of interest, following the same procedures Objective 2.1- We will continue the process of generating transgenic tomato lines, incorporating the optimization that was established during the prior reporting year. We will continue to screen regenerated lines to identify lines with appropriate incorporation of the genetic modifications. Finally, we will initate physiological and metabolic analysis of the identified transgenic lines to determine the impact of the reverse genetic modifications. Objective 2.2- Per the project timeline, experiments under this sub-objective will begin in year three of the project. Objective 2.3- Will will continue metabolic analysis on the transgenic plants. Objective 3.2-We will continue the process of generating transgenic beet lines. We will screen regenerated lines to identify lines with appropriate incorporation of the genetic modifications and downregulation of the target genes. Finally, as lines with appropriate downregulation of the target genes are identified, we will perform preliminary metabolic analyses to assess the contribution of the modified genes toward aromatic amino acid and pigment production.

Impacts
What was accomplished under these goals? Objective 1.1 -As proposed, the full-length sequences of the beet BvDHDSDH2 isoforms was determined at both the nucleotide and the protein level. This work for the first time demonstrates experimentally that the BvDHDSDH2 enzyme exists in two differnt forms with two different lengths. Unexpectedly, the shorter isoform is truncated relative to model predictions, leading to a protein with domains for only one enzymatic activity rather than two. This provides the basis for better understanding the underlying mechanisms by which beets are are to sustain pigment production. This subobjective is fully completed. Objective 1.2- Biochemical characterization requires recombinant expression and purification of the target enzymes, followed by in vitro enzyme assays under carefully controlled condition. During this reporting period the genes were cloned and the proteins expressed and purified. These enzymes are now ready to be assayed. Objective 1.3- During this reporting period, the genes encoding the beet DHDSDH isoforms were subcloned into the appropriate vectors for fusion with fluorescent tags to enable live-cell imaging. Imaging was performed and the subcellular localizations determined. Work is ongoing on performing such localization experiments with proteins from other species. Objective 2.1- As proposed, the determination of the metabolic impact requires generation of stable transgenic lines with the target genes knocked out and/or expression knocked down. We have initiated generation of these transgenic lines. Existing protocols for generation of transgenic tomato resulted in poor rates of shoot and root re-generation from callus under the conditions present at WVU facilities. We have sucessfully optimized this process to increase re-generation rates and continue work towards confirming successful gene modification of the target genes. Generated transgenic lines will be utilize for analysis of the metabolic and physiological impact in future reporting periods. Objective 2.2- Nothing to report in this reporting period under this subobjective. Objective 2.3- Preliminary metabolic analyses were performed on the generated transgenic plant lines for this objective. These preliminary analyses provide the basis for more comprehensive analyses to be completed during future reporting periods. Objective 3.1- As proposed, we determined gene expression for the beet DHDSDH isoforms across multiple beet tissues and assessed the correlation with abundance of betalain pigments, as well as genes known to be involved in betalain pigment biosynthesis and cytosolic aromatic amino acid production. Our results revealed that, contrary to our working hypothesis, BvDHDSDH2 is unlikely to be directly involved in betalain pigment production but is instead likely responsible for ensuring sufficient baseline production of aromatic amino acids for general plant function in species with high rates of tyrosine consumption. This work provides information about fundamental plant function that can be leveraged for enhanced production of phytochemicals generally speaking, and more specifically in modulatingproduction of betalain pigments in beets, an important US crop species. This subobjective is fully complete. Objective 3.2 -As proposed, the determination of the metabolic impact requires generation of stable transgenic lines with the target genes knocked out and/or expression knocked down. We have initiated generation of these transgenic lines following established protocols. Our initial efforts have demonstrated successful tissue regeneration.Generated transgenic lines will be utilized for analysis of the metabolic and physiological impact in future reporting periods.

Publications

  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Smith, Taylor, and Joseph H Lynch. "Testing of a metabolic engineering strategy to increase phenylalanine in petunia." Poster presentation at ASPB Midwest Section 2023 Meeting.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Smith, Taylor, and Joseph H Lynch. "Testing of a metabolic engineering strategy to increase phenylalanine in petunia." Poster presentation at WVU Summer 2023 Symposium.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Roth, Haley, Monika Choudhary, and Joseph H Lynch. "Identifying and Characterizing Functionality of DHDSDH Isoforms in the Production of Phenylalanine." Poster presentation of WVU Summer 2023 Symposium.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Choudhary, Monika, Haley Roth, and Joseph H Lynch. "Specialized roles of plant DHDSDH isoforms in production of downstream metabolites in plants." Poster presentation at Gordon Research Conference on Enzymes, Coenzymes and Metabolic Pathways.
  • Type: Other Status: Other Year Published: 2024 Citation: Lynch, Joseph H. "New Horizons in Plant Shikimate Metabolism." Seminar presentation at East Carolina University Department of Biology.
  • Type: Other Status: Other Year Published: 2024 Citation: Lynch, Joseph H. "New Horizons in Plant Metabolism." Seminar presentation at Marshall University Department of Biomedical Sciences.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Smith, Taylor, and Joseph H Lynch "Testing of a metabolic engineering strategy in plants." Poster presentation at WVU Davis College Graduate Research & Creative Scholarship Day.