Source: UNIVERSITY OF CHICAGO submitted to NRP
INVESTIGATION OF THE INTERACTIONS OF PAMPS AND DAMPS, NAMELY FLG22 AND PHYTOSULFOKINE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1026429
Grant No.
2021-67034-35167
Cumulative Award Amt.
$180,000.00
Proposal No.
2020-09991
Multistate No.
(N/A)
Project Start Date
Jul 1, 2021
Project End Date
Jun 30, 2024
Grant Year
2021
Program Code
[A7101]- AFRI Predoctoral Fellowships
Recipient Organization
UNIVERSITY OF CHICAGO
5801 SOUTH ELLIS AVE.
CHICAGO,IL 60637
Performing Department
Mol Gen/Cell Bio
Non Technical Summary
The first layer of innate immunity in plants involves perception of pathogen associated molecular patterns (PAMPs) by cell surface receptors, including FLS2, a receptor for a fragment (flg22 ) of bacterial flagellin. The purpose of this study is to determine the potential crosstalk between the PAMP response triggered by flg22 and the plant peptide phytosulfokine (PSK). There is a known interaction these two signaling pathways, but the mechanism is not clear. Specifically, I want to know the following: (1) Does PSK/PSKR affect the internalization of flg22/FLS2? (2) How are the spatial temporal dynamics of flg22/FLS2 influenced by PSK and its receptors (PSKR)? (3) Is the downstream signaling of flg22/FLS2 affected by PSK/PSKR? To answer these questions I will use a variety of mutants and microscopy techniques (TIRF & confocal) as well as radiolabeling to track the distal movement of functional labeled peptides. Biosensors will be used to monitor levels of cGMP and calcium produced in mutant plants in response to ligands. I will look at the functional interactions between flg22 and PSK pathways in Arabidopsis and in a crop plant (rice). This study offers a means of understanding how an immune signaling network is modulated by PAMPs and plant signaling peptides. With high applicability to other plant species, the system presented here could be applied to other systems and provide knowledge of different pathways that could hence be optimized for agriculture.
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
20624991090100%
Knowledge Area
206 - Basic Plant Biology;

Subject Of Investigation
2499 - Plant research, general;

Field Of Science
1090 - Immunology;
Goals / Objectives
The first layer of innate immunity in plants involves perception of pathogen associated molecular patterns (PAMPs) by cell surface receptors, including FLS2, a receptor for a fragment (flg22 ) of bacterial flagellin. The purpose of this study is to determine the potential crosstalk between the PAMP response triggered by flg22 and the plant peptide phytosulfokine (PSK). There is a known interaction these two signaling pathways, but the mechanism is not clear. Specifically, this project will address the following:(1) Deterrmine if PSK/PSKR affects the internalization of flg22/FLS2?A. Investigate the impacts of PSK/PSKR on flg22 using total internal reflection fluorescence microscopy.B. Investigate the longer-range, organ wide trafficking of both PSK and flg22 determine whether flg22 movement/trafficking is affected by PSK/PSKR, and whether PSK shows any cell to cell movement like flg22.(2) Determine if the spatial temporal dynamics of flg22/FLS2 are influenced by PSK and its receptors (PSKR).A. Determine if PSKR impacts the flg22 pathway in a manner similar to PEPR, except that it may dampen the immune response instead of amplify it since loss of PSKR enhances flg22 responses.
Project Methods
Experimental MethodsAim 1:To understand when and where PSK influences flg22 signaling, I will start by investigating potential effects in RME. I will use total internal reflection fluorescence (TIRF) and single particle trafficking to study the trafficking of the PSK and flg22 receptor-ligand complexes. I will investigate the interaction of PSK and flg22 in the Arabidopsis root tips. I will use tpst mutant lines to have more control over the PSK signaling pathway, since the only PSK present will be what I add to the system. The TIRF experiments will deploy departure assays for clathrin-mediated endocytosis from Johnson and Vert. This assay relies on dual TIRF imagining and creating a clathrin trace utilizing clathrin light chain with a GFP or RFP tag to create a reference trace for the internalization of different proteins. I will use dual channel time-lapse movies recorded sequentially. Thus, I will visually investigate one peptide at a time. I will apply both PSK and flg22 peptides: 1 with a fluorescent and without a fluorescent label, to track the internalization of each peptide. I will use the following combinations: scrambled flg22 with PSK-TAMRA, flg22 with PSK-TAMRA, nsPSK with FAM-flg22, PSK with FAM-flg22. I will analyze movies using the cmeAnalysis package in MatLab 2013b and using the custom scripts written by Johnson and Vert to determine internalization and trafficking patterns of the peptides.I expect to find a relationship between flg22 and PSK endocytic pathways, or a time dependency between the two given the fact that the two peptides trigger the creation of complexes with so many of the same membrane bound proteins and PSK signaling was inferred to affect flg22 root growth inhibition,The second goal of this objective is to investigate the longer range, organ-wide trafficking of both PSK and flg22, to determine whether flg22 movement/trafficking is affected by PSK/PSKR, and whether PSK shows any cell to cell movement like flg22. I will apply one or both fluorescently labeled PSK-TAMRA and flg22-FAM to the adaxial side of leaves of tpst plants and conduct time courses (using confocal microscopy) to determine if PSK-TAMRA/flg22-FAM are detected on the abaxial side. This will show if flg22 movement is affected by PSK and vice versa. I will use nsPSK and scrambled flg22 for nonfunctional control peptides. I will use tpst/pskr1, tpst/fls2 and tpst/pskr1/fls2 as control plants with one or more of the receptors missing and no competing endogenous PSK. I will test also for distal movement in the plant, orthostichous leaves, the stem, and roots by monitoring TAMRA and FAM fluorescence to see if there is colocalization of PSK and flg22 or if one peptide affects the pattern of movement of the other. As a complimentary method, I will apply radiolabeled peptides and use plant autoradiography to monitor changes in the pattern of the movement of flg22 in response to the addition of PSK. Peptide stability will be assessed via gel electrophoresis. Results will be analyzed using imageJ and the outputs will be reported as percent colocalization. To test the functional effect of PSK on long range trafficking of flg22, I will test if the magnitude of systemic immunity to P. syringae (assayed by pathogen growth) induced by a local flg22 treatment is affected by a prior local PSK treatment, using methods standard in our lab.Aim 2:I hypothesize that PSKR impacts the flg22 pathway in a manner similar to PEPR, except that it may dampen the immune response instead of amplify it since loss of PSKR enhances flg22 responses. First, I will investigate the potential impact that the PSKR/PSK pathway has on the cytosolic production of cGMP by monitoring the influx of calcium into the cytoplasm resulting from the flg22/FLS2 activation. After various peptide treatments, I will measure cytosol localized calcium dependent protein aequorin, which is also chemiluminescent, using the protocol from Qi et al.25 I will also investigate the cGMP production from the various CNGCs associated with PSK/PSKR and flg22/FLS2 (CNGC17 and CNGC2, respectively). I will use the FlincG27 biosensor to measure the in planta changes to cGMP in the response of tpst plants to PSK, flg22, nsPSK, and scrambled-PSK. I will replicate this experiment in rice using transiently transformed plant lines. Carbon nanofibers, which I have developed as part of my graduate work, will be used to deliver FlincG or aequorin expression plasmids. I will assay leaves and roots to determine if there is a difference between organs. I will identify potential genes whose expression pattern changes after calcium is released into the cytoplasm through CNGC channels (early and late responses of PSK/PSKR on flg22/FLS2 signaling cascade). I will use R-studio to mine (a) transcriptional profiling data obtained with tpst mutants treated with PSK and nsPSK by Dian Liu, a graduate student in the Greenberg lab, and (b) data from the literature investigating the transcriptional profiling of flg22/FLS2 signaling in both Arabidopsis and rice plants. Dian is investigating the early and late responses to PSK without an induced immune response. Additionally, there are published RNA-seq results of Arabidopsis exposed to flg22. Highly expressed genes from early and late responses induced by PSK and flg22, respectively that I will confirm with qRT-PCR. Lastly, I will test their expression upon treatment with PSK and flg22, separate and together, and in pskr1 and fls2 plants to test which genes are affected by the presence of one or more ligands.Production of the Carbon NanofibersCarbon based nanofibers with a lateral spacing (pitch) of 10 or 35 μm were made in the Center for Nanophase Material Science at Oak Ridge National Lab using nickel catalyst dots across the top of a silicon wafer via electron beam lithography, metal evaporation, and conventional lift-off using the method described by (Melechko et al., 2009). For the lithography step, the silicon wafers were coated with PMMA resist and exposed using a JEOL 9300FS electron beam lithography system and developed in a solution of xylene:isopropyl alcohol. Electron beam lithography is necessary to define the catalyst dots with diameters between 200 nm and 500 nm. After developing the resist and cleaning with a 6-second exposure to oxygen plasma, electron beam evaporation was used to deposit a thin nickel film on the patterned resist. Sequential sonication in acetone and isopropyl alcohol is used to remove the underlying resist layer, leaving catalyst dots in the desired pattern behind. Nanofiber growth was then conducted using a plasma-enhanced chemical vapor deposition chamber (PEVCD) using an acetylene/ammonia mixture. PECVD growth parameters were optimized to control the length and taper of the nanofibers. After fabricating the VACNFs, their geometry was assessed using scanning electron microscopy.EffortsThe results from this work will be presented in classroom and outreach activities conducted by the PD Jessica Morgan and the mentor Dr. Jean Greenberg.EvaluationTo work towards the goals of the project, I will confer with my primary and collaborative mentors bi-weekly to discuss my current progress. I will attend conferences annually to give progress updates and receive feedback from the community, write progress reports for theUSDA and meet with my thesis committee to evaluate my progress and provide feedback.TimelineY1: Analyze RNA-seq data from Dian Liu and literature. Complete TIRF experiments and singleparticle tracking analysis for Aim 1, write and submit paper. Gather materials for project.Y2: Complete experiments for Aim 1. Perform experiments in aim 2, specifically investigate calciumand cGMP production and other studies with Arabidopsis and rice, write and submit paper.Y3: Finish experiments/writing that may be interrupted by COVID-19.

Progress 07/01/21 to 06/29/23

Outputs
Target Audience:The target audience of this grant were those working in the fields of plant biology. This includes both farmers, scientists, undergraduates, and other members of the project. The aim is to target audiences interested in understanding how plants respond to pathogens and how to use nanomaterials as a means of delivery. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project provided me with the opportunity to work with scientists at Oak Ridge Naiontal Laboratory to work in their clean room facility to create nanomaterials that could be utilized for delivery in plants. How have the results been disseminated to communities of interest?The results have been disseminated to communities of interest through the form of publications. In the past year I have submitted two scientifitc papers, one paper is published and the other is currently in progress. Additionally, I wrote my dissertation and gave a thesis defense where I discussed the work that I had completed while working on my PhD. The paper that is open is currently published is open-access so that anyone can read it. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? In the last year of the project, no progress was made under the first major goal of the progress.All of the experiments performed focused on the goals of the second goal of the project. The second goal of the project was to understand the spatial temporal dynamics of potential crosstalk between the PSK/PSKR and flg22/FLS2 pathways. To this end I performed callose and ROS assays to look at late and early signaling outputs. For the ROS assays I pre-treated plants with PSK for different amounts of time (5 min, 15 min, 30 min, 1 h, 2, 5 h, and overnight) before exposing them to flg22 and measuring ROS as a product of luminescence (using horse radish peroxidase and luminol). For these experimens, different mutants were used, plants lacking tpst (the peptide responsible for sulfating PSK and other peptides) and pskr1/pskr2 mutants, which knocked out the genes encouding for the membrane bound receptors that bind PSK. Shorter periods of pre-exposure did not have any impact on the ROS signal triggered by flg22. Longer pre-treatments of PSK resulted in bigger reductions of ROS signal after flg22 treatment. Additionally, tpst mutants qualitvatitely had larger ROS responses than wildtype and mutants lacking pskr1/pskr2. Callose assays were used to look at later stages of potential cross talk between psk/pskr and fls2/flg22. In this intial experiment, plants were pre-treated with PSK for 24 hours and then treated with flg22 for 24 hours. After both of these treatments, plant samples were fixed and stained such that the callose deposits could be observed microscopically. In this preliminary experiment, the addition of PSK seemed to reduce the number of callose deposits. More experimental replicates are needed to confirm this finding. With this goal of the project, we further developed the utility and application of vertically aligned carbon nanofiber arrays to show that they could be used for delivery in curved plant surfaces and be applied to several different plant species. These results were published inJoVEandFrontiers in Plant Science. Additionally, I started working with Dian Liu to identify marker genes from his RNA seq results that could potentially be used to look at other sources of crosstalk between the two pathways of interest. He will continuing on this since I have graduated.

Publications

  • Type: Journal Articles Status: Published Year Published: 2022 Citation: Morgan, J. M., Jelenska, J., Hensley, D., Retterer, S. T., Morrell-Falvey, J. L., Standaert, R. F., & Greenberg, J. T. (2022). An efficient and broadly applicable method for transient transformation of plants using vertically aligned carbon nanofiber arrays (No. TEXTUAL).
  • Type: Journal Articles Status: Accepted Year Published: 2023 Citation: Morgan, J. M., Jelenska, J., Hensley, D. K., Li, P., Srijanto, B. R., Retterer, S. T., Standaert, R. F., Morrell-Falvey, J. L., Greenberg, J. T. Using Vertically Aligned Carbon Nanofiber Arrays on Rigid or Flexible Substrates for Delivery of Biomolecules and Dyes to Plants. J. Vis. Exp. (Pending Publication), e65602, In-press (2023).
  • Type: Theses/Dissertations Status: Under Review Year Published: 2023 Citation: Morgan, J. (2023). Use of Nanomaterials for Transient Transformation in Plants. University of Chicago. (Under-review).


Progress 07/01/21 to 06/30/22

Outputs
Target Audience:The target audiences reached by my efforts during this reporting period included scientist present at the Plant Molecular Biology Gordon Research Conference through a poster presentation about the project, At this Gordon Research Conference there were graduate students, post-doctoral scholars, professors, and members from industry who were able to hear more about the basis of this project as well as the current status of the research. Changes/Problems:In the first year of the project there were set backs in the completion of the goals of the first year of the project because the project director had a close family member pass away unexpectedly. What opportunities for training and professional development has the project provided?This project has presented the opportunity for the project director to present research findings at the Plant Molecular Biology Gordon Research Conference, in which the project director was able to give a poster presentation. The project director also had the opportunity to train an undergraduate volunteer in the Greenberg lab who were interested in learning basic laboratory techniques. This undergraduate student assisted in generating the first round of genetic crosses necessary for total internal reflection fluorescence assays to investigate potential receptor mediated endocytosis and for other experiments investigated the trafficking patterns of fls2/flg22 and PSKR/PSK. Additionally, the projector director worked with the primary mentor, Dr. Jean Greenberg and the collaborating mentor to submit an application to use the Center for Nanophase Materials Science at Oak Ridge National Laboratory to produce more vertically aligned carbon nanofibers and to transfer these fibers to a flexible substrate. This user proposal was accepted and the project director traveled to Oak Ridge National laboratory in October 2021 and January 2022 to produce more fibers to aid in investigating potential crosstalk between PAMPS and DAMPS after internalization. ? How have the results been disseminated to communities of interest?The project director volunteered as a mentor to middle school students at Lowell Middle School in Lowell Massachusetts. The project director discussed the pathway to becoming an academic researcher and shared information about the current project funded under the USDA NIFA RFA project. The results of this research have also been presented at the Plant Molecular Biology Gordon Research Conference and Seminar and presented in lab meetings as well as collaboration meetings with both of the mentors. ? What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period the plan is to finish genotyping and propagating the required plant lines for investigating the trafficking patterns of PSK/PSKR and flg22/FLS2 specific to the first goal of the project. Additionally, work will be done to investigate how PSK/PSKR affect the trafficking patterns of flg22/fls and vice versa using confocal and total internal reflection microscopy. The project director will analyze RNA-seq data from Dian Liu and the literature. Furthermore, studies will be continued to investigate cGMP and calcium production and how this also influences PSKs attenuation of the flg22 immune response in plants. The project director will also use the experimental methods from Marcec et al., 2021 to perform ROS assays and to measure calcium responses in arabidopsis wild type plants, tpst mutants, and fls2 mutants to investigate how exogenously applied psk affects ROS responses and calcium to exogenously applied flg22. ?

Impacts
What was accomplished under these goals? In the first year of the project the following items were accomplished. In regards to investigating trafficking patterns of psk/pskr and flg22/fls, work was done to begin constructing necessary plant lines for TIRF experiments. Preliminary experiments were conducted using PSK-TAMRA with wildtype (Arabidopsis ecotype Columbia), tpst mutants, pskr1/pskr2 mutants, and fls2 mutants roots of 5-6 day old plants. These plants were grown vertically on ½ MS plates. Roots were exposed to 5-10 uM of PSK-TAMRA for 30 minutes to 2 hours and imaged within 30 minutes post peptide exposure. PSK-TAMRA was observed in both vesicle and vacuolar structures within the roots. Future experiments are needed to determine if the peptide is trafficked from cell to cell in the roots and if this movement is receptor dependent, if the peptide moves between cells without its receptors, and if this movement is influenced by flg22/fls2. Additionally, the project director has been prepping a manuscript for publication for the utility of vertically aligned carbon nanofibers to transiently transform different plant species and organs with various marker genes. These fibers will be utilized for delivering biosensors that can be used for investigating cGMP or calcium. Lastly, work has been started to troubleshoot assays for monitoring changes in ROS and calcium bursts using the protocols from Marcec et al., 2021.

Publications

  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Morgan, J., Jelenska, J., Liu, D., Abakah, B., Standaert, R., Morrell-Falvey, J., and Greenberg,J. (2022, June 11-16). Investigation of the INteractions of PAMPS and DAMPS, Namely FLg22 and Phytosulfokine [Poster presentation]. Plant Molecular Biology Gordon Research Conference. Holderness, NH, United States.