Source: CORNELL UNIVERSITY submitted to NRP
UNDERSTANDING THE ROLE OF INTERCELLULAR COMMUNICATION IN VEGETABLE CROP GRAFTING
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1023059
Grant No.
2020-67011-31882
Cumulative Award Amt.
$180,000.00
Proposal No.
2019-07129
Multistate No.
(N/A)
Project Start Date
Jun 15, 2020
Project End Date
Jun 14, 2023
Grant Year
2020
Program Code
[A7101]- AFRI Predoctoral Fellowships
Recipient Organization
CORNELL UNIVERSITY
(N/A)
ITHACA,NY 14853
Performing Department
Plant Biology
Non Technical Summary
Grafting, the technique of joining two plant parts together, is an ancient technique that is used to propagate plants. Many industries rely on grafting to successfully grow economically significant species, such as apples, where desirable varieties are grafted onto hardy rootstocks. The ability of two different varieties or species to graft is called graft compatibility. While the process of grafting has existed for thousands of years, the mechanisms that underlie graft compatibility remain poorly understood. Due to this, graft compatibility is determined through trial and error. Trial-combinations are not always easily diagnosed as incompatible. A type of graft incompatibility, called delayed incompatibility, occurs when grafts appear to be successful only to fail months or years later. Because woody crops are slow-growing and challenging to use in research, little is known about the molecular basis that leads to graft incompatibility. This project utilizes a non-tree model system: tomato and eggplant grafted as compatible partners and tomato and pepper grafted as incompatible partners. All of these plants are fast growers and easily studied in a research environment.Previous work has shown that compatible grafts require a complex network of molecular and hormonal signaling. This project will investigate the role that these signals play in grafting. We will do this by analyzing known mobile signals and signal transport in both compatible and incompatible grafted plants. We will also assess if necrosis (tissue death) in the graft junction correlates with blocked intercellular transport. Through this project, we aim to advance the understanding of graft biology. A better understanding of graft compatibility will benefit breeders and growers who are negatively affected by the loss of crops during graft incompatibility.
Animal Health Component
10%
Research Effort Categories
Basic
90%
Applied
10%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
20614691020100%
Goals / Objectives
Many tree and vegetable growers rely on grafting to continually propagate essential varieties. While the process of grafting has existed for thousands of years, the mechanisms that underlie graft compatibility remain poorly understood. Due to this, graft compatibility is often tested through a process of trial and error. Trial-combinations are not always easily diagnosed as incompatible. A type of graft incompatibility, called delayed incompatibility, occurs when grafts appear to be successful only to fail months or years later due to failed vascular connections.This project aims to elucidate the mechanisms that determine compatibility, by utilizing the herbaceous model system:Solanum lycopersicum(tomato),Solanum melongena(eggplant), andCapsicum annum(pepper). The broad goal of this project is to investigate the role of intercellular communication in grafted herbaceous plants.The first objective of this project will focus on the timing and importance of symplastic transport at the graft junction by investigating the formation of plasmodesmata.The second objective of this project will determine if mobile signals are transported across the graft junction. This, in combination with our findings regarding plasmodesmata, will provide insight into molecular trafficking across the graft junction.The third objective of this project will investigate how necrosis impacts the intercellular signaling within the graft interface, especially within incompatible grafted plants.These experiments align with the Plant Health and Production and Plant Products program area priority.
Project Methods
Aim 1: Is plasmodesmata formation at the graft junction interface altered in incompatible grafts?Generation of transgenic tomato, eggplant, and pepper with plasmodesmata (PD) fluorescent markers:PDLP5 is a protein that associates with plasmodesmata. Two constructs will be generated for this experiment: pPDLP5::PDLP5-GFP and pPDLP5::PDLP5- RFP. Each of these will be transformed individually into tomato, eggplant, and pepper. Tomato and pepper are known, incompatible graft partners. Tomato and eggplant are known, compatible graft partners. 5-10 lines for each transformation will be grown to the T2 generation for grafting experiments.Grafting as a tool to track the formation of PD at the graft junction:The graft combinations below will be performed: tomato:tomato, pepper:pepper, eggplant:eggplant, tomato:pepper, pepper:tomato, tomato:eggplant, eggplant:tomato. Red and green puncta will indicate half-PD formation, whereas yellow puncta will form when PD-associated proteins colocalize, meaning that whole PD has developed across the junction. No puncta will show a lack of PD at the graft interface. To determine that the marker line has not affected PD formation or the ability of the crops to graft, all transgenic crops will be self-grafted. To quantify the baseline number of PD formed along the graft junction in self-grafted plants, scions with PDLP5-GPF will be grafted to the same genotype expressing PDLP5-RFP. To quantify the formation of interspecies PD along the graft junction in compatible heterografts, tomato expressing PDLP5-GPF will be grafted to eggplant expressing PDLP5-RFP. To quantify the number of interspecies PD formed in incompatible grafts, tomato expressing PDLP5-GPF will be grafted to pepper expressing PDLP5-RFP.Image analysis of graft junctions:Graft junctions will be cut out, 1 cm on either side of the interface daily, for eight days following grafting, and cleared in ClearSee. Samples will be imaged daily using a Zeiss u880 confocal microscope.Image analysis of PD formation: All images will focus on the same cell types and use the same laser settings. Colocalization and imaging analysis will be performed with consistent parameters on ImageJ.Attendance at a scientific conference:This research will be presented at a national or international scientific conference.Aim 2: Are mobile signals required for successful grafts?Generation of transgenic tomato, pepper, and eggplant with markers for mobile signals:Known mobile signals, CLE42 and PEAR1, are present in vascular tissue. Multi-gene constructs will be built using the MoClo system. The constructs will be transformed and grown to the T2 generation in tomato, eggplant, and pepper.Grafting as a tool to track the transcription and movement of mobile signals CLE42 and PEAR1:The graft combinations below will be performed: tomato:tomato, pepper:pepper, eggplant:eggplant, tomato:pepper, pepper:tomato, tomato:eggplant, eggplant:tomato. To determine that the marker line has not affected the ability of the crops to graft and to quantify the baseline levels of gene expression, all transgenic plants will be self-grafted. To determine protein mobility, each transgenic species will be reciprocally grafted with its respective wild type species. To investigate the effect of hetero-grafting, each transgenic line will be reciprocally grafted with each wild type species. One fluorescent reporter will mark the location of expression. The contrasting fluorophore will mark the mobility of the protein. Both of these signals are already known to be mobile and act non-cell autonomously. Thus, we expect to see mobile protein outside of the region of transcription within the parent tissue. The presence of the mobile signal in the wild type plant will show that mobile signals are capable of crossing the graft junction into the grafted partner.Image analysis of graft junction:Graft junctions will be cut out, 1 cm on either side of the interface daily, for eight days following grafting, and cleared in ClearSee. Samples will be imaged daily using a Zeiss u880 confocal microscope.Image analysis of mobile signal transcription and mobility formation:All images will focus on the same region of the stem and use the same laser settings. Colocalization and imaging analysis will be performed with consistent parameters on ImageJ.Attendance at a scientific conference:This research will be presented at a national or international scientific conference.Generation of publication:Aim 1 and aim 2 will be combined to produce a publication describing the role of intercellular signaling on grafting. This effort will advance knowledge for scientists and breeders.Aim 3: Is necrosis a barrier for communication in grafted plants?Grafting incompatible and compatible plants:The following graft combination will be performed with wild type plants. tomato:tomato, pepper:pepper, eggplant:eggplant, tomato:pepper, pepper:tomato, tomato:eggplant, eggplant:tomato.Tissue printing used to trace reactive oxygen species:Cell death is a common symptom of graft incompatibility. Destruction of tissue leads to reactive oxygen species (ROS). ROS are often quantified using DAB stain, which reacts with ROS and forms a brown precipitate. Because DAB stain is unable to penetrate the stem and cutting the tissue would induce a strong peroxidase response, traditional DAB staining cannot be used. To assay the accumulation of ROS in the stem over time, grafted plants will be harvested at seven, fourteen, and twenty-eight days after grafting. Grafted stems will be cut longitudinally and immediately pressed onto DAB soaked nitrocellulose membranes. Ungrafted stems will be cut and pressed as negative controls, and 20 mM of H2O2 will be added to the DAB soaked nitrocellulose membrane as a positive control. Prints will be developed for two minutes and imaged on a flatbed scanner.Image analysis of DAB signal:Images will be quantitatively analyzed in ImageJ to test for statistical differences in the amount of oxidized DAB on each print between compatible and incompatible graft combinations relative to the un-grafted controls.Attendance at a scientific conference:This research will be presented at a national or international scientific conference.Generation of publication:Aim 3 results will be used to produce a publication regarding the effect of grafting on reactive oxygen species. This effort will improve knowledge on graft incompatibility, and hopefully, begin to build a protocol to test for early graft incompatibility.Key milestones:Successful transient fluorescent PD marker linesSuccessful transient mobile signal marker linesGeneration of fluorescent PD marker lines in tomato, pepper, and eggplantGeneration of mobile signal marker lines in tomato, pepper, and eggplantDAB staining completedDAB staining analyzedBegin ROS publicationGraft fluorescent PD lineGraft mobile signal marker linesCollect all graft junctions and imageAnalyze imagesBegin mobiles signal publication

Progress 06/15/20 to 10/24/22

Outputs
Target Audience:My main efforts to deliver thisresearch will be through academic journals and scientific conferences. During the last year, I have been invited to speak at 2 international conferences (Plant Biology 2021 and Plant and Animal Genome 2022) and have written 2 research articles and 1 review which are in the process of being published.Although these media types will mostly reach scientists, they will also reach the true target audience of this project: breeders and growers. Changes/Problems:As mentioned in the previous annual report, significant delays in 2020 affected the progress of Aim 1 and Aim 2, but regardless,all of the proposed transgenic lines were completed. Furthermore, Aim 3 was completed successfully. The most significant change to the proposed project plan is that I graduated one year early and will thus conclude the grant. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?The data generated in the last year will be disseminated in multiple manuscripts, including one currently submitted to the American Journal of Botany. Another research article will be submitted in the next six months. This data was also shared with the broader plant science community through virtual conferences, including Plant Biology 2021 (talk), Plant Animal Genome (2022) (virtual talk), and Plant Vascular Biology this summer (poster). What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? 1. The first objective of this project focused on the timing and importance of symplastic transport at the graft junction by investigating the formation of plasmodesmata. To accomplish aim 1, plasmodesmata-report lines were proposed in tomato. In the last year, a redand green reporter line was generated for the native tomato PDLP5 promoter (pSlPDLP5:PDLP5-tdtomato and pSlPDLP5:PDLP5-eGFP) as well as anoverexpressing red reporter (35S:PDLP5-tdtomato). In addition, an estradiol-inducible plasmodesmata line was generated in tomato. These lines will be utilized for future experiments. 2. The second objective of this project was to determine if mobile signals are transported across the graft junction. This, in combination with our findings regarding plasmodesmata, will provide insight into molecular trafficking across the graft junction. Aim 2 focuses on the mobility of molecules across the graft junction. In order to test this, a transcriptional (pCLE12:tdtomato) and translational reporter (pCLE12:CLE12-eGFP) were generated in tomato. The T1 plants are currently being genotyped. 3. The third objective of this project was to investigate how necrosis impacts the intercellular signaling within the graft interface, especially within incompatible grafted plants. Aim 3 was thoroughly explored in the last year. This was done by conducting a large-scale graft trial between tomato and four pepper varieties. These grafts were all analyzed anatomically via confocal microscopy. TUNEL assays and necrotic staining were performed to determine cell death in these tissues. Furthermore, aRNA-seq timeline was collected over three weeks, tracking the junction of tomato and pepper heterografts. This work will be submitted for publication in the next six months. These experiments aligned with the priority of the Plant Health and Production and Plant Products program.

Publications

  • Type: Journal Articles Status: Submitted Year Published: 2022 Citation: Title: Anatomical and biophysical characterization of intergenic graft-incompatibility within the Solanoideae
  • Type: Theses/Dissertations Status: Accepted Year Published: 2022 Citation: Title: Understanding the genetic processes of grafted vegetable crops


Progress 06/15/21 to 06/14/22

Outputs
Target Audience: My main efforts to deliver this research will be through academic journals and scientific conferences. During the last year, I have been invited to speak at 2 international conferences (Plant Biology 2021 and Plant and Animal Genome 2022) and have written 2 research articles and 1 review, which are in the process of being published. Although these media types willmostly reach scientists, they will also reach the true target audience of this project: breeders and growers. Changes/Problems: As mentioned in the previous annual report, significant delays in 2020 affected the progress of Aim 1 and Aim 2, but regardless, all of the proposed transgenic lines were completed. Furthermore, Aim 3 was completed successfully. The most significant change to the proposed project plan is that I graduated one year early and will thus conclude the grant. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest? The data generated in the last year will be disseminated in multiple manuscripts, including one currently submitted to the American Journal of Botany. Another research article will be submitted in the next six months. This data was also shared with the broader plant science community through virtual conferences, including Plant Biology 2021 (talk), Plant Animal Genome (2022) (virtual talk), and Plant Vascular Biology this summer (poster). What do you plan to do during the next reporting period to accomplish the goals?I graduate in May 2022, thus concluding this grant. I will continue to finalize manuscripts and publish the work from this project.

Impacts
What was accomplished under these goals? 1. The first objective of this project focused on the timing and importance of symplastic transport at the graft junction by investigating the formation of plasmodesmata. To accomplish aim 1, plasmodesmata-report lines were proposed in tomato. In the last year, a red and green reporter line was generated for the native tomato PDLP5 promoter (pSlPDLP5:PDLP5-tdtomato and pSlPDLP5:PDLP5-eGFP) as well as an overexpressing red reporter (35S:PDLP5-tdtomato). In addition, an estradiol-inducible plasmodesmata line was generated in tomato. These lines will be utilized for future experiments. 2. The second objective of this project was to determine if mobile signals are transported across the graft junction. This, in combination with our findings regarding plasmodesmata, will provide insight into molecular trafficking across the graft junction. Aim 2 focuses on the mobility of molecules across the graft junction. In order to test this, a transcriptional (pCLE12:tdtomato) and translational reporter (pCLE12:CLE12-eGFP) were generated in tomato. The T1 plants are currently being genotyped. 3. The third objective of this project was to investigate how necrosis impacts the intercellular signaling within the graft interface, especially within incompatible grafted plants. Aim 3 was thoroughly explored in the last year. This was done by conducting a large-scale graft trial between tomato and four pepper varieties. These grafts were all analyzed anatomically via confocal microscopy. TUNEL assays and necrotic staining were performed to determine cell death in these tissues. Furthermore, a RNA-seq timeline was collected over three weeks, tracking the junction of tomato and pepper heterografts. This work will be submitted for publication in the next six months. These experiments aligned with the priority of the Plant Health and Production and Plant Products program.

Publications


    Progress 06/15/20 to 06/14/21

    Outputs
    Target Audience:My main efforts to deliver this research will be through academic journals and scientific conferences. During the duration of this project, I will attend and present at three or more conferences and publish at least two papers. Although these efforts will mostly target scientists, they will also reach the true target audience of this project: breeders and growers. There are populations of growers within the United States, such as apple growers, who depend on compatible grafts to maintain economically profitable varieties. Changes/Problems:1. Due to significant delays caused by COVID-19 quarantine and campus closure, constructs were synthesized instead of generated in-house. Due to budget and time constraints, it was necessary to focus on CLE42 rather than PEAR1.Additionally, any transgenic lines proposed to occur in pepper and eggplant are expected to experience delays outside of the scope of this grant. Thus, tomato transgenic lines have been prioritized. 2. Previously Aim 3 described the use of DAB to quantify cell death in grafted stems. Through protocol optimization, programmed cell death was found to be a more reliable metric for cell death than ROS accumulation. Thus, Aim 3 now describes the use of a TUNEL assay instead of DAB prints. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?The data generated in the last year wassubmitted as a publication to The Plant Cell. This data was also shared with the broader plant science community through virtual conferences including Plant Biology 2020 (poster), 2020 Sainsbury Lab Symposium (poster), 2021 Northeast Regional Meeting of the Society ofDevelopmental Biology (poster), and Plant Biology 2021 this summer (talk). What do you plan to do during the next reporting period to accomplish the goals?Based on a detailed project plan for this grant, the remaining goals include: Aim 1: Is PD formation at the graft junction interface altered in incompatible grafts? Grafting as a tool to track the formation of PD at the graft junction: Tomato will be grafted with the red PD marker as the scion and the green PD marker as the stock.Red and green puncta will indicate half-PD formation, whereas yellow puncta will form when PD-associated proteins colocalize, indicating that whole PD has formed across the junction. No puncta will indicate a lack of PD at the graft interface. To determine that the marker line has not affected PD formation or the ability of the crops to graft, all transgenic crops will be self-grafted. To quantify the baseline number of PD formed along the graft junction in self-grafted plants, scions with PDLP5-GPF will be grafted to the same genotype expressing PDLP5-RFP. Image analysis of graft junctions: Graft junctions will be cut out, 1 cm on either side of the interface daily, for 8 days following grafting, and cleared in ClearSee. Samples will be imaged daily using a Zeiss u880 confocal microscope. Image analysis of PD formation: All images will focus on the same cell types and use the same laser settings. Colocalization and imaging analysis will be performed with consistent parameters on ImageJ. Attendance at a scientific conference: This research will be presented at a national or international scientific conference. Aim 2 : Are mobile signals required for successful grafts? Grafting as a tool to track the transcription and movement of mobile signals CLE42 : The graft combinations below will be performed: tomato:tomato,tomato:pepper, pepper:tomato, tomato:eggplant, eggplant:tomato. To determine that the marker line has not affected the ability of the crops to graft and to quantify the baseline levels of gene expression, transgenic plants will be self-grafted. To determine protein mobility, transgenic species will be reciprocally grafted with their respective wild-type species. To investigate the effect of hetero-grafting, the transgenic lines will be reciprocally grafted with non-self wild-type species. One fluorescent reporter will mark the location of expression. The contrasting fluorophore will mark the mobility of the protein. Both of these signals are already known to be mobile and act non-cell autonomously. Thus, we expect to see mobile protein outside of the region of transcription within the parent tissue. The presence of the mobile signal in the wild-type plant will show that mobile signals are capable of crossing the graft junction into the grafted partner. Image analysis of graft junction: Graft junctions will be cut out, 1 cm on either side of the interface daily, for 8 days following grafting, and cleared in ClearSee. Samples will be imaged daily using a Zeiss u880 confocal microscope. Image analysis of mobile signal transcription and mobility formation: All images will focus on the same region of the stem and use the same laser settings. Colocalization and imaging analysis will be performed with consistent parameters on ImageJ. Attendance at a scientific conference: This research will be presented at a national or international scientific conference. Generation of publication: Aim 1 and aim 2 will be combined to produce a publication describing the role of intercellular signaling on grafting. This effort will advance knowledge for scientists and breeders. Aim 3: Is necrosis a barrier for communication in grafted plants? TUNEL assay a test for programmed cell death: Cell death is a common symptom of graft incompatibility. Cell death will be quantified using a TUNEL assay which fluorescently labels cells undergoing programmed cell death.To assay the accumulation of cell death in the stem over time, grafted plants will be harvested at 7, 14, and 28 days after grafting. Grafted stems and ungrafted stemswill be cut longitudinally fixed. The tissue will be processed for paraffin embedding and sectioning and then histologically processed using a TUNEL assay kit. Image analysis of fluorescent labeling: Samples will be imaged using a Zeiss u880 confocal microscope and analyzed with ImageJ. Attendance at a scientific conference: This research will be presented at a national or international scientific conference. Generation of publication: Aim 3 results will be used to produce a publication regarding the effect of grafting on reactive oxygen species. This effort will improve knowledge on graft incompatibility, and hopefully, begin to build a protocol to test for early graft incompatibility.

    Impacts
    What was accomplished under these goals? Under goals 1 and 2, fluorescent reporter constructs were generated and are currently being transformed into tomatoes. Under goal 3, a working protocol has been finalized to quantify necrosis in tomatoes. Together these achievements have represented significant progress towards the completion of the 3 main goals.

    Publications

    • Type: Journal Articles Status: Submitted Year Published: 2021 Citation: Thomas, H., Van den Broeck, L., Spurney, R., Sozzani, R., and Frank, M. (Submitted). Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation. Bioarxiv. https://doi.org/10.1101/2021.02.26.433082