Source: TEXAS TECH UNIVERSITY submitted to NRP
TISSUE-CULTURE INDEPENDENT GENE EDITING OF SHOOT APICAL MERISTEM CELLS BY A LONG-DISTANCE RNA TRANSPORT SYSTEM
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1026293
Grant No.
2021-67013-34738
Cumulative Award Amt.
$144,830.00
Proposal No.
2020-05663
Multistate No.
(N/A)
Project Start Date
May 1, 2021
Project End Date
Apr 30, 2023
Grant Year
2021
Program Code
[A1191]- Agricultural Innovation through Gene Editing
Recipient Organization
TEXAS TECH UNIVERSITY
(N/A)
LUBBOCK,TX 79409
Performing Department
Plant and Soil Science
Non Technical Summary
Genomic information is rapidly being generated not only for major crops such as maize, wheat and rice, but also for other economically important crops including common bean, chili pepper, papaya, grapevine, etc. The increasing amount of information about plant genomes has allowed the use of different strategies, such as genome wide association studies, comparative genomics and use of mutant and mapping populations, to identify genes that contribute to different traits important for plant productivity. To validate candidate genes in most cases it is necessary to produce knockout or altered mutants of the gene of interest. The development of the CRISP/Cas9 technology that allows to edit genetic information to produce knockout, point mutations, changes in promoter strength (promoter bashing), DNA insertions, and gene replacements, has changed the way we do biology. Successful application of gene editing has been reported for many crop plants including maize, rice, soybean, cotton, among several others, but the tissue culture step to produce gene edited plants is time consuming and limited to the few laboratories that have the expertise in cell culture to regenerate these crop plants. To overcome the tissue culture hurdle to produce gene edited plants, we propose to design and develop a tissue-culture independent gene editing system that should be generally applicable to most broad leave crops, such as cotton, soybean, common beans, sunflowers, etc., and simple enough that could be carried out in a common greenhouse by people with basic training in horticulture or other plant science areas. The rational of this proposal is to use natural long-distance RNA mobility to supply cells in the shoot apical meristem with the RNAs required for gene editing without the need of the target cells to be directly subjected to the process of DNA, RNA, protein delivery, or the regeneration process. If we transfect leaf or cotyledon cells with the genes required to produce the editing machinery and only the RNAs move into meristematic cells, we will prevent undesirable DNA insertions, genetic and epigenetic alterations in the genome of the target cells that are often associated with the Agrobacterium-mediated transformation processes or abnormal developmental processes such as de novo meristem formation from differentiated cells. Gene-edited cells will still be part of the normal apical meristem, which later will rise to gametes that will produce gene edited seed under normal greenhouse conditions.
Animal Health Component
(N/A)
Research Effort Categories
Basic
50%
Applied
(N/A)
Developmental
50%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
20124991040100%
Goals / Objectives
General Objective: Design of a system to efficiently edit shoot apical meristem cells via a long-distance transport of the RNAs required for genome editing.Specific Objectives:1) Identification of an RNA motif capable of efficiently rendering long-distance mobility and entry into SAM cells encoding Cas9 and guide-RNAS. To achieve this objective, we will first examine the capacity of the UTRs of CENTRORADIALIS and GAI mRNAs, the 102 bases 5'UTR of FT mRNA movement motifs to efficiently mediate long-distance transport and entry into the SAM of large RNAs. We will also test the efficiency as zip-code elements of tRNAMet (TAIR No. At5g57885) and tRNAGly (TAIR No. At1g71700), which have been shown to be present in phloem sap and be capable of mobilizing mRNAS into meristems and flowers (Zhang et al., 2016). We will first produce a construct encoding a mCherry-GUS and mCherrry-Cas9 reporter gene fusions which will be linked to the different zip-code elements to test their capacity to mediate the long-distance transport and entry into the SAM of large mRNAs (Figure 3). The mRNAs will be produced using a binary vector containing a geminiviral origin of replication to amplify the DNA template for transcription and a gene construct to express the mCherry-GUS and mCherrry-Cas9 mRNAs under control of the double CaMV35S promoter and the terminator of the heat shock protein (HSP) gene, which has been shown to increase gene expression in several plants (Hirai et al., 2011).2) Design of constructs to produce the different components of the gene editing machinery with the signal to be transported into and process in SAM cells.To ensure that the Cas9 and the gRNAs are produced in the same cells of the SAM, we will use a polycistronic RNA containing the coding sequence of Cas9 and the sgRNA(s). The design requires the polycistronic RNA to be processed in a way that a Cas9 mRNA with a poly-A tail and mature sgRNAs are liberated. Multiple sgRNAs to target the same gene can be included in the polycistronic RNA to enhance gene editing. With that purpose, we will build the construct illustrated in figure 3. The construct contains the following components in 5' to 3' order: 1) the long intergenic region loop (LIR) of BeYDV to amplify the number of copies of the T-DNA as is commonly used in agroinfiltration experiments to enhance the levels of transcription; 2) a double CaMV35S promoter to achieve a very high level of transcription of the Cas9/sgRNA polycistronic cassette (Kay et al., 1987); 3) a zip-code sequence, i.e. the 102 nt 5' UTR of the Arabidopsis FT transcript; 4) the Cas9 coding sequence with codon optimization for dicots; 5) a synthetic poly-A tail, which will promote further polyadenylation and mRNA export from the nucleus upon processing of the polycistronic RNA by Cys4 (Dower et al., 2004); 6) a Cys4 recognition and cleavage sequence; 7) the sequence of the sgRNA(s) flaked by another Cys4 processing sequence; 8) and a double terminator of the Arabidopsis heat shock protein terminator and the Nos terminator and polyadenylation sequence, that has been shown to enhance transcript accumulation probably preventing transcriptional readthrough that reduces transcript stability (Yamamoto et al., 2018), and 9) the SIR, replicase gene and a second long intergenic region loop to complete the replication machinery of BeYDV. If a zip-code element other than the FT movement signal is found to be more efficient for long-distance transport and entry into de SAM, it will be placed in the polycistronic RNA after the last Cys4 cleavage sequence but before the transcription terminator sequences. 3) Delivery of Cys4 and Cas9/gsRNA into the SAM cells.For the processing of the Cas9/sgRNA polycistronic transcript, the presence in the same cells of Cys4 is required. However, it is probably not desirable to produce both the Cas9/sgRNA and the Cys4 transcripts in the same cells because processing would probably take place rapidly and before long-distance transport. Therefore, we will produce the Cas9/gsRNA and Cys4 transcripts in different leaves and at different timepoints. This will increase the probability that Cys4, upon translation in SAM cells, will process the Cas9/sgRNA transcript to produce Cas9 and mature sgRNAs for gene editing. To test when and where is most convenient to express Cys4 to be able to effectively provide Cys4 nuclease in SAM cell for the processing of the Cas9/sgRNA transcript, we will use a test system based on the requirement of a poly-A tail for efficient translation. We will test the following constructs: 1) a GFP or mCherry coding sequence followed by a ribozyme and its target site, and the Nos 3'end; the ribozyme will release a transcript lacking poly-A tail, 2) the fluorescent protein coding sequence followed by an artificial poly-A tail, a Cys4 processing signal and ribozyme and its target site that will release a transcript lacking a natural poly-A tail at the 3' end of the transcript, 3) a control having the fluorescent protein coding sequence followed by the Nos terminator and polyadenylation sequence. All constructs will include an RNA mobility signal or zip-code element such as the 102 nt FT movement motif.4) Selection of tissues to produce the RNAs required for gene editing.We will use agroinfiltration of leaves to produce the Cas9/sgRNA and Cys4 transcripts, which we expect to move via the phloem into SAM where meristematic cells would be subjected to gene editing. Agroinfiltration will be done on the abaxial side of leaves using a needleless syringe (different leaves or different areas of the same leave for each construct). For each Agrobacterium strain (Cas9/sgRNA or Cys4) we will test i) one, two and three agroinfiltrations, once every 24 h in the same leaf; ii) one, two or three simultaneous agroinfiltrations on the same leaf; and iii) two different leaves agroinfiltrated simultaneously one to three times or agroinfiltrated one 24 h after the other. N. benthamiana plants will be agroinfiltrated at the 4, 6 and 8 leaf stages. After agroinfiltration treatments, plants will be allowed to grow and the appearance of white photobleached sectors will be monitored. If white sectors are detected, derived from gene editing of the two PSD alleles in tobacco and 4 alleles in cotton, we will follow to seed production. At Texas Tech University, we have state-of-art greenhouse facility that in addition to light and temperature control, has a system to control light spectrum and light quality to modulate/accelerate the flowering time. Using this greenhouse system, we can have three to four cycles of N. benthamiana per year. Thus, we will have no problem to do experiments all year round and accelerate flowering when needed.5) Gene editing confirmation.We expect to observed white sectors in leaves that form after the DNA transfection processes either in greenhouse plants or germinating seeds, which size will depend on the number of cells in the SAM harboring edited PDS or CHL1 genes. However, if only one of the alleles has been edited, we will not see white sectors even do one of the two copies of the gene is mutated. Therefore, whether we see or not white sectors we will collect tissue of the apical tip of the plant from several plants, amplify the regions of the PDS or CHL1 genes and sequence the amplicon using an Illumina MySeq platform.
Project Methods
-MethodsAgrobacterium strains and agroinfiltrationFor agroinfiltration experiments we will test two A. tumefaciens strains, C58C1 and AGL1. Plasmids will be mobilized into A. tumefaciens strains via electroporation (Dower et al., 1988). Recombinant Agrobacterium will be prepared for infiltration using a modified protocol of Sainsbury and Lomonossoff (ref) [32]. Briefly, a single colony of recombinant bacteria will be inoculated into liquid LB media (10g/L tryptone, 5g/L yeast extract; 10g/L NaCl, pH 7) containing kanamycin (100mg/L) and rifampicin (50mg/L). Cultures will be grown overnight at 28°C with shaking. Bacteria will be concentrated by centrifugation (14,000g for 5min) and resuspended to an OD600 = 0.5 in MMA (10mM MES pH 5.6, 10mM MgCl2, 500μM acetosyringone) supplemented with 5 uM lipoid acid as recommended by Norkunas et al. (2018) to maximize transient expression. For transient expression, bacteria will be delivered by "syringe agroinfiltration" into the abaxial side of leaves of 2, 4 and 8-week old greenhouse grown plants-month using a blunt tipped plastic syringe and applying gentle pressure. The same agroinfiltration procedure will be applied for N. benthamiana and cotton, as good results have been reported for both species using similar protocols (Gu at al., 2014; Norkunas et al., 2018).Particle bombardmentEmbryos or cotyledons will be bombarded using a conventional PDS-1000/He System particle bombardment equipment from Biorad with an Hepta devise to optimize particle distribution. For transient expression in leaves of greenhouse plants a hand-held Helios Gene Gun System from Biorad. DNA coating and bombardment procedures will be essentially those described by Cabrera-Ponce, Vegas-Garcia and Herrera-Estrella (1995) with some modifications: 50 ml M-17 tungsten particles(15 mg/ml), 10 ml DNA (1ug/ml), 50 ml 2±5mCaCl and 20 ml of 1 mM spermidine are mixed in sequential order, then briefly sonicated. The mixture is centrifuged at10 000 rpm for 10 sec. The supernatant is discarded, and the pellet resuspended in 100 % ethanol. After a short sonication, aliquots are delivered onto the center of each macrocarrier. The tissue is bombarded twice at 1200 psi (4 h interval between bombardments). DNA coated particles for the Gen Gun system will be prepared using the same protocolVector constructionAll vectors will be constructed using the Golden Gate (GG) Strategy (Engler and Marillonnet 2014). The different components of each construct will be synthesized and inserted into L0 vectors from the GG Plant Toolkit (Engler et al., 2014). Then we will perform the L1 synthesis reaction and finally clone into an L2 GG binary vector containing the BeYDV origin of replication.

Progress 05/01/21 to 04/30/23

Outputs
Target Audience:The target audience for the work performed in this project is graduate students, postdoctoral fellows, and faculty interested in using gene editing strategies to study plant biology and crop improvement. Sorghum Checkoff and Cotton Incorporated are also intended audiences with whom we met to test the system we are developing in cotton and sorghum. Changes/Problems:Although the proposed strategy of long-distance gene editing was successful in vegetative tissue, no edited albino progeny was obtained. This showed that the integrity and efficiency of these movable RNAs were not high enough to provide sufficient functional gene editing in meristematic tissues. Therefore, we generated new gene constructs using the FT movement signal as well as tRNAs to enhance long-distance RNA transport; we also decided to use a recently reported codon-optimized/intronized Zea maize Cas9 (zCas9i) that increased editing efficiency in Arabidopsis from 5 to 70% (Grützner et al., 2021). We also included two nuclear localization signals to enhance the entry of Cas9 into the nucleus after translation in the cytoplasm. We are currently testing this construct using two alternative strategies: 1) based on the originally proposed Agro-infiltration strategy and 2) using stable expression in transgenic roots induced by inoculating with Agrobacterium rhizogenes. In the second strategy, we would continuously produce the mRNA encoding the gene editing machinery to enhance the efficiency of reaching target cells in the shoot apical meristem. Testing of the new constructs and strategies is ongoing, and we expect results for the second half of 2023. What opportunities for training and professional development has the project provided?A graduate student, Benjamin Perez, completed his MSc program and initiated a Ph.D. program working on this project. Drs. Damar López Arrendondo and Gunvant Patil, two early carrier scientists at our Institute IGCAST, participated in the design of new strategies and data analysis. PI Herrera-Estrella advised the two young investigators in grant writing and participated in two graduate courses (Synthetic Biology for Crop Improvement and Plant Experimental Design) attended by 35 students, in which he gave lectures on gene transfer in plants and different strategies for tissue-culture-independent gene editing strategies. How have the results been disseminated to communities of interest?PI Herrera-Estrella presented the advances in developing tissue-culture-independent gene editing in plants in a Special Seminar for students, postdocs, and faculty at the Salk Institute of Biological Sciences. MSc student Benjamín Perez presented his work on gene editing at the annual poster competition for graduate students of the Davis College of Agricultural Science and Natural Resources of Texas Tech University. He received an award for third place in the competition in which over 70 graduate students participated. MSc student Benjamín Perez also presented his work at the annual meeting of the Institute of Genomics for Crop Abiotic Stress Tolerance at Texas Tech University, which was attended by 60 graduate students, postdoctoral fellows, and faculty. MSc Benjamín Perez was accepted to participate in the NSF-funded Plant Transformation Workshop to be held August 1-4, 2023, at the Wisconsin Crop Innovation Center facility at the University of Wisconsin-Madison. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? First, we tested the capacity of the signal sequence of the FLOWERING LOCUS T transcript or tRNAs to promote the movement of RNAs encoding a fusion protein of mCHERRY and b-glucuronidase into the shoot apical meristem of tobacco plants. Plants with these constructs were Agro-infiltrated in the 4th leave of 20-day-old tobacco plants; after 10 days, the meristems of these plants were excised, and the presence of mCHERRY and GUS were examined. We found that both signals could mobilize the mCHERRY-GUS transcript into tobacco shot apical meristem. We then produced gene constructs encoding the Cas9 protein with guide RNA flanked Cys4 cutting sites and an independent construct encoding the Cys4 protein. We used the Fast-TrACC transient expression system to evaluate whether seedlings expressing both constructs could edit target genes. We found that Csy4 can process the guide RNAs releasing a Poly A+ RNA encoding Cas9 and that the editing machinery was functional, as sequencing the target sites of the guide RNAs showed that mutations had occurred at the expected position. We then made a single construct encoding Csy4 fused to Cas9 with a P2A peptide between the two proteins for self-processing, and the guide RNAs separated by Csy4 cutting sites. Using the Fast-TraACC system, we could show that this single construct efficiently produced the gene editing machinery, and mutations in the target sites could be detected at a reasonable frequency (5-30%). Then, we tested whether the proposed strategy for long-distance RNA transport was effective. Using qRT-PCR, we showed that incorporating the FLOWERING LOCUS T movement signal to the mRNA encoding the CRISPR/Cas9 editing machinery was sufficient to promote the transport of the mRNA from Agro-infiltrated leaves into the plant's apex. To assess the functionality of our approach, we targeted the PDS genes in Nicotiana benthamiana as the loss of function of these two genes (PDS1 and PDS2) results in chlorophyll photobleaching, which produces a distinguishable albino phenotype. We detected albino sectors in new leaves of Aagro-infiltrated plants, showing that the editing machinery could move into new tissues and effectively edit the target genes. Then, we evaluate the progeny produced by Agro-infiltrated plants. Visual inspection of the progeny showed that none of the seedlings had the albino phenotype, suggesting that the integrity and efficiency of these movable RNAs were not high enough to provide sufficient functional gene editing in meristematic tissues. Therefore, we generated a new gene construct using the FT movement signal as well as tRNAs to enhance long-distance RNA transport; we also decided to use a recently reported codon-optimized/intronized Zea maize Cas9 (zCas9i) that increased editing efficiency in Arabidopsis from 5 to 70% (Grützner et al., 2021). We also included two nuclear localization signals to enhance the entry of Cas9 into the nucleus after translation in the cytoplasm. We are currently testing this construct using two alternative strategies: 1) based on the originally proposed Agro-infiltration strategy and 2) using stable expression in transgenic roots induced by inoculating with Agrobacterium rhizogenes. In the second strategy, we would continuously produce the mRNA encoding the gene editing machinery to enhance the efficiency of reaching target cells in the shoot apical meristem. Testing of the new constructs and strategies is ongoing, and we expect results for the second half of 2023.

Publications


    Progress 05/01/21 to 04/30/22

    Outputs
    Target Audience: Nothing Reported Changes/Problems:The main problem we had was the COVID-19 contingency that significantly slowed down our activities.We are far from claiming success, but the results obtained in this first year are promising. What opportunities for training and professional development has the project provided?The project has been very important for the training of a MSc students, who will star a PhD program in June 2022 to continue working in the project. It has also been important for the professional development of two young faculty, Drs. Damar Lopez-Arredondo and Gunvant Patil, that participated in executing the proposed reserach and writting the PCT patent application How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?1. We need to determine whether the movement of Cas9 and Csy4 transcripts into the apex of the plant can indeed lead to gene editing of meristematic cells and the efficiency of the process. We will perform DNA sequencing of the PDS target gene, in a similar way as that used for the TrACC assays, with Sanger sequencing to determine the occurrence of gene editing events. 2. We will produce progeny of Agroinfiltrated plants to determine whether albino mutants are present in the population and its frequency. 3. We will build an alternative gene editing construct using the Casø nuclease. This nuclease is about half the size of Cas9, thus the corresponding transcript is significantly smaller and might be more mobile in the phloem of Agroinfiltrated plants. Additionally, since Casø can process by itself its sgRNAs (denominated crRNAs in this case), we will need a single construct to produce the complete gene editing machinery. We hypothesize that Casø might be more efficient than our original split system since it depends on a single smaller transcript.

    Impacts
    What was accomplished under these goals? The development of the CRISP/Cas9 technology that allows editing genetic information has changed the way we do biology and crop improvement. Successful application of gene editing has been reported for many crop plants including maize, rice, soybean, cotton, among several others. However, the tissue culture steps required to produce gene edited plants is time consuming and limited to the few laboratories that have the expertise in cell culture to regenerate these crop plants. To overcome the tissue culture hurdle to produce gene edited plants, we propose to design and develop a tissue-culture independent gene editing system that should be generally applicable to most broad leave crops, such as cotton, soybean, common beans, sunflowers, etc., and simple enough that could be carried out in a common greenhouse by people with basic training in horticulture or other plant science areas. Among the objectives achieves in this reporting period I can mention the following: We built gene constructs that will allow us to test whether a polycistronic mRNA containing the Cas9 nuclease and guide RNAS for the target gene can be processed by the nuclease Csy4. The system is composed of two component one encoding the CRISPR/Cas9 machinery and the second the Cys4 nuclease to process the polycistronic RNA. We designed and constructed individual plasmids to produce a single mRNA containing the Cas9 nuclease coding sequence and four sgRNAs (to target the PDS gene) spaced with Csy4 cut sites. To process the Cas9/sgRNAs, we produced a second plasmid coding for Csy4 the nuclease that naturally process sgRNAs in bacteria. These two original transcription units, Cas9/sgRNAs and Cys4, contain the whole Flowering Locus T CDS sequence as part of the 3' UTR, but lacking an initiation codon to prevent its translation, or the FT 5'UTR only. We included the FT sequences to promote transport of the Cas9/sgRNAs and Cys4 transcript into the meristem of Agro-inoculated plants. In addition to the split editing systems in which the nuclease genes and guide RNAs were produced as separate transcripts, we also produced Single Transcriptional Units for both CRISPR/Cas systems. This approach combines the nuclease sequences, the guide RNAs, and the RNA processing machinery into a single transcriptional unit driven by a single promoter. The translatable part of the transcripts is separated from the guide RNA tandem by a synthetic poly Adenine sequence (50X A). For the Cas9 Single Transcript Unit, the processing Csy4 enzyme is separated from Cas9 by a 2A self-cleaving peptide sequence to separate the two polypeptides after translation. This sequence can induce ribosomal skipping during translation, splitting the forming peptide and allowing equimolar amounts of the two enzymes. To achieve a maximum level of the transcripts described in points 1 and 2, we integrated the replication machinery of the Bean Yellow Dwarf Virus (BeYDV) in our vectors, a strategy initially proposed by Zhang & Mason (2005). To test the expression of the construct described in points 1 and 2, we used the published Fast-TrACC methodology (Nasti et al. 2021). In this protocol, one-week-old seedlings are co-cultivated with the bacterial strain in liquid media for two days before evaluating transgene expression. We simplified this method and included a vacuum infiltration step to make the system more reproducible. We found that both constructs were expressed at good levels by monitoring expression of the GFP or mCHERRY fluorescent proteins included in our plasmid constructs. We also verified expression of Cas9 and Csy4 by quantitative real-time RT-PCR. To determine whether the single or split constructs were able to edit the target gene, we pooled seedlings from each treatment and extracted genomic DNA with the CTAB protocol. Then we selectively amplified the PDS genes from the DNA extracted from the seedlings Agroinfiltrated with each of the editing constructs and the PCR products subjected to Sanger sequencing. Interestingly, background noise from aberrant base calls was present in the analyzed electropherograms, showing that gene editing had occurred in the plantlets. Using short-time amplification PCR to enrich small amplicons allowed us to identify the largest deletions and confirm that the vectors are functional. So far, we have been able to characterize in detail a 3,140 bp and a 2,928 bp deletions in seedlings treated with Agrobacterium tumefaciens harboring the Cas9-sgRNA and Cys4 gene constructs. To test whether the FT movement signals can mobilize the Cas9 and Csy4 mRNA into meristematic cells, we agroinfiltrated the 4 and 5 leaves of 20-day-old Nicotiana benthamiana plants. After 5 days of agroinfiltration the shoot apex of each plant was collected to extract total RNA. RT-PCR was used to determine whether the Cas9 and Csy4 transcript had moved from the leaves to the shoot apical meristematic region. We found that in 60% of the plant had at least one of the two mRNAs and that in about 30% of the plants both components were detected. We subjected the RT-PCR amplicons to Sanger sequencing to verify the identity of the transcripts and found that, indeed, they correspond to the Csy4 and Cas9 transcripts. Nasti, R. A., Zinselmeier, M. H., Vollbrecht, M., Maher, M. F., & Voytas, D. F. (2021). Fast-TrACC: A Rapid Method for Delivering and Testing Gene Editing Reagents in Somatic Plant Cells. Frontiers in genome editing, 2, 32. Zhang, X., & Mason, H. (2006). Bean yellow dwarf virus replicons for high?level transgene expression in transgenic plants and cell cultures. Biotechnology and bioengineering, 93(2), 271-279.

    Publications