Source: UNIVERSITY OF CALIFORNIA, DAVIS submitted to
EXPANDING BENEFITS OF GENE EDITING TO MINOR CROPS WITH LOW REGENERATION EFFICIENCY BY USING A PLANT GROWTH-REGULATOR WITH ENHANCED ACTIVITY
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1022267
Grant No.
2020-67013-31545
Cumulative Award Amt.
$299,963.00
Proposal No.
2019-07109
Multistate No.
(N/A)
Project Start Date
Jun 15, 2020
Project End Date
Jun 14, 2023
Grant Year
2020
Program Code
[A1191]- Agricultural Innovation through Gene Editing
Recipient Organization
UNIVERSITY OF CALIFORNIA, DAVIS
410 MRAK HALL
DAVIS,CA 95616-8671
Performing Department
Agr & Env Sci Deans Office
Non Technical Summary
Genome editing is a revolutionary technology that allow one to make precise changes in a plant's genetic blueprint for agriculture. However, its application to many minor crops like alfalfa, grapevines, lemons, limes and oranges, is limited. The limitation in using gene-editing techniques in these crops is mainly due to the inability of stem cells of these plants to reform whole plants in tissue culture. There are only a very few varieties of alfalfa, oranges, limes, lemons and grapevines for which we are capable of forming whole plants from cells in tissue culture and the few varieties that we have been successful with do so at a very low frequency.We recently discovered that a gene sequence encoding a chimeric protein that comprises a GROWTH REGULATING FACTOR (GRF) and its cofactor GRF INTERACTING FACTOR (GIF) (henceforth GRF-GIF) dramatically increased the ability of wheat stem cells to reform whole plants in tissue culture. When combined with the gene editing system CRISPR-Cas9, we found that this technology also significantly increases the total number of gene-edited plants we can produce using tissue culture. A novel feature of this technology is that although the chimeric gene enhances regeneration in young cells, the chimeric gene is turned off in older tissue so that the plant grows normally to maturity. In wheat, the technology also allows us to make gene edits in plants without the use of a plant selectable marker gene. The GRF-GIF system stimulates the cells that contain it to reform plants on tissue culture plates that lack certain growth factors normally added to the culture medium and which are required for the cells to reform plants in a petri dish. Plant selectable marker genes are used to allow plant cells to grow on compound on which they normally cannot grow. These selective agents allows only cells containing the new gene edit along with the plant selectable marker gene to reform whole plants in the presence of the selective agent. Plant selectable marker genes currently used are often those that confer resistant to antibiotics or herbicides. Although regulatory agencies have approved genetically modified plants containing these genes for commercialization, the public would prefer not to have these genes in their food supply.Promising preliminary results in citrus suggest that this technology may be applicable to multiple plant species. Therefore the overall goal of this proposal is to use this technology to expand the benefits of gene editing to minor crops by increase the efficiency with which plant cells reform plants across multiple varieties of alfalfa, citrus and Vitis vinifera. In addition, we want to use the ability of the GRF-GIF technology to replace antibiotic and herbicide plant cell selection system. Lastly, we want to combine GRF-GIF technology with Genome Editing for each of the crop to enhance the production of gene-edited plants. This project will open the door to multiple minor crops to benefit from the power of genome editing technologies
Animal Health Component
30%
Research Effort Categories
Basic
70%
Applied
30%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2011640103033%
2010999103033%
2011139103034%
Goals / Objectives
The overall goal of this proposal is to expand the efficient GRF-GIF regeneration technology from wheat to other minor crops to improve their transformation efficiencies so they can benefit from gene editing technologies. The ability to generate large number of transgenic events combined with genome editing will be a significant improvement in the breeding and research approaches used in these species. For this project, we selected an economically important and diverse group of minor crops that includes alfalfa, citrus and grape. Regeneration frequencies are low and highly genotype dependent for each of these minor crops.Alfalfa (Medicago sativa) is a cross-pollinated, polyploid, perennial legume that is distributed throughout the entire United States, and provides high quality hay and grazing. It is a heterozygous, continually segregating population in which every seedling is genetically different. Therefore, an alfalfa cultivar is not a uniform population but instead a random, interbreeding population of plants. Transformation of alfalfa like wheat relies on somatic embryogenesis. The transformation process is strongly limited by genotype with non-dormant genotypes of alfalfa particularly difficult to transform due to their inability to undergo somatic embryogenesis. Even for alfalfa cultivars that are competent to regenerate, only a very limited number of seedlings within the population exhibit efficient regeneration. Therefore, one needs to identify specific individual seedlings within the segregating population that are competent to regenerate, establish a clone of that seedling in vitro and maintain the clone as a tissue culture stock plant. This limitation significantly complicates the development of transgenic cultivars, since the breeding population must be recreated by incorporating the transgenic allele back into the segregating population. If the GRF-GIF technology allows transformation of more expanded germplasm, more individuals within the segregation populations could be transformed accelerating the reestablishment of the breeding populations.Grapevine (Vitis vinifera): A limited number of grapevine clones have been used for many decades to produce high quality wine. These clones are maintained by vegetative propagation to preserve the intrinsic quality of this material. Therefore, the introduction of new traits into existing Vitis cultivars without altering their essential characters and identity is crucial. Transformation, coupled with genome editing is a powerful method to achieve this goal, but is currently limited by the low transformation efficiency in this species. Table grapes and rootstock are more amenable to transformation, but wine grapes have proven particularly difficult to transform. A major bottleneck in transformation of wine grape is the regeneration of embryos and shoots from transgenic tissue. Indeed, inoculation of wine grape genotypes with an Agrobacterium-engineered to express the DsRed marker, gives high frequencies of transgenic tissues. However, the success in converting this transgenic tissue into embryos and plants has been limited. The transformation process in this species is further complicated because, pro-embryogenic callus must be generated from anther filaments of immature flowers collected in the spring of each year. The frequency of filaments that produce embryogenic callus is extremely variable, ranging from 8.9% in some rootstocks to a 0.7 % for Cabernet and Chardonnay. Even lower percentages are observed for other wine grapes such as Zinfandel and Pinot noir. Furthermore, the transformation process is slow and very laborious requiring 8 to 12 months for generating transgenic plant lines. Currently, there are only a few facilities in the US capable of grape transformation. Like wheat, grape transformation process utilizes embryogenesis. If the GRF4-GIF1 chimera allows for higher regeneration frequencies from callus of wine grapes, it would allow for genetic engineering of these important genotypes. If GRF4-GIF1 transgenic lines could be created for these wine grapes, this would also facilitate the identification of more accessible tissue (e.g. leaves and internodes) to be used as sources for Agrobacterium-mediated transformation.Citrus: Citrus farmers and industry are currently threatened by the devastating effects of the Citrus Greening or Huanglongbing (HLB) disease. Most of the commercial citrus trees in Florida are currently infected, and the insect vector of the disease is now present in California. Therefore, one of the main motivations for the selection of this species is to improve the efficiency and range of citrus genotypes amenable to transformation to accelerate research and development of HLB resistant plants. Currently the most efficient citrus transformation uses juvenile epicotyl tissue from seedlings generated from nucellar embryos. Although plants generated from nucellar embryos generate plants with the identical genotype, those plants require an extended time to fruiting. Low transformation efficiencies have made it difficult to evaluate the efficacy of transgenes against HLB since a large number of independent insertion events must be evaluated to assess the efficacy of each construct.The specific objectives of this proposal are to:1. Increase regeneration efficiency in multiple cultivars of alfalfa, citrus and Vitis vinifera (grape) usingthe GRF-GIF technology.2. Establish a positive selection method that does not require plant pest sequences.3. Combine GRF-GIF technology with Genome Editing systems for each of the three species toenhance the efficiency of recovery of gene-edited plants.This project will open the door to multiple minor crops to benefit from the power of genome editing technologies.
Project Methods
Methods to increase regeneration efficiency in multiple cultivars of alfalfa, citrus and Vitis vinifera using the GRF-GIF technology.GRF-GIF chimeras for each species will be generated by gene synthesis of the closest homologs to wheat GRF4 and GIF1 identified in the phylogenetic analysis . The resulting synthetic genes will be cloned in binary vectors under the control of Arabidopsis UBIQUITIN promoters. In these initial vectors, antibiotic-based selection markers will be included in the same T-DNA. In addition to the regular GRF-GIF chimeras, we are going to generate GRF-GIF versions with silent mutations in the miR396 target site that abolish the miR396-mediated repression, which will be referred hereafter as resistant GRF-GIF or simply rGRF-GIF. The presence of this mutation interferes with the cleavage of the GRF-GIF chimera in tissues with high levels of miR396. Since miR396 levels are particularly high in fully developed tissues, the rGRF-GIF chimera will particularly useful for transformation protocols involving developed tissues (like leaf, root and epicotyl explants). For all three species, we will test the ability of different GRF-GIF chimeras (regular and rGRF-GIF) to improve regeneration efficiency in standard Agrobacterium-based transformation protocols, which are routinely used at the UC Davis Plant Transformation Facility. In all species, regeneration efficiencies (the number of explants regenerating divided by the number of explants plated) will be compared with a similar vector without the GRF-GIF chimera and with the heterologous GRF-GIF chimeras from the other species. Alfalfa transformation will be performed on trifoliate leaflets harvested from in vitro grown individual seedlings of the non-dormant cultivar Highline and the breeding line UC2705. We will collect ten trifoliate leaves from ten independent seedlings and co-cultivate with Agrobacterium strain EHA105 containing alfalfa-specific GRF-GIF and rGRF-GIF chimeras. The empty vector and the heterologous GRF-GIF chimeras from wheat, grape and citrus will be used as controls. The frequency of leaflet regenerating shoots per plant and the frequency of transformable plants will be scored for the GRF-GIF chimeras and controls. For citrus transformation, seeds of the rootstock cultivar "Carrizo", a hybrid of Poncirus trifoliata L. will be surface sterilized and germinated in vitro. Epicotyls from 2-5 week-old etiolated seedlings will be collected, sectioned into internodal pieces and inoculated with Agrobacterium containing a citrus-specific GRF-GIF chimera (regular and rGRF-GIF). Additionally, new experiments will be performed with the citrus-specific chimeras using Citrus sinensis cv.Valencia seeds. Furthermore, we will determine if expressing the GRF-GIF chimeric genes allows regeneration from non-epicotyl tissue. Transgenic "Carrizo" plants expressing the GRF-GIF chimera will be maintained in vitro in large SteriConTM vessels, and leaves and stems of these plants will be tested as explants sources for regeneration. If we observed positive results we will test transformation with the GRF-GIF chimeras using mature tissue from "Carrizo", Valencia orange and navel orange addition. If regeneration from mature tissue is successful, clones of the GRF-GIF plants will be acclimated to soil in order to provide a source of mature explants for citrus transformation in the future. Grape transformation is performed on embryogenic callus that are induced from anther filaments collected from immature flowers which are only available during a small 3 week window in the spring. We hypothesize that a GRF-GIF chimera might increase regeneration efficiency from other easier-to-obtain tissues. We already have transgenic embryos of Thompson Seedless developing from embryogenic callus inoculated with the grape-specific GRF-GIF chimeric, rGRF-GIF chimera and an empty vector as control. This material will allow us to evaluate the ability of the GRF-GIF chimeras to promote regeneration in our standard transformation protocol. Moreover, to test if the GRF-GIF chimeras allow regeneration from other tissues, we will collect root, leaf, internodes and apices tissues from the T0 GRF-GIF and rGRF-GIF plants and compare their regeneration capacity with the same tissues collected from the corresponding controls transformed with an empty vector. If we see increase regeneration efficiency, we will start transformation of most regenerative tissues from Thompson Seedless and wine cultivars Merlot and Chardonnay as well as the grape rootstock Freedom.2. Methods to establish a positive selection protocol that does not require plant pest sequences.Once we have established efficient transformation protocols, we will test the ability of the GR-FGIF and rGRF-GIF chimeras to regenerate transgenic shoots in the absence cytokinins. Transformation experiments will be set varying the concentration of cytokinins in the culture medium as previously done in wheat. If we observe shoot regeneration in the absence of cytokinins, we will select the shoots and transfer them to rooting media. If we do not see regeneration in the absence of cytokinins, we will test increasing levels of cytokinins that are suboptimal for regeneration in the absence of the GRF-GIF chimera. If we see an increased production of shoots in the tissues transformed with the GRF-GIF chimera, we will transfer them to rooting media and determine the proportion of regenerated plants that are transgenic. If we obtain a very low number of false positives, we will repeat the experiment using a similar vector but without the selectable markers.3. Methods to combine GRF-GIF technology with Genome Editing systems to enhance the efficiency of recovery of gene-edited plants.As previously done in wheat, we will combine in the same T-DNA the best GRF-GIF chimera version for each species and the CRISPR-Cas9 cassettes. First, we will test a guide RNA (gRNAs) targeting the PDS (phytoene desaturase) gene in each of the three species. Mutations in this gene generate albino plants, a phenotype that is easy to score. We will also test two additional gRNAs that have been described in the literature for editing citrus and alfalfa. The generated vectors will be transformed by Agrobacterium and the frequency of regenerated shoots will be scored. Then, the independent regenerated T0 shoots will be analyzed for the frequency of editing by scoring the photo-bleaching phenotype of leaves. In the additional gRNA for citrus and alfalfa, we will test the frequency of editing events by using the disruption of restriction sites in the edited region.

Progress 06/15/20 to 06/14/23

Outputs
Target Audience:The target audience includes researchers developing transgenic or gene editing monocotyledonous and dicotyledonous plants. To that end, we have distributed a number of our GRF-GIF vectors to AddGene (https://www.addgene.org/). We have also made available other non-published GRF-GIF vectors through MTAs. These vectors are available to researchers in the public domain for use in their research studies. Changes/Problems:We requested and been granted a one year no cost extension due to the University of California at Davis was under suspended operation or reduced operations due to the Covid 19 pandemic during much of the first two years of the grant. What opportunities for training and professional development has the project provided?We have provided the GRF-GIF chimeric constructs to the International Maize and Wheat Improvement Center (CIMMYT) and the John Innes Center for use in wheat transformations. Both institutions have successfully implemented GRF-GIF to increase the efficiency of wheat transformations and expand the range of genotypes amenable for transformation. We have also shared wheat and maize GRF-GIF construct with Dr. Andrea Gallavoti (Rutgers University) and Dr. Laurens Pauwels (VIB, Belgium) whom developed efficient transformation protocol in maize using GRF-GIF. We have also been working with other labs regarding potential strategies for using the GRF-GIF chimeric gene in dicotyledonous. We have provided our vectors to Dr. Richard Michelmore Lab (UC Davis), where PhD student Tawni Bull has observed increased transformation efficiency and reduced genotype dependency in lettuce as part of her thesis. We are also working in collaboration with Dr. Steve Strauss (Oregon State University), who is testing GRF-GIF vectors in poplar and eucalypts. Dr. Kan Wang (Iowa State University) is currently testing GRF-GIF vectors in soybean.At our Transformation Facility, we are training an SRA (Danielle Inchaurregui) on the use of developmental regulators to improve transformation protocols in citrus, grape and alfalfa, and now tomato. How have the results been disseminated to communities of interest?We have discussed our results in alfalfa, citrus and grape with other researchers working in the field of improving transformation systems in their crops. We have discussed the abnormal phenotypes which are produced when the resistant GRF-GIF constructs are used and brainstormed ways which we have tried to modify the miRNA binding site to attenuate the system. We have observed that a DEX-inducible miR396 resistant GRF-GIF construct is functional and can be controlled exogenously by the addition of DEX. We have described our observation with other researchers using GRF-GIF on dicots of an early enhanced regeneration of non-transgenic shoots which resolves over time. We have also shared our observation regarding how the promoter driving the GRF-GIF chimeric gene can affect the regeneration response. We were invited to present our work in the SIVB 2021 and PAG 2023 conferences. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Alfalfa To test the GRF-GIF system in alfalfa we decided first to generate a construct using Fabales-specific sequences. To this end, we identified the best GRF and GIF candidate genes from soybean based on sequence homology with GRF and GIF genes from other species that we already have results on improvements on regeneration. We then generated the soybean GRF-GIF gene (GmaGRF-GIF) by gene synthesis and subcloned under 35S promoter in the pGWB14 binary vector, which includes a selection marker for Hygromycin and one for Kanamycin. We have also cloned the GRF-GIF gene under a Arabidopsis Ubiquitin promoter in case 35S promoter does not work well. We germinated 10 individual seedlings from alfalfa genotype Highline and from a UC Davis breeding line 2705 in tissue culture vessels and collected trifoliate leaves and inoculated them with 35S::GmaGRF-GIF and an empty vector (pGWB14 without GRF-GIF). As a positive control, we included leaf explants from seedling line 2525-14 which we have previously identified as being highly amenable to agrobacterium-mediated transformation. We did not see an enhancement in regeneration frequency in the highly amenable alfalfa line 2525-14. However, the GmaGRF-GIF gene was able to induce transgenic embryo formation in two seedling selections of Highline (2 out of 10) and one of 2705 (1 out of 10) that failed to generate transgenic embryos using the control vector. From work done in tomato, we knew that the promoter driving the GRF-GIF chimeric can affect its efficacy. Therefore, we have repeated these experiments using alfalfa line 2525-14 and 2525-51 using the soybean GRF-GIF driven by the Arabidopsis ubiquitin promoter. However we did not observe enhanced regeneration in the GmaGRF-GIF inoculated 2525-51 seedlings compared to those inoculated with the control vector. Taken together, the results indicate that the GRF-GF system can expand the range of alfalfa genotype amenable to transformation. However, selection of the right promoter could be relevant to get the best result. Citrus The citrus GRF-GIF construct was generated by gene synthesis. GRF genes contain a complementary sequence to the microRNA miR396, which represses GRF expression at the post-transcriptional level. Since miR396 is expressed at high level in mature tissues, we thought that this repression could limit the expression GRF-GIF during the transformation of leaf tissues. Therefore, we generated two other GRF-GIF versions that included silent mutations in the miR396 target site of the GRF gene. We tested the ability of these chimers to induce organogenesis from leaf tissue. We inoculated in vitro grown epicotyls of the citron rootstock Carrizo with the citrus GRF-GIF, citrus rGRF-GIF, and citrus rGRF-GIF mut T constructs and cultured them on shoot induction medium and regenerated stable transgenic plants which we maintained as whole plants in vitro. We collected leaf explants from these plants and plated them on medium known to induce organogenesis from citrus epicotyls. We scored the number of leaf explants that developed de-novo shoots. Interestingly, while only 1.5 % of the leaves collected from plants transformed with an empty vector generated plants, 7.8 and 8.0 % of the leaves from plants transformed with the citrus GRF-GIF or rGRF-GIF mut T construct respectively produce de novo shoots from the leaf explants. We also noticed that miR396-resistant GRF-GIF generated large transgenic calli that failed to regenerate shoots. Therefore, we developed a DEX induced version of rGRF-GIF, which would be active only when DEX is added to the media. We evaluated supplementation of the regeneration medium with 5 or 10 µm DEX at different times throughout the culture process. We observed that continual supplementation of DEX from the beginning of the process resulted in large calli that failed to regenerate shoots. Also, continual supplementation of DEX but only after a period of cultures without DEX resulted in large calli too. In contrast, supplementation of DEX only at the beginning of the process (early pulse) and then continuing without DEX did not result in large calli, but we could not observe clear enhancement in regeneration when compared with a non-DEX control. These results indicated that the construction is functional and that we can control rGRF-GIF activity exogenously by the addition of DEX. However, the timing of the induction is critical to get a beneficial response. For example, we hypothesize that a short pulse of dex at later culture steps could have a positive effect. Grape Similarly, to the citrus and soybean GRF-GIF constructs, we generated a grape GRF-GIF by gene synthesis. We then cloned it in pGWB14 vector under 35S promoter. We also generated a version with 4 silent mutations in the miR396 target site of the GRF gene (grape rGRF-GIF). We ran three sets of experiments to compare the transformation efficiency of the grape GRF-GIF, the grape rGRF-GIF chimera, or a vector control (pGWB14 without GRF-GIF) using somatic embryos of the table grape Thompson Seedless. We observed that plants transformed with the grape GRF-GIF developed into plants with a normal phenotype, whereas those transformed with the grape rGRF-GIF developed abnormally, but often produced much more secondary embryos. We think that in the future it could be interesting to test a DEX inducible rGRF-GIF vector, since it could allow to generate a large number of secondary embryos that in absence of DEX would develop normally. Including Cas9 in the same T-DNA, it would allow to have a highly embryogenic explant that can be transformed with gRNAs to generate independent editing events. 2. Establish a positive selection method that does not require plant pest sequences. We are testing the ability of the soybean GRF-GIF chimera to stimulate regeneration of transgenic embryos without in use of a selectable marker gene in alfalfa. We transformed in vitro grown trifoliate leaves of the alfalfa line 2525-14 with the GRF-GIF chimera construct or an empty vector control and co-cultured them on medium with or without cytokinin. We replicated this study twice. We did not see any significant differences between the number of explants regenerating embryos between the GRF-GIF chimeric construct or the control. We also inoculated citrus epicotyls with a control plasmid or the citrus rGRF-GIF. After co-cultivation, epicotyls were transferred to regeneration medium without antibiotic selection. We monitored the cultures for larger, more aggressive growing shoots, enhanced bud multiplication. However, we were unable to observe any differences in the vigor of shoot development between shoots developing from epicotyls inoculated with rGRF-GIF verses the control construct. 3. Combine GRF-GIF technology with Genome Editing systems for each of the three species to enhance the efficiency of recovery of gene-edited plants. We have generated several vectors including editing components and GRF-GIF, which are described below. However, we have dedicated most of our effort to test the effect of GRF-GIF on regeneration efficiency. Alfalfa: We have generated a vector containing the soybean GRF-GIF and gRNA to targeting the PDS gene. Grape: We have generated a vector containing the grape GRF-GIF and 3 gRNAs targeting the DELLA domain of the VvGAI1 gene (GSVIVT01011710001). Multiple mutations disrupting the DELLA domain could potentially generate GA insensitive alleles [Amino acid changes (grape), premature stop codons (wheat), or small deletions (Arabidopsis or maize)]. Citrus: We have generated a vector containing the citrus GRF-GIF and a gRNA targeting the CsLOB1 (Jia et al., 2016). We selected this target gene since the activity of the gRNA was already validated in literature and mutations in this gene resulted in improvement of citrus canker resistance in Duncan grapefruit.

Publications


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

    Outputs
    Target Audience:The target audience includes researchers developing transgenic or gene editing monocotyledonous and dicotyledonous plants. To that end, we have distributed a number of our GRF-GIF vectors to AddGene (https://www.addgene.org/). These vectors are available to researchers in the public domain for use in their research studies. Changes/Problems:We have requested and been granted a one year no cost extension due to the University of California at Davis was under suspended operation or reduced operations due to the Covid 19 pandemic during much of the first two years of the grant. What opportunities for training and professional development has the project provided?We have provided the GRF-GIF chimeric constructs to the International Maize and Wheat Improvement Center (CIMMYT) and the John Innes Center for use in wheat transformations. Both institutions have successfully implemented GRF-GIF to increase the efficiency of wheat transformations and expand the range of genotypes amenable for transformation. We have also shared wheat and maize GRF-GIF construct with Dr. Andrea Gallavoti (Rutgers University) and Dr. Laurens Pauwels (VIB, Belgium) whom developed efficient transformation protocol in maize using GRF-GIF. We have also been working with other labs regarding potential strategies for using the GRF-GIF chimeric gene in dicotyledonous. We have provided our vectors to Dr. Richard Michelmore Lab (UC Davis), where PhD student Tawni Bull has observed increased transformation efficiency in lettuce as part of her thesis. We are also working in collaboration with Dr. Steve Strauss (Oregon State University), who is testing GRF-GIF vectors in poplar and eucalypts. Dr. Kan Wang (Iowa State University) is currently testing GRF-GIF vectors in soybean. At our Transformation Facility, we are training an SRA (Danielle Inchaurregui) on the use of developmental regulators to improve transformation protocols in citrus, grape and alfalfa. How have the results been disseminated to communities of interest?We have discussed our results in alfalfa, citrus and grape with other researchers working in the field of improving transformation systems in their crops. In particular we have discussed the abnormal phenotypes which are produced when the resistant GRF-GIF constructs are used and brainstormed ways which we have tried to modify the miRNA binding site to attenuate the system. We have also shared our observation regarding how the promoter driving the GRF-GIF chimeric gene can affect the regeneration response. We were invited to present our work in the PAG 2022 conference. However the conference was cancelled due COVID. What do you plan to do during the next reporting period to accomplish the goals?Preliminary data indicate that the promoter used to drive GRF-GIF expression is important. In the next reporting period we will evaluate the effect of different promoters (like 35S and 2X35S; Ubiquitin promoters from Arabidopsis, Lotus japonica, Parsley and soybean) to induce transgenic calli and shoot regeneration. We have also observed that a DEX-inducible miR396 resistant GRF-GIF construct is functional and can be controlled exogenously by the addition of DEX. In these initial experiments, we have constantly cultured citrus explants in media supplemented with 10 µm DEX, which stimulated the formation of large transgenic calli, as normally observed in regular miR396 resistant GRF-GIF. In the next reporting period we will analyze different DEX dosage and different time periods of DEX treatment to identify conditions that result in optimal regeneration frequency.

    Impacts
    What was accomplished under these goals? Alfalfa To test the GRF-GIF system in alfalfa we decided first to generate a construct using Fabales-specific sequences. To this end, we identified the best GRF and GIF candidate genes from soybean based on sequence homology with GRF and GIF genes from other species that we already have results on improvements on regeneration. We then generated the soybean GRF-GIF gene by gene synthesis and subcloned under 35S promoter in the pGWB14 binary vector, which includes a selection marker for Hygromycin and one for Kanamycin. We have also cloned the GRF-GIF gene under a Lotus japonica Ubiquitin promoter in case 35S promoter does not work well. We germinated 10 individual seedlings from alfalfa genotype Highline and from a UC Davis breeding line 2705 in tissue culture vessels. After germination we created four clones of each of the 10 seedling and collected trifoliate leaves and inoculated them with soybean GRF-GIF and an empty vector (pGWB14 without GRF-GIF). As a positive control, we included leaf explants from seedling line 2525-14 which we have previously identified as being highly amenable to agrobacterium-mediated transformation. We recorded the number of calli producing embryos on explants inoculated using the soybean GRF-GIF verses the empty vector. We did not see an enhancement in regeneration frequency in the highly amenable alfalfa line 2525-14. However, the GRF-GIF gene was able to induce transgenic embryo formation in two seedling selections of Highline and one of 2705 that failed to generate transgenic embryos using the control vector. In addition, we know from work done in tomato that the promoter driving the GRF-GIF chimeric can affect its efficacy. Therefore, we plan to repeat this experiment using alfalfa line 2525-14 using the soybean GRF-GIF driven by the ubiquitin promoter. Citrus The citrus GRF-GIF construct was generated by gene synthesis. GRF genes contain a complementary sequence to the microRNA miR396, which represses GRF expression at the post-transcriptional level. Since miR396 is expressed at high level in mature tissues, we thought that this repression could limit the expression GRF-GIF during the transformation of leaf tissues. Therefore, we generated two other GRF-GIF versions that included silent mutations in the miR396 target site of the GRF gene. In one version we introduced 4 silent mutations (citrus rGRF-GIF) that we expect would eliminate miR396 interaction, and in the second we introduced only one mutation (rGRF-GIF mut T) to reduce but not eliminate miR396 repression. We tested the ability of these chimers to induce organogenesis from leaf tissue. We inoculated in vitro grown epicotyls of the citron rootstock Carrizo with the citrus GRF-GIF, citrus rGRF-GIF, and citrus rGRF-GIF mut T constructs and cultured them on shoot induction medium and regenerated stable transgenic plants which we maintained as whole plants in vitro. We collected leaf explants from these plants and plated them on medium known to induce organogenesis from citrus epicotyls. We scored the number of leaf explants that developed de-novo shoots. Interestingly, while only 1.5 % of the leaves collected from plants transformed with an empty vector generated plants, 7.8 and 8.0 % of the leaves from plants transformed with the citrus GRF-GIF or rGRF-GIF mut T construct respectively produce de novo shoots from the leaf explants. We also noticed that miR396-resistant GRF-GIF generates large transgenic calli that failed to regenerate shoots. So, we developed a DEX induced version of rGRF-GIF, which would be active only when DEX is added to the media. Preliminary results indicate that the construction is functional and that we can control rGRF-GIF activity exogenously by the addition of DEX. Grape Similarly, to the citrus and soybean GRF-GIF constructs, we generated a grape GRF-GIF by gene synthesis. We then cloned it in pGWB14 vector under 35S promoter. We also generated a version with 4 silent mutations in the miR396 target site of the GRF gene (grape rGRF-GIF). We ran three sets of experiments to compare the transformation efficiency of the grape GRF-GIF, the grape rGRF-GIF chimera, or a vector control (pGWB14 without GRF-GIF) using somatic embryos of the table grape Thompson Seedless. We observed that plants transformed with the grape GRF-GIF developed into plants with a normal phenotype, whereas those transformed with the grape rGRF-GIF developed abnormally with a stunted stature and twisted, distorted leaves. Interestingly, we also noted that somatic embryo inoculated with the rGRF-GIF often produced a much greater number of secondary embryos than embryos inoculated with the non-resistant grape GRF-GIF. Therefore, we plan to use this phenomenon to try to develop an inducible Cas9 system that will allow for multiple independent edited events. We have generated rGRF-GIF constructs that have a DEX inducible Cas9 with gRNAs that will target both the rGRF-GIF and an ortholog gene. We are producing transgenic grape embryos with this construct and generating secondary embryos off the primary transgenic embryos. Once sufficient secondary embryos are produced, we will transfer the cultures to medium containing DEX which will induce Cas9 to inactivate rGRF-GIF and generate knockouts in an ortholog gene. 2. Establish a positive selection method that does not require plant pest sequences. We are testing the ability of the soybean GRF-GIF chimera to stimulate regeneration of transgenic embryos without in use of a selectable marker gene in alfalfa. We transformed in vitro grown trifoliate leaves of the alfalfa line 2525-14 with the GRF-GIF chimera construct or an empty vector control and co-cultured them on medium with or without cytokinin We replicated this study twice. We did not see any significant differences between the number of explants regenerating embryos between the GFR-GIF chimeric construct or the control. One limitation of this approach could be the 35S promoter used to drive GRF-GIF, so we are planning to test a Ubiquitin promoter. We also inoculated citrus epicotyls with a control plasmid or the citrus rGRF-GIF. After co-cultivation, epicotyls were transferred to regeneration medium without antibiotic selection. We monitored the cultures for larger, more aggressive growing shoots, enhanced bud multiplication. However, we were unable to observe any differences in the vigor of shoot development between shoots developing from epicotyls inoculated with rGRF-GIF verses the control construct. 3. Combine GRF-GIF technology with Genome Editing systems for each of the three species to enhance the efficiency of recovery of gene-edited plants. Alfalfa: We have generated a vector containing the soybean GRF-GIF and gRNA to targeting the PDS gene. Grape: We have generated a vector containing the grape GRF-GIF and 3 gRNAs targeting the DELLA domain of the VvGAI1 gene (GSVIVT01011710001). Multiple mutations disrupting the DELLA domain could potentially generate GA insensitive alleles [Amino acid changes (grape), premature stop codons (wheat), or small deletions (Arabidopsis or maize)]. Citrus: We have generated a vector containing the citrus GRF-GIF and a gRNA targeting the CsLOB1 (Jia et al., 2016). We selected this target gene since the activity of the gRNA was already validated in literature and mutations in this gene resulted in improvement of citrus canker resistance in Duncan grapefruit.

    Publications


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

      Outputs
      Target Audience:The target audience includes researchers developing transgenic or gene editing monocotyledonous and dicotyledonous plants. To that end, we have distributed a number of our GRF-GIF vectors to AddGene (https://www.addgene.org/) These vectors are available to researchers in the public domain for use in their research studies. Changes/Problems:Progress on the project was delayed due to the pandemic. For most of 2020 the University of California was on suspended operations with lab occupancy reduced to 33% What opportunities for training and professional development has the project provided?We had hoped to invite other researchers to work in our lab to help them apply the GRF-GIF technology to their crops of interest, but the pandemic has prevented that from happening. How have the results been disseminated to communities of interest?1. Juan M. Debernardi, David Tricoli, Javier Palatnik and Jorge Dubcovsky. A New Transformation Technology That Improves Regeneration Efficiency of Genome Edited Plants (2020). ASA-CSSA-SSSA International Annual Meeting. . 2. Juan M. Debernardi, David Tricoli, Javier Palatnik and Jorge Dubcovsky. GRF-GIF: A New Transformation Technology That Improves Regeneration Efficiency of Genome Edited Plants. Society for In Vitro Biology's virtual annual meeting, SIVB 2021:In Vitro OnLine. 3. Juan M. Debernardi, David Tricoli, Javier Palatnik and Jorge Dubcovsky. GRF-GIF Transformation Technology Improves Regeneration Efficiency of Genome Edited Plants. Masterclasses in Crop Transformation for Genome Editing. 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: Increase regeneration efficiency in multiple cultivars of alfalfa, citrus and Vitis vinifera (grape) using the GRF-GIF technology. Alfalfa To test the GRF-GIF system in alfalfa we decided first to generate a construct using Fabales-specific sequences. To this end, we identified the best GRF and GIF candidate genes from soybean based on sequence homology with GRF and GIF genes from other species that we already have results on improvements on regeneration. We then generated the soybean GRF-GIF gene by gene synthesis in a pDONR vector. The GRF-GIF gene was then subcloned by L/R gateway reaction in the pGWB14 binary vector, which includes a selection marker for Hygromcin and one for Kanamycin. We have also cloned the GRF-GIF gene under a Lotus japonica Ubiquitin promoter in case 35S does not work well. We germinated 10 individual seedlings from alfalfa genotype Highline and from a UC Davis breeding line called 2705 in tissue culture vessels. After germination we created four clones of each of the 10 seedling and collected trifoliate leaves and inoculated them with soybean GRF-GIF and an empty vector (pGWB14 without GRF-GIF). As a positive control, we included leaf explants from seedling line 2525-14 which we have previously identified as being highly amenable to agrobacterium-mediated transformation. We transferred tissue to fresh medium every 14 days. This study will determine if the GRF-GIF technology can increase transformation efficiencies for genotypes that are already amenable to transformation as well as germplasm that are currently recalcitrant to transformation. Citrus The citrus GRF-GIF construct was generated by gene synthesis in a pDONR vector. GRF genes contain a complementary sequence to the microRNA miR396, which represses GRF expression at the post-transcriptional. Since miR396 is expressed at high level in mature tissues, we thought that this repression could limit the expression GRF-GIF during the transformation of this type of leaf or epicotyl tissues. Therefore, we generated two other GRF-GIF versions that included silence mutations in the miR396 target site of the GRF gene. In one version we introduced 4 silent mutations (citrus rGRF-GIF) that we expect would completely eliminate miR396 interaction, and in the second we introduced only one mutation (rGRF-GIF mut T) to reduce but not eliminate miR396 repression. We inoculated in vitro grown epicotyls of the citron rootstock Carrizo with the citrus GRF-GIF, citrus rGRF-GIF, and citrus rGRF-GIF mut T constructs and cultured them on shoot induction medium. We transferred tissue every 21 days to fresh medium until buds developed and subsequently transferred the tissue to elongation medium. We determined the number and percent of inoculated epicotyls that produced transgenic shoots. We observed that seventeen percent of epicotyls inoculated with the control vector produced shoots (78/454), while epicotyls transformed with the citrus GRF-GIF, the citrus rGRF-GIF and the citrus rGRF-GIF mutT produced thirty-two (109/338), twenty-five (27/102) and twenty-four (27/112) percent transgenic shoots respectively. In addition to increasing transformation frequencies, the citrus GRF-GIF produced larger more robust shoots in vitro. Testing regeneration from petiole and leaf explants We have also transferred citrus shoots transformed with the grape and citrus GRF-GIF and resistant GRF-GIF to large culture vessels. We collected leaf and petiole sections from these plants and plated them on medium known to induce organogenesis from citrus epicotyls. We are monitoring the explants for organogenic or embryogenic regeneration to determine if the GRF-GIF chimera gene can enhance regeneration from tissues other than epicotyls. Grape We generated a grape GRF-GIF by gene synthesis. We then cloned it in pGWB14 vector under 35S promoter. We also generated a version with 4 silent mutations in the miR396 target site of the GRF gene to avoid the miRNA regulation (grape rGRF-GIF). We ran three sets of experiments to compare the transformation efficiency of the grape GRF-GIF the grape rGRF-GIF chimera or a vector control (pGWB14 without GRF-GIF) using somatic embryos of the table grape Thompson Seedless. After inoculation, we sub-cultured the embryos every two weeks onto embryo induction medium. The quantity of transgenic embryo developing from the various plate were documented. We observed significant variability in the efficiency of grape transformation from experiment to experiment, and due to this variability, no definitive conclusion could be drawn from these experiments. Interestingly, we noted that plants transformed with the grape GRF-GIF developed in to plants with a normal phenotype whereas those transformed with the grape r-GRF-GIF developed abnormally with a stunted stature and twisted, distorted leaves. We also noted that somatic embryo inoculated with the rGRF-GIF often produced secondary embryos in much great number than embryos inoculated with the non-resistant grape GRF-GIF. Testing regeneration from stems, petiole and leaf explants We harvested leaves, stems and petioles of Thompson Seedless plants transformed with the GRF-GIF, rGRF-GIF and control vectors and plated them on medium known to induce embryogenic callus in grape. All of the explants plated on medium formulated to induce somatic embryos from grape anther filaments developed callus tissue, but none of the calli appears to be embryogenic and none have formed embryos. 2. Establish a positive selection method that does not require plant pest sequences. We are testing the ability of the soybean GRF-GIF chimera to stimulate regeneration of transgenic embryos without in use of a selectable marker gene. We transformed in vitro grown trifoliate leaves of the alfalfa line 2525-14 with the GRF-GIF chimera construct or an empty vector control and co-cultured on medium with or without cytokinin. After three days of co-cultivation, we transferred the leaf pieces to embryo induction medium with or without cytokinin. We anticipate that control tissue cultured on medium without cytokinin will fail to produce. However if alfalfa respond like wheat, cells expressing the chimera gene will form embryos. We also inoculated citrus epicotyls with a control plasmid or the citrus rGRF-GIF. After co-cultivation, epicotyls were transferred to regeneration medium without antibiotic selection. We are monitoring the cultures for larger, more aggressive growing shoots, enhanced bud multiplication or other visual responses which we believed would be indicative of shoots transformed with the GRF-GIF gene. 3. Combine GRF-GIF technology with Genome Editing systems for each of the three species to enhance the efficiency of recovery of gene-edited plants. Alfalfa: We have generated a vector containing the soybean GRF-GIF and gRNA to targeting the PDS gene. Grape: We have generated a vector containing the grape GRF-GIF and 3 gRNAs targeting the DELLA domain of the VvGAI1 gene (GSVIVT01011710001). Multiple mutations disrupting the DELLA domain could potentially generate GA insensitive alleles [Amino acid changes (grape), premature stop codons (wheat), or small deletions (Arabidopsis or maize)]. Citrus: We have generated a vector containing the citrus GRF-GIF and a gRNA targeting the CsLOB1 (Jia et al., 2016). We selected this target gene since the activity of the gRNA was already validated in literature and mutations in this gene resulted in improvement of citrus canker resistance in Duncan grapefruit.

      Publications

      • Type: Journal Articles Status: Published Year Published: 2020 Citation: A GRF-GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nature Biotechnology,2020 Nov;38(11):1274-1279.