Progress 10/01/17 to 09/30/21
Outputs
Target Audience:The target audience for this project is primarily the academic science community, specifically those working on plant biology and plant-microbe interactions. This research also has future agricultural applications and will be of interest to farmers and the general public. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?This project has provided extensive training and professional development opportunities for the graduate student, Zachary Keyser. First and foremost, Zachary has gained substantial experience with molecular biology and plant biology techniques, including some cutting-edge methods such as CRISPR. Zachary has also had many opportunities to present this work at various conferences, lab meetings, and seminars. These experiences have been essential for honing his presentation and communication skills and providing networking opportunities. Furthermore, Zachary has trained several undergraduate students while working on this project. This has been a source of mentoring experience for this graduate student and training opportunities for the undergraduate students. How have the results been disseminated to communities of interest?The results from this research have been presented at numerous seminars across the UW-Madison campus in multiple different departments. Furthermore, current results from the study have been shared at scientific conferences through poster presentations at the UW-Madison Plant Breeding & Plant Genetics 50th Anniversary Symposium, the 2018 Plant Cell Dynamics Conference, and the UW-Madison Plant Breeding & Plant Genetics 9th annual Plant Sciences Symposium. The results have also been disseminated to an international scientific audience at the Plant and Animal Genome conference in San Diego, California, in January 2020. The results of this project have been presented and published in Zachary Keyser's Ph.D. dissertation. This dissertation is searchable in the UW-Madison database and will be publicly available to download. What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
We identified HMGR genes in two sequenced accessions of Medicago truncatula, Jemalong A17, and R108. We found that Jemalong A17 has 11 HMGR genes in the genome, while R108 has eight. We decided to use R108 for further analysis because of the fewer copies of HMGR in the genome. Using the R108 genomic context of the identified HMGRs, we have designed an optimized CRISPR construct that will be stably transformed into M. truncatula R108. This new CRISPR construct will allow us to study the symbiotic activity of five different HMGR genes close to one another in the genome. The CRISPR construct is designed to knock out all five of these genes, reducing or eliminating the effects of genetic redundancy and allowing us to more precisely investigate the roles of individual HMGR genes in symbiosis signaling. To investigate protein interactors of HMGRs, we performed co-immunoprecipitation assays. We generated constructs of each HMGR sequence, and three known symbiotic receptor-like kinases (DMI2, LYK3, and NFP) fused to separate epitope tags for detection with Western blots. These co-immunoprecipitation assays identified HMGR1 as an interactor of all three receptor-like kinases. We are continuing to assess the interactors of the remaining HMGRs through various means, including using a newer method, TurboID, which will identify proteins, including unknown proteins, proximal to HMGRs. We have created and tested an inducible system to place HMGRs in the symbiosis signaling pathway. We designed constructs that contain a constitutively active version of HMGR1 (the catalytic domain of HMGR1) from M. truncatula R108 driven by an ethanol-inducible promoter. We used this construct to transform wild-type M. truncatula and various known M. truncatula symbiosis signaling mutants. Upon induction of HMGR1, we measured the expression of an early nodulation gene, ENOD11. Using this system, we found ENOD11 expression when we induced autoactive HMGR1 in wild-type plants and several mutants in the absence of rhizobia. This indicates that HMGR1 is sufficient to activate the symbiosis signaling pathway and functions downstream of known early symbiosis genes. In addition to the inducible system described above, we have created and tested the ability of two other HMGR1 constructs to activate the symbiosis signaling pathway to validate the results from the inducible system. One of these constructs was designed to overexpress the full-length HMGR1 constitutively, and the other constitutively overexpresses the autoactive version of HMGR1. Using these constructs, we also found ENOD11 expression in wild-type M. truncatula in the absence of rhizobia, similar to what we found using the inducible system. Furthermore, we found the autoactive version of HMGR1 was potentially able to induce greater expression of ENOD11 in the presence of the symbiotic signal. The mechanism of this result can be explored further. Furthermore, we used a biochemical approach to provide additional support for HMGR activity in symbiotic signaling. HMGRs are integral in the mevalonate pathway; we, therefore, utilized inhibitors that block various stages of the mevalonate pathway to determine their effect on symbiosis signaling. We found that direct inhibition of HMGRs by the pharmaceutical compound lovastatin decreased ENOD11 expression in response to symbiotic signals. We also found that a farnesyl pyrophosphate synthase inhibitor reduces the symbiotic response, evidenced by decreased ENOD11 expression. These results support the model that HMGRs are essential for symbiotic signaling and suggest downstream products from the mevalonate pathway are also involved in this signaling.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2022
Citation:
Kleist TJ, Bortolazzo A, Keyser ZP, Perera AM, Irving TB, Venkateshwaran M, Atanjaoui F, Tang, RJ, Maeda J, Cartwright HN, Christianson ML, Lemaux PG, Luan S, An� JM (2022). Stress-associated developmental reprogramming in moss protonemata by synthetic activation of the common symbiosis pathway. iScience 25(2) 103754.
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Progress 10/01/19 to 09/30/20
Outputs
Target Audience:This research's initial target audience is the academic science community, especially those involved in the plant-microbe symbiosis and nitrogen fixation field. With the future applications impacting the agricultural field, our findings will ultimately be of interest to farmers and the entire general public since they will benefit from the improved agricultural production. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?The project provided many opportunities for the professional development of a graduate student, Zachary Keyser. He obtained extensive training in classical molecular biology and plant biology techniques and options for exploring other methods on his own. The project has also provided a graduate student with mentoring experience. Under this research project, he mentored five undergraduate students on various tasks related to the topic. This project has also provided these undergraduate students with beneficial exposure to general lab work and hands-on learning of essential techniques, methods, and experimental preparation. How have the results been disseminated to communities of interest?The proposed research and results have been presented at numerous seminars across the UW-Madison campus in multiple departments. Results from the study were shared at scientific conferences through poster presentations at the UW-Madison Plant Breeding & Plant Genetics 50th Anniversary Symposium, at the 2018 Plant Cell Dynamics Conference, and the UW-Madison Plant Breeding & Plant Genetics 9th annual Plant Sciences Symposium. Our most recent results on the involvement of HMGRs in symbiosis were shared with other scientific community members at the 2020 Plant and Animal Genome conference in San Diego, California, on January 11-15th. What do you plan to do during the next reporting period to accomplish the goals?We are currently assessing the ability of HMGR1 to rescue the nodulation defects in the hmgr1-1 mutant line. This experiment will determine whether the transposon insert in HMGR1 or CCaMK is responsible for the observed phenotype. To clarify the current results of the amiRNA experiments, we are also evaluating the effectiveness of the amiRNAs by measuring the expression level of the various HMGRs in the transformed plants with qRT-PCR. The final amiRNA experiment targeting HMGR6 is in the process of determining the effect on nodulation, and we will be getting the results for this shortly. Additionally, we plan to test the remaining M. truncatula R108 HMGRs for their ability to interact with each of the symbiotic receptor-like kinases. Multiple protein-protein interaction systems have been obtained and designed for the use of testing these interactions. By the next reporting period, we expect to receive the results of both the Co-IP and split-luciferase experiments, identifying and confirming the interactions between HMGRs and symbiotic receptor-like kinases. As we have confirmed HMGR activity can stimulate the symbiotic signaling pathway, we plan to use this newly created system for identifying where in the pathway, in relation to known components, HMGRs are involved. We have various plant lines with mutants in molecular components involved in different steps of the pathway. Specifically, we hypothesize HMGRs transduce the signal from the plasma membrane to the nuclear envelope, so we are testing the effect of triggering HMGR activity on the symbiotic response in two mutants, dmi2 and dmi1, which play a role before and after this processes, respectively. These findings from these experiments, which will be accomplished shortly, will help piece together the missing steps in the pathway. As a follow-up to our finding that inhibitors of early steps in the mevalonate pathway can block subcellular signaling for symbiotic responses, we aim to dissect further which steps and products of the mevalonate pathway are involved in this process. Inhibitors of enzymes at different branch points of the mevalonate will be used to determine their ability to inhibit symbiotic responses. By the next reporting period, we will be determining if the prenylation of proteins is essential for symbiotic signaling by testing the ability of prenyltransferase inhibitors to prevent Nod factor triggered ENOD11 expression.
Impacts
What was accomplished under these goals?
We identified all HMGR gene sequences of Medicago truncatula R108 and Medicago truncatula cultivar Jemalong A17 in the most recent genome assemblies through thorough bioinformatics analyses. This search revealed that M. truncatula R108 has 8 HMGR genes, while M. truncatula accession Jemalong A17 contains 11. This information led us to conclude that M. truncatula R108 is the best genetic background for our study. With clear identification of all M. truncatula HMGR genes of interest, we are now assessing each HMGR gene's role in symbiotic association with rhizobia. We have identified M. truncatula retrotransposon insertion mutant lines as candidates to contain an insertion in genes of the HMGR family. At least one insertion line corresponding to each different M. truncatula isoform was obtained from the Noble Research Institute. By PCR genotyping, we identified insertion mutants in HMGR1, HMG2b, HMGR2c, HMGR3, HMGR4, and HMGR5. Homozygous mutants of each of these lines was selected and bulked for phenotyping. Additionally, we pinpointed the retrotransposon insert's precise location in each of the genes of interest through sequencing. We phenotyped these phenotypes for various symbiotic characteristics. Both hmgr1-1 and hmgr2-1 mutant lines exhibited no defects in nodule number as compared to wild-type plants but produced nodules that were defective in their ability to fix nitrogen. Surprisingly, a separate hmgr1 mutant line (hmgr1-2) formed fully functional nodules. Through further assessment of the hmgr1-1 and hmgr2-1 mutant lines, we later discovered and verified additional retrotransposon inserts in genes with known roles in the symbiotic signaling pathway, which are likely responsible for these symbiotic defects. The remaining identified homozygous HMGR insertion mutants (hmgr3, hmgr4, and hmgr5) were also assessed for the same phenotypes mentioned above, but none were observed. These findings suggest that one of the untested HMGRs (HMGR2a or HMGR6) may be involved in symbiotic signaling, or more likely a role for multiple HMGRs in forming symbiotic associations. To test these hypotheses, we targeted multiple HMGRs with artificial micro RNAs (amiRNAs) for simultaneous knockdown of expression. To rule out the chance of a single HMGR being solely involved in symbiotic signaling, we also designed amiRNAs for HMGR2a and HMGR6, which did not have corresponding retrotransposon insertion mutant lines. We are currently evaluating the symbiotic phenotypes of these transgenic roots. To further determine the mechanism as to how HMGRs function in symbiotic signaling, we investigated possible protein interactors of HMGRs. We generated constructs of each HMGR sequence, and the symbiotic receptor-like kinases (NORK, LYK3, and NFP) fused to separate epitope tags for detection with Western blots. So far, Co-IPs identified HMGR1 as an interactor of LYK3 and NFP as well as NORK. We are continuing to assess the interactors of the remaining HMGRs. As another way to test for the protein interactions between HMGR1 and the symbiotic receptor-like kinases, we have also created the necessary constructs for a split-luciferase assay in Nicotiana benthamiana. This approach includes constructs for each pairwise combination of each HMGR fused to half of a luciferase gene along with one of NORK, LYK3, or NFP fused to the other half of the luciferase gene. To examine the ability of HMGRs to active symbiotic responses and confirm the involvement of HMGRs in the common symbiosis pathway, we tested the effect of autoactive HMGR in M. truncatula. We created constructs with an inducible ethanol promoter driving the expression of the catalytic domain of HMGR1, which is constitutively active, and transformed it into Medicago. The activation of HMGR activity with ethanol led to strong expression of the early nodulation gene, ENOD11. Our result confirmed that HMGR activity is sufficient to stimulate the common symbiosis signaling cascade. Additionally, we used a biochemical approach to provide further support for HMGR activity in symbiotic signaling. As HMGRs perform the mevalonate pathway's rate-limiting step, we investigated whether inhibitors of different stages in this pathway can prevent symbiotic signaling. As expected, inhibition of HMGRs directly by lovastatin decreased the symbiotic response of MtENOD11 expression in response to Nod factors. We also found that a farnesyl pyrophosphate synthase inhibitor is also capable of reducing this symbiotic response. These findings support that HMGRs are essential for symbiotic signaling and suggest downstream products from the mevalonate pathway in transducing the subcellular signaling required for symbiotic responses.
Publications
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2020
Citation:
Keyser, Z., Jayaraman, D., Riely, B., Cook, D., An�, J.-M. Root nodulation requires multiple 3-hydroxy-3-methylglutaryl coenzyme A reductates in Medicago truncatula. Poster presented at the Plant and Animal Genome Conference; 2020 Jan 11-15; San Diego, CA.
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Progress 10/01/18 to 09/30/19
Outputs
Target Audience:The primary target audience for this research is the academic science community, especially those also involved in the plant-microbe symbiosis and nitrogen fixation fields. With the future applications having an impact on the agricultural field, our findings will ultimately be of interest to farmers and the entire general public since they will benefit from the improved agricultural production. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?The project has provided several opportunities for the professional development of a graduate student, Zachary Keyser. He obtained extensive training in classical molecular biology and plant biology techniques, as well as opportunities for exploring other methods on his own. The project also provided the graduate student with mentoring experience. Under this research project, he has mentored five undergraduate students on small projects relating to the topic. This also provided these undergraduate students with beneficial exposure to general lab work and hands-on learning of essential techniques, methods, and experimental preparation. How have the results been disseminated to communities of interest?The results from this research have been presented at numerous seminars across the UW-Madison campus in multiple different departments. Current results from the study have been shared at scientific conferences through poster presentations at the UW-Madison Plant Breeding & Plant Genetics 50th Anniversary Symposium, at the 2018 Plant Cell Dynamics Conference, and the UW-Madison Plant Breeding & Plant Genetics 9th annual Plant Sciences Symposium. With new results coming shortly, the current and further information attained on the involvement of HMGRs in symbiosis will be shared with other members of the scientific community at the 2020 Plant and Animal Genome conference in San Diego, California, in January 2020. What do you plan to do during the next reporting period to accomplish the goals?We are currently assessing the remaining identified homozygous HMGR insertion mutants (hmgr2b, hmgr3, hmgr4, and hmgr5) for defects root nodulation, as was completed for the hmgr1-1 and hmgr2-1 mutants. The particular step of symbiosis which is affected will be determined for each mutant by the next reporting period. Along with the assessment of these individual mutants, we expect to have the CRISPR/cas9 system for deleting multiple HMGRs optimized. As we have the CRISPR constructs for the deletion of four HMGRs already transformed into Agrobacterium rhizogenes, this system will be optimized shortly. With this, we will soon have the results for the assessment of the symbiotic phenotype caused by multiple HMGR knockout mutants, along with the evaluation of the individual mutants. Additionally, we plan to test protein interactions between the eight M. truncatula R108 HMGRs with each of the symbiotic receptor-like kinases. Multiple protein-protein interaction systems have been obtained and designed for the use of testing these interactions. In addition to having the cloning completed for the CoIP and split-luciferase systems, we will also complete the cloning necessary for testing all the interactions of split-ubiquitin yeast-two hybrid. As split-ubiquitin yeast-two hybrid is a quick method for high throughput screening of interactions, we will have the results for which HMGRs interact with the receptor-like kinases with this method by the next reporting period.
Impacts
What was accomplished under these goals?
Through bioinformatic analysis, we identified all HMGR genes in the Medicago truncatula R108 and accessions Jemalong A17 in the most recent genome assemblies. This study revealed M. truncatula R108 contains 8 HMGR genes, while Jemalong A17 contains 10 of them. This information led us to choose R108 as the best line for this study. We are now assessing the role of each HMGR gene in symbiotic associations with rhizobia and arbuscular mycorrhizal fungi. We have identified various M. truncatula retrotransposon insertion mutant lines as candidates to contain an insertion in genes of the HMGR family. By PCR genotyping, we identified insertion mutants in HMGR1, HMG2b, HMGR2c, HMGR3, and HMGR4. Homozygous mutants of each of these lines have already been selected and bulked for characterization. With these mutants, we have begun to characterize them for various symbiotic phenotypes. The hmgr1-1 mutant line exhibits no defects in nodule number as compared to wild-type plants but produces nodules that are defective in their ability to fix nitrogen. We observed a similar phenotype with the hmgr2-1 mutant. The remaining identified homozygous HMGR insertion mutants are currently being analyzed. Our recent findings indicate that multiple HMGRs are involved in the development of symbiotic associations. As we expect that multiple M. truncatula HMGRs may have a functionally redundant role in symbiosis, we created a CRISPR/Cas9 construct that targets a region of the genome containing four HMGRs located in tandem. With this construct, the four best candidates to have a role in symbiosis will be deleted at once. Currently, we are assessing the efficiency of the system to eliminate the full region in M. truncatula transgenic roots. We are also in the process of assessing the interactions of M. truncatula HMGR proteins with known players in the common symbiotic signaling pathway. Constructs containing all the necessary parts for co-immuno-precipitation in Nicotiana benthamiana have been generated through GoldenGate assembly. This includes plasmids containing each pairwise combination of an epitope-tagged HMGR1 sequence along with epitope-tagged versions of the receptor-like kinases, NORK, LYK3, and NFP. Through Western blots of the transformed plant extracts, we have optimized the expression and detection methods of the tagged proteins. As another approach to test for these protein interactions, we have also created constructs for a split-luciferase assay. This includes constructs for each pairwise combination of HMGRs fused to half of the luciferase along with one of NORK, LYK3, or NFP combined to the other half of the luciferase.
Publications
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2019
Citation:
Keyser, Z., Jayaraman, D., Riely, B., Cook, D., An�, J.-M. Multiple Medicago truncatula 3-hydroxy-3-methylglutaryl coenzyme A reductases are required for root nodule development. Poster presented at the Midwest Plant Cell Dynamics; 2018 May 29-Jun 1; Madison, WI.
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2019
Citation:
Keyser, Z., Jayaraman, D., Riely, B., Cook, D., An�, J.-M. Multiple Medicago truncatula 3-hydroxy-3-methylglutaryl coenzyme A reductases are required for root nodule development. Poster presented at the Plant Breeding and Plant Genetics 50th Anniversary Symposium; 2018 Jun 7-8; Madison, WI.
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2019
Citation:
Keyser, Z., Jayaraman, D., Riely, B., Cook, D., An�, J.-M. Root nodulation requires multiple 3-hydroxy-3-methylglutaryl coenzyme A reductates in Medicago truncatula. Poster presented at the 9th Annual Plant Sciences Symposium; 2019 Nov 15; Madison, WI.
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Progress 10/01/17 to 09/30/18
Outputs
Target Audience:The initial target audience for this research is the academic science community, especially those also involved in the plant-microbe symbiosis and nitrogen fixation field. With the future applications having an impact on the agricultural field, our findings will ultimately be of interest to farmers and the entire general public since they will benefit from the improved agricultural production. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?The project has provided many opportunities for the professional development of a graduate student, Zachary Keyser. He has obtained extensive training in classical molecular biology and plant biology techniques as well as opportunities for exploring other methods on his own. The project has also provided the graduate student with mentoring experience. Under this research project, he has mentored two undergraduate students on small projects relating to the topic. This has also provided these three undergraduate students with beneficial exposure to general lab work and hands-on learning of essential techniques, methods, and experimental preparation. How have the results been disseminated to communities of interest?So far, the proposed research plans have been presented at seminars across the UW-Madison campus in multiple different departments. Current results from the research have been shared through poster presentations at the UW-Madison Plant Breeding & Plant Genetics 50th Anniversary Symposium and at the 2018 Plant Cell Dynamics Conference. With new results coming shortly, the information attained on the involvement of HMGRs in symbiosis will be shared with other members of the scientific community. This will be in the form of several presentations at conferences relating to plant-microbe symbioses. What do you plan to do during the next reporting period to accomplish the goals?We are currently determining the HMGR1 expression level in the HMGR1 insertion mutant, as well as working on further assessing the other Tnt1 HMGR insertion mutant for the insertion location and different symbiotic phenotypes. The remaining Tnt1 lines we ordered will also be genotyped to determine the location of the insert, and the homozygous seeds will be bulked for use in determining their symbiotic phenotypes. As we anticipate that multiple Medicago HMGRs may have a functionally redundant role in symbiosis, we will also create a CRISPR/Cas9 construct that targets the five tandem HMGRs for deletion. This construct, also containing a selectable marker, will then be introduced into Medicago and we will generate a stable line that does not contain HMGR1, HMGR2a, HMGR2b, HMGR2c, and HMGR2d. We will then bulk the seeds and begin characterizing the plants for their symbiotic phenotypes, such as nodulation. Subsequently, also in this time frame, we plan to test the interaction of HMGR1 with each of the receptor-like kinases, LYK3, NFP, and NORK. We will perform Co-IPs with each combination and detect for the interactions with Western blots.
Impacts
What was accomplished under these goals?
Through a bioinformatic analysis, we identified all the HMGR genes in the updated genome assembly of Medicago truncatula R108. This study revealed that our model organism contains 8 HMGR genes. We are now assessing the role of each HMGR gene in symbiotic associations with rhizobia and arbuscular mycorrhizal fungi. We have identified various Medicago truncatula retrotransposon insertion mutant lines as likely candidates to contain an insertion in genes of the HMGR family. At least one insertion line corresponding to each different M. truncatula isoform has been ordered from the Noble Foundation and obtained. So far, by PCR genotyping we identified a mutant containing an insert disrupting the Medicago truncatula R108 HMGR1 gene and that the insert is homozygous. Additionally, we identified another insertion line which contains an insert interrupting a different HMGR. Although it is currently unclear which HMGR gene the insert is in, PCR genotyping shows it is not in HMGR1. With these mutants mentioned above, we have begun to phenotype them for various symbiotic characteristics. Currently, we are assaying plants containing the insert in the unknown HMGR for the ability of Nod factors to trigger the symbiosis-specific response of nuclear calcium spiking. Although all experimental replicates have not been completed, our initial findings show a decrease in nuclear calcium spiking response compared to wild-type plants. This suggests a role for this HMGR in symbiotic signaling and the ability to form symbiotic associations. To begin studying the interactions of Medicago HMGR proteins with known players in the common symbiotic signaling pathway, a system for checking the protein interactions needs to be generated. Constructs containing all the necessary parts for co-immuno-precipitation in Nicotiana benthamiana have been created through Golden Gate assembly. This includes plasmids containing each pairwise combination of an epitope-tagged HMGR1 sequence along with an epitope-tagged version one of the receptor-like kinases, NORK, LYK3, or NFP, involved in detecting microbial signals for initiating symbiotic signaling. We have tested each of these plasmids and have confirmed the ability of each of them to be expressed in planta. Through Western blotting of the transformed plant extracts, we have optimized the expression and detection methods of the tagged proteins. As another way to test for the protein interactions between HMGR1 and the symbiotic receptor-like kinases, we have also created the necessary constructs for a split-luciferase assay in Nicotiana benthamiana. This includes constructs for each pairwise combination of HMGR1 fused to half of a luciferase gene sequence along with one of either NORK, LYK3, or NFP fused to the other half of the luciferase gene. We have also designed a plasmid containing a nuclear-localized calcium sensitive green fluorescent protein to be expressed in a stable line of Medicago. Currently, we are transforming Medicago with this construct and generating a stable line. This will allow for the visualization of changes in calcium concentrations in the nucleus. Using this line will increase the efficiency of future experiments. We will be able to perform various tests where the symbiotic signaling pathway is altered genetically or biochemically in the line and determine the effects they have on calcium spiking. Specifically, we will over-activate HMGR activity and assess for spontaneous nuclear calcium spiking.
Publications
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2018
Citation:
Keyser, Z., Jayaraman, D., Riely, B., Cook, D., An�, J.-M. Multiple Medicago truncatula 3-hydroxy-3-methylglutaryl coenzyme A reductases are required for root nodule development. Poster presented at the Midwest Plant Cell Dynamics; 2018 May 29-Jun 1; Madison, WI.
- Type:
Conference Papers and Presentations
Status:
Accepted
Year Published:
2018
Citation:
Keyser, Z., Jayaraman, D., Riely, B., Cook, D., An�, J.-M. Multiple Medicago truncatula 3-hydroxy-3-methylglutaryl coenzyme A reductases are required for root nodule development. Poster presented at the Plant Breeding and Plant Genetics 50th Anniversary Symposium; 2018 Jun 7-8; Madison, WI.
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