Source: CORNELL UNIVERSITY submitted to NRP
ENHANCING CHILLING TOLERANCE IN RICE AND MAIZE BY MODIFYING A CASEIN KINASE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1017095
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2018
Project End Date
Sep 30, 2022
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
CORNELL UNIVERSITY
(N/A)
ITHACA,NY 14853
Performing Department
Plant Biology
Non Technical Summary
Chilling stress poses a threat to the growth and reproduction of major crop plants including cereals, vegetables and fruits. Recent events of extreme temperature fluctuations have caused yield losses of many agricultural products. Breeding chilling tolerant plants is an effective way to enhance the production under extreme conditions and expand growth area and growth season of crop plants. Earlier studies using natural variations of chilling tolerance in rice has identified CAK1 as a critical gene for chilling tolerance and a CAK1 variant associated with high tolerance. This project aims at using this elite natural variant of CAK1 to improve chilling tolerance in maize and rice. Four major objectives of this research are: 1) determine the function of CAK1 in chilling tolerance in maize, 2) establish the activities of the two CAK1 variants in rice, 3) determine the effectiveness of using CAK1-in4 in chilling tolerance enhancement in maize, 4) identify pathways/processes regulated by CAK1 genes using RNA-Seq. Together, this study will provide genetic materials and gene resources for breeding chilling tolerant crops. It will also forward our understanding of chilling tolerance mechanism and therefore will advance fundamental knowledge of plant adaptation to the environment.
Animal Health Component
50%
Research Effort Categories
Basic
30%
Applied
50%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
20115101080100%
Knowledge Area
201 - Plant Genome, Genetics, and Genetic Mechanisms;

Subject Of Investigation
1510 - Corn;

Field Of Science
1080 - Genetics;
Goals / Objectives
Chilling stress (low but non-freezing temperature) poses a threat to the growth and reproduction of major crop plants including cereals, vegetables and fruits. Recent events of extreme temperature fluctuations have caused yield losses of many agricultural products. Breeding chilling tolerant plants is an effective way to enhance the production under extreme conditions and expand growth area and growth season of crop plants. Compared to conventional breeding, molecular breeding is more effective and faster. However,it is limited by the lack of sufficient knowledge of chilling tolerance and the availability of genes and elite alleles contributing to chilling tolerance in crops.Current knowledge on low temperature responses largely comes from freezing tolerance studies in Arabidopsis thalianawhich is a chilling tolerant plant (Thomashaw, 1999; Hua, 2009). A large number of crop plants includingmaize and ricehave tropical and subtropical origins and arechilling sensitive, unlike Arabidopsis thaliana. My research group has started using rice as a model for chilling tolerance studies. Besides its small genome and ample research resources,rice has rich variations in chilling tolerance resulting froma large number of quantitative trait loci (QTL), making it a good model for chilling tolerance studies. We haveidentified several QTLs usinggenome wide association study for chilling tolerance at seedling stage in rice.One candidate gene for a major QTL for chilling tolerancehas been verified ascasein kinase 1 (CAK1). Using CRISPR/CAS9 method, we generated two knockout mutants of the OsCAK1 gene, and both of them exhibited reduced chilling tolerance compared to the wild type assayed by tolerance index, survival rate and ion leakage. In addition, polymorphisms in the OsCAK1 gene were found to be correlated with chilling tolerance in rice varieties. In particular,a haplotype of OsCAK1 that encodes a protein variant with an extra 4 amino acids is correlated with high chilling tolerance. Furthermore, this CAK1-in4 variant had a higher kinase activity than the other variantwhen assayed in vitro. Therefore, CAK1-in4 is a promising natural variant or elite allele of CAK1 that confers chilling tolerance in rice, and identified one causal gene and a potential allele that is associated with high chilling tolerance. The proposed researchaims at translating this finding from rice into maize to facilitate the breeding of chilling tolerant maize and other crops.Four major objectives of this research are:1. Determine the function of CAK1 in chilling tolerance in maize2. Establish the activities of the two CAK1 variants in rice3. Determine the effectiveness of using CAK1-in4 in chilling tolerance enhancement in maize4. Identify pathways/processes regulated by CAK1 genes using RNA-Seq.
Project Methods
1. Determine the function of CAK1 in chilling tolerance in maize.Maize has one CAK1 gene (we will refer as ZmCAK1) that appears to be orthologous to the rice CAK1 gene based on tree analysis. We will use CRISPR/CAS9 technology (Peng et al 2018) to knockout the activity of ZmCAK1 in maize. Constructs will be made to target the ZmCAK1 gene and transgenic maize plants will be generated via Agrobacterium mediated transformation at the Cornell transformation facility. Transgenic plants will be assayed by PCR and sequencing to identify those with desired mutations at ZmCAK1 that would cause disruption of the gene function. Progenies of the transgenic lines will be selected for CAS9 free and homozygous for the knockout mutations. At least three independent lines will be assayed for chilling tolerance with the wild type plant as control. Survival rate, leaf death, and ion leakage will be measuredduring or after chilling treatment to indicate the level of tolerance.Once a chilling sensitive phenotype is established for these lines, co-segregation analysis among progenies of a heterozygous plant can be used to corroborate the mutant phenotype.2. Establish the activity of the twovariants of OsCAK1 in rice.The OsCAK1-in4 variantwith an extra 4 residues was shown to havea higher protein kinase activity at chilling temperature, and this variation is associated with higher chilling tolerance in the natural population of indica rice. We will use transgenic approachto confirm that this variant of CAK1 indeed could enhancechilling tolerance. We will transformOsCAK1-int4 and OsCAK1 (from the reference accession) into the Oscak1 knockout mutant respectively. Four independent transgenic plants of eachvariant will be assayed for chilling tolerance by both cold tolerance index and survival rate in the second generation. We expect that those with OsCAK1-in4 will have a higher tolerance than those with OsCAK1.3. Determine the effectiveness of using CAK1 variants in chilling tolerance enhancement in maize.We will analyzenatural variants of ZmCAK1 in maize natural populations. Similar adaptation or selection may have occurred in ZmCAK1 as in OsCAK1leading to variationsat the ZmCAK1 gene associated with chilling tolerance. If so, we will transform the high tolerant variant and a reference variant into the ZmCAK1 knockout plants. Transgenic lines will be assayed for chilling tolerance to determine if indeed the variant confers higher chilling tolerance. If no apparent variants could be identified in existing maize varieties, we will generate an equivalent variant of ZmCAK1-in4 by in vitro mutagenesis. The reference ZmCAK1 and ZmCAK1-in4 variants will be transformed into the maize ZmCAK1 knockout plant respectively. Transgenic plants will be assayed for chilling tolerance to determine the effect of ZmCAK1-in4.4. Identify pathways/processes regulated by CAK1 genes using RNA-Seq.To better understand chilling tolerance mechanism, we willanalyze transcriptome changes in theCAK1 mutants to reveal potential pathways and processes associated with chilling tolerance. We will compare the transcription profiles of knockout mutants of OsCAK1 and ZmCAK1 to those of their respective wild types under chilling stress. The cak1 mutants and the wild-type plants will be grown at normal temperature till 3 leaf stage and then be transferred to a low temperature. RNA samples prepared from leaf tissues collected at 0 hour (hr), 3hr and 24hr after chilling will be submitted to Cornell Sequencing Facility where 3'-RNA-Seq will be conducted. Differentially expressed genes (DEGs) between wild type plants and the mutants will be identified in rice and maize respectively. DEGs shared between the Oscak1 and Zmcak1 mutants under chilling will be selected. Specifically enriched GO terms in these DEGs may reveal the pathway(s) that is defective in the cak1 mutants andlikely important for chilling tolerance. This analysis will form the foundation for further mechanistic investigation oftolerance mechanism and provide additional resource for candidate gene selection to improve chilling tolerance.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:The efforts have reached to undergraduate students who were taking either a laboratory course on plant genetic engineering or were working as independent study in my group. The students learned the concept of genome editing (as used in this project) and genetic improvement of crops through genetic variations. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Nothing Reported 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?We will identify and characterize the maize CAK1 mutant generated by the transformation facility. We will further investigate the importance of pathways revealed by RNAseq for chilling tolerance in maize. We will characterize chilling tolerance properties of transgenic lines carrying the two rice haplotypes.

Impacts
What was accomplished under these goals? Here are what we have accomplished under the four objectives 1. Determine the function of CAK1 in chilling tolerance in maize We have generated CRISPR/Cas9 construct for knocking out the gene function. The construct has been sent to the maize transformation facility in Iowa. The transgenic lines are expected to come out early spring of 2021. 2. Establish the activitiesof the two CAK1variantsin rice We have transformed the two variants of CAK1 haplotypes in rice and transgenic lines are now generated. They are being propagated for further characterization. 3. Determine the effectiveness of using CAK1-in4 in chilling tolerance enhancement in maize We are waiting for the CAK1 mutant in maize for this transformation. Because natural variations of CAK1 are identified in maize, we will use alternative approach (such as association study among natural accessions)to investigate the effectiveness of the CAK1 variant in maize. 4. Identify pathways/processes regulated by CAK1 genes using RNA-Seq. We have carried out an RNA seq analysis of maize accessions containing a functional CAK1 (two accessions) and a non-functional CAK1 gene (two accessions) grown under normal and chilling conditions. Preliminary studies have revealed that the ABA response and the JA response are different between these accessions, likely contributing to the chilling tolerance difference. Additional activities related to chilling tolerance in maize 1. We have analyzed the RNAseq data on tissue specificity as well as local and distal response. We found that different tissues have both shared and distinct responses to chilling and meristem tissues differ from differentiated tissues. Differential responses in local and distal tissues from chilling are also observed. The involvement of hormone and stress response pathways in chilling tolerance is tested by comparing chilling tolerant and chilling susceptible accessions. The findings are now being prepared for a manuscript publication.

Publications


    Progress 10/01/18 to 09/30/19

    Outputs
    Target Audience: Nothing Reported Changes/Problems:Because we have already identified natural variants of CAK1 in maize and these variations are associated with chilling tolerance, we do not need to use CAK1 variant in rice for functional studies. Instead, we will directly use maize CAK1 variants for functional study. They can be directly used in maize breeding for chilling tolerance improvement. What opportunities for training and professional development has the project provided? Nothing Reported 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?We are now verifying the function of maize CAK1 by generating its mutant by CRISPR/Cas9 in the accession with theCAK1 wild type variant. In the next reporting period, we will generate CAK1 mutant using the Plant Transformation Facility and will characterize the mutants when they are ready. We are also starting the chilling treatment on several accessions with either wild type or LOF CAK1 variants for RNA-seq experiment. We will analyze transcriptome profiles of CAK1 wild type variant and LOF variant under chilling to reveal how CAK1 might affect chilling tolerance.

    Impacts
    What was accomplished under these goals? We have made significant progress toward identifying the function of maize CAK1 and obtained exciting new leads in natural variants of CAK1 in maize. We have surveyed the maize CAK1 gene in the maize diversity panel with 282accessions. To our surprise and delight, wefound three major types of variants of CAK1 gene with two predicted to be loss-of-function (LOF). Interestingly, more tropical accessions tend to have the LOF variant. In addition, we found that chilling tolerance in accessions with the LOF CAK1 variant were more chilling tolerant thanaccessions with the wild type CAK1, These datasupport the hypothesis that CAK1 confers chilling tolerance.

    Publications