Targeted Mutagenesis of NAC Transcription Factor Gene, OsNAC041, Leading to Salt Sensitivity in Rice

doi:10.1016/j.rsci.2018.12.005

摘要/Abstract

关键词: rice, NAC transcription factor, CRISPR, Cas9, RNA-seq, salinity

. [J]. Rice Science, 2019, 26(2): 98-108.

Fig. 1. Expression profile and subcellular location analysis of OsNAC041.A, Quantitative real-time PCR (qRT-PCR) analysis of OsNAC041 expression in samples of root, stem and leaf from two-week-old wild-type (WT) plants. B, qRT-PCR analysis of OsNAC041 expression patterns in WT plants before (NaCl-) and after (NaCl+) salt stress. C, Nuclear localization of OsNAC041 protein in the rice protoplast. NLS, Nuclear localization signal. Scale bar = 20 µm. Data represent Mean ± SE (n = 3). **, Significance at the 0.01 level.

Fig. 2. Targeted mutagenesis of the OsNAC041 locus using CRISPR-Cas9 system.A, Design of sgRNA sites for the OsNAC041 exons. B, Single-strand conformation polymorphism analysis of 10 independent OsNAC041- sgRNA01 T0 lines. M, Marker; WT, Wild-type. C, Sanger sequencing of the target site in the OsNAC041-sgRNA01 T0 lines. D, Phenotypic analysis of OsNAC041 T1 mutant lines under normal condition.

Fig. 3. OsNAC041 targeted mutants showed the salt-sensitive phenotype.A, Germination of OsNAC041 T1 mutant and wild-type (WT) seeds grown on 1/2 MS medium supplemented with NaCl (150 mmol/L). B, Phenotypic analysis of OsNAC041 T1 mutant lines under salt stress. C, Growth of OsNAC041 T1 mutant lines in plugs. D, Levels of O2- and H2O2 in WT and OsNAC041 T1 mutant lines subjected to salt stress. Salt-stressed leaf samples were incubated in nitro-blue tetrazolium (NBT) or diaminobenzidine (DAB) solution. E, Chlorophyll content after 15-day salt stress. F, H2O2 content after 15-day salt stress. G, O2- production rate after 15-day salt stress. H, Malondialdehyde (MDA) content after 15-day salt stress. I, Catalase (CAT) activity after 15-day salt stress. J, Peroxidase (POD) activity after 15-day salt stress. K, Superoxide dismutase (SOD) activity after 15-day salt stress. Data represent Mean ± SE (n = 3). **, Significant at the 0.01 level.

Fig. 4. Targeted knockout of OsNAC041 resulted in global gene expression changes in rice.A, Number of differentially expressed genes (DEGs) in the wild-type (WT) and osnac041 (A/A) T1 mutant lines, based on expression profiles obtained by RNA-Seq. B, Clustering analysis of DEGs in WT and osnac041 T1 mutant lines. Targeted knockout of osnac041 resulted in global changes compared with the WT both with and without salt stress. The color scale corresponds to log2(FPKM) values of the genes. C, Gene ontology classification of DEGs in the following two comparisons: WT and osnac041 T1 mutant lines under normal and salt stress conditions. x-axis shows user selected GO terms; y-axis shows the percentages of genes (number of a particular gene divided by total gene number).

Fig. 5. Transcriptome analysis of genes systemically regulated in the wild-type (WT) and osnac041 T1 mutant lines in response to salt stress.A, Photosynthesis-related genes. B, Peroxisome-related genes. C, Water deprivation-related genes. D, Mitogen-activated protein kinase signal-related genes. E, Eukaryotic-type ABC transporter-related genes. F, Plant hormone regulatory pathway-related genes. Log2(Fold change, FC) of differentially expressed genes in WT and osnac041 T1 mutant lines before (NaCl-) and after (NaCl+) salt stress is defined as [-1.5 > log(FC) > 1.5] with false discovery rate (FDR) < 0.05, and the top 30 most significant differences are shown in the heat-map.

Supplemental Table 1 Result of the NLS-mapper predictions of the location of OsNAC041 expression.

Predicted bipartite NLS position	Sequence	Score
17	DLPGFRFHPTEEELLDFYLSRVVLGKKLHFNI	2.4
37	RVVLGKKLHFNIIGTLNIYRHDPWDLPGMAKI	2.4
37	RVVLGKKLHFNIIGTLNIYRHDPWDLPGMAKIGE	2.1
91	RTTERGFWKATGSDRAIRSSGDPKRVIGLKKTLV	2.2
91	RTTERGFWKATGSDRAIRSSGDPKRVIGLKKTLVFY	2.9
115	RVIGLKKTLVFYQGRAPRGTKTDWVMNEYRLPD	2
141	NEYRLPDYGAARAAAPPPKEDMVLCKIYR	2.9
161	DMVLCKIYRKATPLKELEQRASAMEEMQRGS	2.4
NLS, Nuclear localization signal.

Supplemental Table 2 Oligonucleotides used in this study

Name	Primer sequence
OsActin-RT-F	AGCTGCGGGTATCCATGAGA
OsActin-RT-R	GCAATGCCAGGGAACATAGTG
4324705-RT-F	GTTCTTCGTCCAGGCCATCGTCA
4324705-RT-R	GTAGGCCCATGCGTTGTTGTTGA
4324706-RT-F	GTCTTCGTCAGTGGCAACCTC
4324706-RT-R	GAAACATCTGGCTGAACCTGAG
4324707-RT-F	GGTCGCGTAGTTCAAGTGGG
4324707-RT-R	TCGCCTGACATTATTTCACCAA
4324708-RT-F	TGGACTCGCTGGACCAGAAC
4324708-RT-R	CGGTGTAGGGCTGGAACG
4324709-RT-F	GCAGACGCAGACCAAGAAGAA
4324709-RT-R	GGCGGCAGAGGAAAGAGC
4324710-RT-F	GCCACCATCGAGAAGACGAAGCG
4324710-RT-R	AGCAGGCCGAACTTGCCGTAG
4324711-RT-F	GTGGTTCGGTTCGCCAAGGTG
4324711-RT-R	ATCTCGTCCAGGGCGTAGTTGT
4324712-RT-F	TTGAAGGGATAGGAAGGACC
4324712-RT-R	AGACAGAGTCAGAAGGGAAG
4324713-RT-F	ACTGGAGGAATGTGGGACTGGC
4324713-RT-R	TCACCGACCCGAACAGCAAA
4324714-RT-F	CGCAGCTCCGACAACATCT
4324714-RT-R	GCTGGGTGACACTCTCTCTACAAG
OsNAC041-sgRNA01-F	GTGTGCGTAGGGAGACAGGCAGTGC
OsNAC041-sgRNA01-R	AAACGCACTGCCTGTCTCCCTACGC
NAC041-F	GCAAAATGATCGGAATGAAGTG
NAC041-R	GCGAAGACCAAAAGATTGATTG

Supplemental Fig. 1 Validation of the RNA-seq results by quantitative real-time PCR.

Supplemental Fig. 2 Venn diagram analysis of the differentially expressed genes.

Supplemental Fig. 3 Alignment between OsNAC041 and AtNAC036.

Supplemental Fig. 4 Phylogenetic tree analysis of OsNAC041.

Supplemental Fig. 5 Analysis of photosynthesis-related differentially expressed genes and photosynthesis-antenna proteins.

Supplemental Fig. 6 Analysis of peroxisome-related differentially expressed genes.

Supplemental Fig. 7 Analysis of MAPK signaling-related differentially expressed genes.

Supplemental Fig. 8 Analysis of eukaryotic-type ABC transporter-related differentially expressed genes.

Supplemental Fig. 9 Analysis of plant hormone signal transduction-related differentially expressed genes.

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