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Research ArticleENVIRONMENTAL STRESS AND ADAPTATION
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Arabidopsis CBF3/DREB1A and ABF3 in Transgenic Rice Increased Tolerance to Abiotic Stress without Stunting Growth

Se-Jun Oh, Sang Ik Song, Youn Shic Kim, Hyun-Jun Jang, Soo Young Kim, Minjeong Kim, Yeon-Ki Kim, Baek Hie Nahm, Ju-Kon Kim
Se-Jun Oh
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Sang Ik Song
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Youn Shic Kim
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Hyun-Jun Jang
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Soo Young Kim
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Minjeong Kim
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Yeon-Ki Kim
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Baek Hie Nahm
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Ju-Kon Kim
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Published May 2005. DOI: https://doi.org/10.1104/pp.104.059147

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  • Figure 1.
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    Figure 1.

    Production of Ubi1:CBF3 and Ubi1:ABF3 plants. A, Ubi1:CBF3 and Ubi1:ABF3 consist of the maize ubiquitin promoter (Ubi1) linked to the CBF3 and ABF3 coding regions, respectively, and the 3′-region of the potato proteinase inhibitor II gene (3′pinII), and a gene expression cassette that contains the 35S promoter, the bar coding region, and the 3′-region of the nopaline synthase gene (3′nos). The entire expression cassette is flanked by the 5′-matrix attachment region (MAR) of the chicken lysozyme gene (Phi-Van and Strätling, 1996). B, RNA gel-blot analysis was performed using total RNAs from young leaves of 6 Ubi1:CBF3 (top) and 5 Ubi1:ABF3 (bottom) lines and from NC plants. The blots were hybridized with the CBF3 and ABF3 probes (described in Supplemental Fig. 1) and reprobed with the rice RbcS gene (Kyozuka et al., 1993). Ethidium bromide (EtBr) staining of total RNA was for equal loading of RNAs.

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    Figure 2.

    Growth characteristics of Ubi1:CBF3 and Ubi1:ABF3 plants. A, Growth phenotypes of 3 independent T4 homozygous lines for Ubi1:CBF3, Ubi1:ABF3, and NC plants at indicated days after germination (DAG). B, Dry weight and fresh weight accumulation of Ubi1:CBF3, Ubi1:ABF3, and NC plants. Plants grown in the greenhouse during the same time course shown in A were harvested and fresh and dry weight/10 plants measured. Each data point represents the mean ± sd of triplicate experiments with three different transgenic lines.

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    Figure 3.

    Appearance of plants and changes in chlorophyll fluorescence during drought stress. A, Four and three independent T4 homozygous lines for Ubi1:CBF3 and Ubi1:ABF3, respectively, and NC seedlings were grown in the greenhouse for 4 weeks and then subjected to 4 d of drought stress followed by 5 to 7 d of watering. Eighteen plants per each line were tested. Photos were taken at 1- or 2-d intervals; + followed by number denotes days of watering. B, Fv/Fm of the transgenic and NC plants in the same time course of drought stress shown in A was measured using a pulse modulation fluorometer (mini-PAM). Fv/Fm is a measure of accumulated photooxidative damage to PSII. Each data point represents the mean ± se of triplicate experiments (n = 6).

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    Figure 4.

    Changes in chlorophyll fluorescence during drought, high-salinity, and low-temperature stresses. Three independent T4 homozygous lines for Ubi1:CBF3, Ubi1:ABF3, and NC seedlings grown in the greenhouse for 14 d were subjected to various stress conditions as described: for drought stress, the seedlings were air-dried for 2 h at 28°C and for high-salinity stress seedlings were exposed to 400 mm NaCl for 2 h at 28°C. For low-temperature stress, they were exposed to 4°C for 6 h. All of the experiments were carried out under continuous light of 150 μmol m−2 s−1. Each data point represents the mean ± se of triplicate experiments (n = 6).

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    Figure 5.

    Induction of stress-related genes in Ubi1:CBF3 and Ubi1:ABF3 plants. Three independent T4 homozygous lines for Ubi1:CBF3, Ubi1:ABF3, and NC seedlings were grown in the greenhouse for 14 d. Transgenic and NC plants were then treated for 2 h with drought (the seedlings excised before being air-dried for 2 h), high salinity (400 mm NaCl) at the greenhouse, and with low-temperature stress (4°C) at the cold chamber under continuous light of 150 μmol m−2 s−1. For ABA treatments, 100 μm ABA was applied to each 14-d-old seedling for 2 h. RNA gel blots of total RNAs from transgenic and NC plants grown either under normal growth conditions (left) and under stress conditions (right) are indicated. RNA gel blots of NC plants grown under normal growth conditions were included on the left-hand side of each section for clarity of comparison. The blots were hybridized with probes for CBF3, ABF3, Lip5 (AB011368), Dip1 (AY587109), Jacalin1 (AK066682), Jacalin2 (AK101991), LOX (AJ270938), PSLS (AK072958), Hsp70 (CF280418), PP2Ca (CF304401), Wsi18 (D26536), Rab21 (Y00842), LEA4 (AK107930), PP2Cb (AK069274), and RbcS (Kyozuka et al., 1993). EtBr staining of total RNA was used to ensure equal RNA loading.

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    Figure 6.

    Transactivation of the Wsi18:GUS fusion by ABF3. The Wsi18:GUS construct was cotransformed with the effector constructs, either Ubi1:CBF3 or Ubi1:ABF3, or with the expression vector alone; 4 μg of each construct with 2 μg of Ubi1:LUC as an internal standard was used in all cases. Each bar represents the mean value of the relative GUS/LUC activities from four independent experiments.

Tables

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    Table I.

    Survival of Ubi1:CBF3 and Ubi1:ABF3 plants under drought stress

    PlantsaTotalbSurvivalcSurvival Rated
    Ubi1:CBF3
        NC3600%
        1-4-1363494%
        2-1-13636100%
        4-8-13636100%
        6-5-1361439%
    Ubi1:ABF3
        NC3638%
        1-4-1362158%
        2-1-1362467%
        5-8-1361850%
    • ↵a Four-week-old soil-grown plants withheld water for 4 d followed by watering for 7 d and results scored. Plants were considered dead if there was no regrowth 7 d of rewatering. Water loss during the drought periods was similar for all pots.

    • ↵b Total number of plants used in each assay.

    • ↵c Number of survival plants.

    • ↵d Percent of survived plants (survival/total × 100).

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    Table II.

    List of genes that are up-regulated in Ubi1:CBF3 and Ubi1:ABF3 plants under normal and drought stress

    Numbers appearing in bold are the ones that are induced 1.6-fold or more in Ubi1:CBF3 or Ubi1:ABF3 plants.

    Gene NameAccession No.aNormalbDroughtd
    Ubi1:CBF3cUbi1:ABF3cUbi1:CBF3cUbi1:ABF3c
    Jacalin1AK0666823.56−1.113.042.92
    Jacalin2AK1019913.32−1.172.422.10
    Dip1AY5871091.661.131.101.39
    Lip5AB0113682.321.291.20−1.10
    Lipoxygenase (LOX)AJ2709383.101.43−1.591.11
    GlutelinAK1072382.18−1.10−1.221.13
    Bowman Birk trypsin inhibitor1AK0658461.831.08−1.191.27
    Bowman Birk trypsin inhibitor2AK1054551.65−1.22−1.191.10
    Receptor kinase containing LRR repeatsAK1198231.671.641.371.99
    Unknown proteinAK0592021.62−2.071.121.26
    Cyt P450AK0693941.341.115.213.30
    Seed imbibition protein (Sip1)AK0651001.03−1.032.201.12
    Sicrotubule-associated protein MAP65-1aAK102553−1.081.061.911.22
    Unknown proteinNM_188534−1.071.091.931.06
    Unknown proteinAK1076241.10−1.071.861.17
    Unknown proteinAK061456−1.03−1.001.681.25
    Polygalacturonase (PG2)AK1084771.021.091.701.47
    FtsJ cell division proteinAK0700751.101.101.78−1.02
    mRNA cleavage factor I subunitAK0612601.031.131.791.04
    BeclinAK1010331.191.021.731.05
    Cyclophilin (CyP)AK1116541.04−1.011.701.21
    Phospho sulfolactate synthase (PSLS)AK072958−1.01−1.041.611.02
    Gag-pol polyproteinAK063408−1.08−1.181.82−1.01
    α-Expansin OsEXPA5AF3945461.161.141.411.94
    Hsp70AK0728301.991.941.391.28
    Protein phosphatase 2Ca (PP2Ca)XM_4633641.651.671.211.48
    Wsi18D265361.002.111.062.27
    RAB21Y00842−1.032.601.221.54
    Phosphate-induced protein 1(phi1)AK070419−1.111.671.10−1.39
    Antioxidant proteinAK0664521.171.681.251.15
    LEA4AK107930−1.011.021.084.33
    Protein phosphatase 2Cb (PP2Cb)AK0692741.121.051.053.45
    PHD-type zinc finger proteinAK059311−1.171.091.073.11
    Unknown proteinAK063747−1.161.091.172.83
    Little protein (LP1)AK0636341.091.09−1.223.01
    Unknown proteinAK0720341.081.06−1.112.66
    Unknown proteinAK063680−1.00−1.05−1.082.63
    CCCH-type zinc finger proteinAK1063921.371.051.402.56
    26S proteasome AAA-ATPase subunitAK1039361.051.22−1.002.26
    Unknown proteinNM_197832−1.341.18−1.002.24
    Unknown proteinXM_4803951.011.091.052.34
    Unknown proteinAK0588511.03−1.00−1.122.38
    Aquaporin (TIP4)AK1216711.08−1.061.072.62
    Disease resistance protein (RPH8A)AK0725311.131.18−1.072.10
    Unknown proteinAK1041551.051.00−1.012.20
    1,4-β-d xylan xylanohydrolaseNM_1841041.091.041.031.97
    Spore coat proteinAK1089171.02−1.021.051.93
    CellulaseXM_469540−1.061.071.211.98
    LTI6B-likeAK104060−1.121.09−1.071.88
    Fusarium resistance proteinAK0583431.051.11−1.032.20
    ABC transporterAK105712−1.081.17−1.191.91
    LEAAK0675561.131.101.221.87
    LEA3AK102039−1.021.17−1.172.14
    • ↵a GenBank accession numbers for full-length cDNA sequences of corresponding genes.

    • ↵b Microarrays were hybridized with Cy3- and Cy5-labeled probe pairs of either Ubi1:CBF3 and nontransgenic plants or Ubi1:ABF3 and nontransgenic plants grown in normal growth conditions.

    • ↵c The microarray-data sets can be found at the www.http://www.ncbi.nlm.nih.gov/geo/ (Gene Expression Omnibus, GEO). GEO accession number of microarray-data set is GSE2211.

    • ↵d Microarrays were hybridized with Cy3- and Cy5-labeled probe pairs of either Ubi1:CBF3 and nontransgenic plants or Ubi1:ABF3 and nontransgenic plants grown in drought-stress conditions.

Additional Files

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    Supplemental Figures, Tables, and Material

    Files in this Data Supplement:

    • Supplemental Data - Supplemental Figure 1A
    • Supplemental Data - Supplemental Figure 1B,C
    • Supplemental Data - Supplemental Figure Legend
    • Supplemental Data - Supplemental Table I
    • Supplemental Data - Supplemental Table II
    • Supplemental Data - Supplemental Material Legend
    • Supplemental Data - Supplemental Material 1A
    • Supplemental Data - Supplemental Material 1B,C
    • Supplemental Data - Supplemental Material 2
    • Supplemental Data - Supplemental Material 3
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Arabidopsis CBF3/DREB1A and ABF3 in Transgenic Rice Increased Tolerance to Abiotic Stress without Stunting Growth
Se-Jun Oh, Sang Ik Song, Youn Shic Kim, Hyun-Jun Jang, Soo Young Kim, Minjeong Kim, Yeon-Ki Kim, Baek Hie Nahm, Ju-Kon Kim
Plant Physiology May 2005, 138 (1) 341-351; DOI: 10.1104/pp.104.059147

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Arabidopsis CBF3/DREB1A and ABF3 in Transgenic Rice Increased Tolerance to Abiotic Stress without Stunting Growth
Se-Jun Oh, Sang Ik Song, Youn Shic Kim, Hyun-Jun Jang, Soo Young Kim, Minjeong Kim, Yeon-Ki Kim, Baek Hie Nahm, Ju-Kon Kim
Plant Physiology May 2005, 138 (1) 341-351; DOI: 10.1104/pp.104.059147
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Plant Physiology: 138 (1)
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