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Original Research ARTICLE

Front. Plant Sci., 15 August 2019 | https://doi.org/10.3389/fpls.2019.01025

A Novel Sweetpotato Transcription Factor Gene IbMYB116 Enhances Drought Tolerance in Transgenic Arabidopsis

Yuanyuan Zhou1, Hong Zhu1,2, Shaozhen He1, Hong Zhai1, Ning Zhao1, Shihan Xing1, Zihao Wei1 and Qingchang Liu1*
  • 1Key Laboratory of Sweetpotato Biology and Biotechnology, Ministry of Agriculture/Beijing Key Laboratory of Crop Genetic Improvement/Laboratory of Crop Heterosis and Utilization, Ministry of Education, College of Agronomy & Biotechnology, China Agricultural University, Beijing, China
  • 2College of Agronomy, Qingdao Agricultural University, Qingdao, China

Several members of the MYB transcription factor family have been found to regulate growth, developmental processes, metabolism, and biotic and abiotic stress responses in plants. However, the role of MYB116 in plants is still unclear. In this study, a MYB transcription factor gene IbMYB116 was cloned and characterized from the sweetpotato [Ipomoea batatas (L.) Lam.] line Xushu55-2, a line that is considered to be drought resistant. We show here that IbMYB116 is a nuclear protein and that it possesses a transactivation domain at the C terminus. This gene exhibited a high expression level in the leaf tissues of Xushu55-2 and was strongly induced by PEG6000 and methyl-jasmonate (MeJA). The IbMYB116-overexpressing Arabidopsis plants showed significantly enhanced drought tolerance, increased MeJA content, and a decreased H2O2 level under drought stress. The overexpression of IbMYB116 in Arabidopsis systematically upregulated jasmonic acid (JA) biosynthesis genes and activated the JA signaling pathway as well as reactive oxygen species (ROS)-scavenging system genes under drought stress conditions. The overall results suggest that the IbMYB116 gene might enhance drought tolerance by activating a ROS-scavenging system through the JA signaling pathway in transgenic Arabidopsis. These findings reveal, for the first time, the crucial role of IbMYB116 in the drought tolerance of plants.

Introduction

Drought seriously affects the productivity of agricultural crops in the world (Yang et al., 2010; Boyer et al., 2013). Improving the drought tolerance of crops has become important for food security (Tester and Langridge, 2010; Zhu, 2016). Plants adapt to drought stress by developing a variety of mechanisms, including growth and development regulation, osmotic adjustment, ion homeostasis, and detoxification (Bohnert et al., 1995; Zhu, 2002). In response to water deficits, plants increase water uptake by forming long roots to promote their survival (Yu et al., 2008; Wang et al., 2016a). At the phytohormone level, jasmonic acid (JA), abscisic acid (ABA), salicylic acid (SA), and ethylene (ETH) play important roles in plant growth and development as well as protective responses against biotic and abiotic stresses (Fujita et al., 2005; Dong et al., 2014; Vargas et al., 2014; Zhang et al., 2015a; Jin et al., 2016; Xu et al., 2017).

Jasmonates (JAs), including JA, methyl-jasmonate (MeJA), and JA-isoleucine (JA-Ile), are important regulators of plant responses to environmental stresses, such as drought, salt, and ozone exposure (Overmyer et al., 2000; Turner et al., 2002; Lorenzo et al., 2003; Rojo et al., 2003; Wasternack et al., 2006; Dhakarey et al., 2017; Zhang et al., 2017). In JA biosynthesis, plastidial 13-lipoxygenase (LOX), allene oxide synthase (AOS), and allene oxide cyclase (AOC) catalyze linolenic acid to cis-12-oxophytodienoic acid (OPDA); OPDA reductase (OPR) further reduces OPDA to 3-oxo-2(2’(Z)-pentenyl)-cyclopentane-1-octanoic acid (OPC-8:0). Subsequently, the carboxyl chain of OPC-8:0 is shortened by three β-oxidation steps, which form JA with the key enzymes CoA ligase 1 (OPCL1), acyl-CoA oxidase (ACOX1, ACOX3), enoyl-CoA hydratase (MFP2), acetyl-CoA acyltransferase (fadA), and acetyl-CoA acyltransferase 1 (ACAA1) (Mueller, 1997; Berger, 2002; Wasternack and Hause, 2013). Furthermore, coronatine-insensitive 1 (COI1), jasmonate ZIM-domain (JAZ) and myelocytomatosis (MYC) proteins are the components of the core JA signaling pathway (Chini et al., 2007; Wasternack and Hause, 2013; Liu and Avramova, 2016). The JA signaling pathway plays a critical role in regulating the response to drought stress in plants (Liu et al., 2015; Ahmad et al., 2016).

In plants, several types of transcription factors (TFs), including MYB/MYC, NAC, bZIP, AP2/ERF, PHD, and WRKY, control biological processes by regulating target genes in response to stresses (Shiriga et al., 2014; Zong et al., 2016; Wang et al., 2017a; Wang et al., 2017b). MYB is a large transcription factor family in higher plants (Riechmann et al., 2000). Based on the number of repeats of the MYB domain, this family is divided into four major classes: 1R-MYB, R2R3-MYB, 3R-MYB, and 4R-MYB. ZmC1 from Zea mays was the first plant MYB gene (Paz-Ares et al., 1987). To date, more than 200 MYB TFs have been identified in several plant species, such as Arabidopsis, rice, and soybean (Dubos et al., 2010; Aoyagi et al., 2014; Smita et al., 2015). R2R3-MYB TFs have been found to play important roles in plant responses to biotic and abiotic stresses (Dubos et al., 2010). Accumulated evidence has indicated that R2R3-MYB TFs mediate stress-signaling pathways, such as salinity, drought, and extreme temperature (Hajiebrahimi et al., 2017). In Arabidopsis, several R2R3-MYB TFs, including AtMYB2, AtMYB15, AtMYB44, AtMYB60, AtMYB61, AtMYB96, and AtMYB102, were involved in drought stress responses (Denekamp and Smeekens, 2003; Abe et al., 2003; Liang et al., 2005; Chen et al., 2006; Jung et al., 2008; Rusconi et al., 2013; Lee et al., 2014). The overexpression of GmMYB84 and GmMYB174 in soybean, GaMYB85, GmMYBJ1, and GmMYBJ2 in Arabidopsis, OsMYB2 in rice, MdSIMYB1 in tobacco and apple, and SbMYB8 in tobacco improved drought tolerance in transgenic plants (Yang et al., 2012; Su et al., 2014; Wang et al., 2014; Su et al., 2015; Wang et al., 2015; Yuan et al., 2015; Butt et al., 2017; Wang et al., 2017b). Until now, the role of MYB116 in plants has not been reported.

The productivity of sweetpotato, Ipomoea batatas (L.) Lam., as an important food crop is seriously affected by drought stress. It has been shown that drought tolerance of sweetpotato could be improved through gene engineering (Park et al., 2011; Wang et al., 2016b; Fan et al., 2017; Kang et al., 2018a, Kang et al., 2018b; Kim et al., 2018). However, MYB TFs from sweetpotato have not been functionally characterized to date. In this study, we cloned a novel MYB TF gene named IbMYB116 from a drought-tolerant sweetpotato line Xushu55-2 and found its overexpression in Arabidopsis enhanced drought tolerance through the JA signaling pathway.

Materials and Methods

Plant Materials

The drought-tolerant sweetpotato line Xushu55-2 was applied to isolate the IbMYB116 gene. The expressed sequence tag (EST) was screened from the transcriptome sequencing data of Xushu55-2 (Zhu et al., 2018). The function of IbMYB116 was identified using Arabidopsis thaliana Columbia-0.

Cloning and Sequence Analysis of IbMYB116 and Its Promoter

The total RNA from in vitro-grown plants of Xushu55-2 was transcribed into the first-strand cDNA (Kang et al., 2018a). The rapid amplification of cDNA ends (RACE) procedure was used to amplify the full-length cDNA of IbMYB116. The genomic sequence of IbMYB116 was amplified from the genomic DNA of in vitro-grown Xushu55-2. Its promoter was obtained from the genomic DNA of in vitro-grown Xushu55-2 by homology cloning strategy. All of the specific primers are listed in Supplementary Table S1. IbMYB116 was analyzed with online BLAST, ORF Finder, DNAMAN software, Splign tool, and MEGA 7.0, and the cis-acting regulatory elements in its promoter region were defined online (Kang et al., 2018b).

Subcellular Localization of IbMYB116

For subcellular localization, the coding sequence of IbMYB116 was inserted into the pMDC83 vector. The fusion construct (35S::IbMYB116::GFP) and the empty vector (35S::GFP) were separately transformed into the EHA105 strain of Agrobacterium tumefaciens and further infiltrated the leaves of Nicotiana benthamiana (Strasser et al., 2007; Li et al., 2017). After 48 h of growth in a greenhouse, agroinfiltrated leaf sections were imaged at room temperature using a laser scanning confocal microscope with an Argon laser (LSM710, Zeiss, Germany). GFP was excited at 488 nm, and the emitted light was captured at 505–555 nm.

Transactivation Activity Assay of IbMYB116

The transactivation activity of IbMYB116 was tested in yeast (Saccharomyces cerevisiae) (Jiang et al., 2014). The full-length (construct 1) and a series of deletion mutations of IbMYB116 (constructs 2–9) were fused to the yeast expression vector pGBKT7 (pBD). The expression vector pBD-IbMYB116, pGAL4 (positive control), and pBD (negative control) were transferred into the host strain AH109. After the cells were cultured on the SD/-Trp medium, the yeast was further cultured on medium with X-α-Gal (SD/-Trp/-His/X).

Expression Analysis of IbMYB116 in Sweetpotato

The transcript levels of IbMYB116 in the roots, stems, and leaves of the in vitro-grown Xushu55-2 plants were analyzed using quantitative real-time PCR (qRT-PCR), the expression levels were normalized to Ibactin (AY905538), and the relative expression levels in different tissues were calibrated using the roots (Schmittgen and Livak, 2008; Liu et al., 2014). Furthermore, in vitro-grown Xushu55-2 plants were treated in Hoagland solution with H2O, 30% PEG6000, and 100 μM MeJA; the plants were sampled 0, 1, 3, 6, 12, and 24 h after treatments and then analyzed for the expression of IbMYB116. The expression levels were normalized to Ibactin (AY905538), and the relative expression levels in different treatments were calibrated using the plant sampled 0 h after treatment. The specific primers were designed in the nonconserved domain (Figure S1 and Supplementary Table S1).

Production of the Transgenic Arabidopsis Plants

The overexpression vector pC3301-35S-IbMYB116 was generated by inserting the expression cassette 35S-IbMYB116 into pCAMBIA3301, and then, it was transferred into the A. tumefaciens strain GV3101. The transgenic Arabidopsis plants were produced and further grown in pots to obtain T3 seeds as described by Kang et al. (2018b). The transcript levels of IbMYB116 in wild-type and transgenic lines were analyzed using qRT-PCR, and the expression levels were normalized to Atactin (NM112764) (Supplementary Table S1). The relative expression levels in transgenic lines were calibrated using the transgenic line with the lowest IbMYB116 expression.

Assay for Drought Tolerance

For the germination rate assay, T3 and wild-type (WT) seeds sterilized with 2% NaClO for 5 min were sown on 1/2 MS medium with mannitol (0, 100, 200, and 300 mM). Approximately 50 seeds per line were sown for each experiment, and their germination rates were investigated after 3 days. For the root length assay, 5-day-old seedlings of T3 and WT formed on 1/2 MS basal medium were vertically cultured on 1/2 MS medium with 0 (as a control) or 300 mM mannitol, and their roots were took out, and the primary root lengths were measured with a ruler after 3 weeks.

Furthermore, the 7-day-old seedlings obtained on 1/2 MS basal medium were transplanted in pots; after 2 weeks, they were stressed by a 4-week drought followed by 2-day rewatering for investigating their phenotypes. The 6-week normal treatment with water was used as a control.

Expression Analysis of the Related Genes and Measurements of MeJA and H2O2 Contents

T3 and WT plants were pot grown for 2 weeks under drought stress conditions after 2 weeks of normal treatment with water, and they were employed to analyze the expression of the genes involved in JA biosynthesis and signaling pathways as well as the reactive oxygen species (ROS)-scavenging system with qRT-PCR and Atactin (NM112764) as an internal control (Supplementary Table S1), and the relative expression levels in T3 and WT plants were calibrated using WT. Their MeJA and H2O2 contents were determined using high-performance liquid chromatography (HPLC) and an H2O2 Assay Kit (Comin Biotechnology Co., Ltd. Suzhou, China), respectively. The 4-week normal treatment with water was used as a control.

Statistical Analysis

Three biological replicates were performed for all experiments. Difference analysis of data presented as the mean ± SE was done with Student’s t-test (two-tailed analysis) using SPSS 20.0 Statistic Program. Significance levels at P < 0.05, P < 0.01, and P < 0.001 were indicated with ∗, ∗∗, and ∗∗∗, respectively.

Results

Cloning and Sequence Analysis of IbMYB116 and Its Promoter

The IbMYB116 full-length cDNA was 958 bp in length and contained an 849-bp ORF that encoded a polypeptide of 282 residues with a predicted molecular weight of 31.998 kDa and a pI of 6.79. The IbMYB116 protein had two conserved MYB domains that belonged to R2R3-MYB TFs and shared a high-sequence identity with MYB TFs from Ipomoea nil (InMYB21, XP_019189643.1, 91.23%), Glycine max (GmMYB184, NP_001235837.1, 49.12% and GmMYB84, NP_001235789.1, 43.83%), and Arabidopsis thaliana (AtMYB116, AT1G25340.1, 43.24%) (Figure 1A). The protein was characterized with a highly conserved DNA-binding sequence at the N-terminus (Figure 1A). Phylogenetic analysis along with 125 Arabidopsis R2R3-MYB TFs belonging to 24 groups (Dubos et al., 2010) revealed that IbMYB116 belonged to group S20 of the MYB family and had a close relationship with AtMYB116 (At1G25340.1) (Figure 1B). The genomic DNA of IbMYB116 was 1,498 bp with three exons and two introns (Figure 1C). Its promoter region (∼1,455 bp) contained the cis-acting regulatory elements associated with stresses and phytohormones, including LTR, HSE, MBS, GARE-motif, CGTCA-motif, TGACG-motif, P-box, and SARE (Figure S2).

FIGURE 1
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Figure 1 Sequence analysis of IbMYB116. (A) Sequence alignment of IbMYB116 with its homologues from other plants. Conserved amino acids are indicated by a dark background. Characteristic regions of MYB are indicated above the IbMYB116 sequence. —, R2 SANT domain; —, R3 SANT domain. (B) Phylogenetic analysis of IbMYB116 and MYB transcription factors from Arabidopsis thaliana. (C) Exon and intron constituents of IbMYB116. Exons are represented by boxes and introns by lines.

Subcellular Location of IbMYB116

IbMYB116-GFP showed fluorescence in the nuclei of Nicotiana benthamiana leaf hypodermal cells, while the fluorescence of GFP was distributed in the entire cell (Figure 2). These results clearly indicated that IbMYB116 is a nuclear protein.

FIGURE 2
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Figure 2 Subcellular localization of IbMYB116 in tobacco leaf hypodermal cells. Confocal scanning microscopic images show localization of IbMYB116-GFP fusion proteins to nuclei in the right column vs. GFP as the control in the left column. Bars = 20 µm.

Transactivation Activity of IbMYB116 in Yeast

All of the transformed yeast cells grew well on the SD/-Trp medium, which indicated that expression vectors (pBD-IbMYB116-1, -2, -3, -4, -5, -6, -7, -8, -9; Figure 3A) had been successfully transferred into yeast cells (Figure 3B). The yeast cells harboring pBD-IbMYB116-1, -4, -5, -6, -7, and pGAL4 (positive control) grew well and turned blue, but the cells with pBD-IbMYB116-2, -3, -8, -9, and pBD (negative control) failed to grow on medium with X-α-Gal (SD/-Trp/-His/X) (Figure 3C). These results demonstrated that IbMYB116 contained the transactivation activity domain at the region of amino acids 215–282.

FIGURE 3
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Figure 3 Transactivation activity assay of IbMYB116 in yeast. (A) Diagram showing a full-length construct (construct 1) and a series of deletion mutations of IbMYB116 (constructs 2–9). (B) The transformed yeast cells harboring different expression vectors (constructs 1–9) were drawn onto SD/-Trp medium. pBD () and pGAL4 (+) were used as negative and positive controls, respectively. (C) The transformed yeast cells harboring different expression vectors (constructs 1–9) were drawn onto SD/-Trp/-His medium supplemented with X-α-Gal. pBD () and pGAL4 (+) were used as negative and positive controls, respectively.

Expression of IbMYB116 in Sweetpotato

A significantly higher expression level of IbMYB116 was found in the leaves of Xushu55-2 than that in the roots and stems (Figure S3). Its expression in Xushu55-2 was strongly induced by 30% PEG6000 and 100 μM MeJA, and it reached the highest level at 12 h (4.78-fold) and 24 h (4.15-fold), respectively (Figure 4).

FIGURE 4
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Figure 4 Expression analysis of IbMYB116 in the in vitro-grown plants of Xushu55-2 after different times (h) in response to H2O, 30% PEG6000, and 100 µM MeJA, respectively. Data are presented as the means ± SE (n = 3). *, ** and *** indicate significant differences from WT at P <0.05, P <0.01, and P <0.001, respectively, according to the Student’s t-test.

Production of the Transgenic Arabidopsis Plants

The transgenic Arabidopsis plants were obtained using the protocols of Kang et al. (2018b). Eight transgenic plants named L1, L2, …, L8 were randomly selected to analyze the expression level of IbMYB116 with qRT-PCR (Figure S1). The results showed that all of the transgenic plants exhibited significantly higher expression levels of IbMYB116 than the WT (Figure S4).

Enhanced Drought Tolerance

Three transgenic Arabidopsis plants (L1, L2, and L3) with high expression levels of IbMYB116 were selected for investigating their drought tolerance. The transgenic and WT plants showed no differences in germination rates on 1/2 MS media with 0 (control) and 100 mM mannitol (Figure 5). However, the transgenic plants provided significantly higher germination rates than the WT under 200 and 300 mM mannitol stress conditions (Figure 5). The transgenic and WT plants showed similar growth on 1/2 MS media without mannitol, but the transgenic plants formed significantly longer roots than the WT at the level of 300 mM mannitol (Figure 6).

FIGURE 5
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Figure 5 Germination assay of the transgenic Arabidopsis and WT seeds sown for 3 days on 1/2 MS medium with 0, 100, 200, and 300 mM mannitol, respectively. * and ** indicate significant differences from WT at P < 0.05 and P < 0.01, respectively, according to the Student’s t-test.

FIGURE 6
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Figure 6 Primary root lengths of the transgenic Arabidopsis and WT seedlings cultured for 3 weeks on 1/2 MS medium without (control) and with 300 mM mannitol, respectively. All the plants were grown in a standard square plate of 12 × 12 cm. Data are presented as the mean ± SE (n = 3). * and ** indicate significant differences from WT at P < 0.05 and P < 0.01, respectively, according to the Student’s t-test.

Furthermore, the transgenic and WT plants grown in pots had no differences in growth without drought stress (Figure 7A). However, after being stressed by drought, the transgenic plants exhibited better growth, increased MeJA content, and decreased H2O2 content compared with the WT (Figures 7A, B). These results indicated that the transgenic Arabidopsis plants had significantly enhanced drought tolerance compared with the WT.

FIGURE 7
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Figure 7 Responses of the transgenic Arabidopsis plants and WT to drought stress. (A) Phenotypes of the transgenic plants vs. WT stressed by a 4-week drought followed by 2 days rewatering after 2 weeks of normal treatment with water. The 6-week normal treatment was used as a control. (B) Contents of MeJA and H2O2 in the leaves of the transgenic and WT plants grown for 4 weeks under normal treatment (control) and 2 weeks under drought stress after 2 weeks of normal treatment, respectively. *, **, and *** indicate significant differences from WT at P < 0.05, P < 0.01, and P < 0.001, respectively, according to the Student’s t-test.

Expression of the Related Genes

Systematic upregulation of the JA biosynthesis key enzyme genes AtLOX, AtAOS, AtAOC, AtOPR, AtOPCL, AtACOX3, AtfadA, and AtACAA1, except for AtACOX1 (no change) and AtMFP2 (downregulated), was found in the transgenic Arabidopsis plants under drought stress conditions (Figure 8A). In the JA signaling pathway, AtCOI1 and AtJAZ were downregulated, but AtMYC2 was upregulated under drought stress conditions (Figure 8B). The genes encoding ROS scavenging enzymes superoxide dismutase (SOD), glutathione peroxidase (GPX), and peroxidase (POD) were also upregulated, and both AtCAT and AtDHAR apparently had not changed (Figure 8C).

FIGURE 8
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Figure 8 Transcript levels of the related genes in the leaves of the transgenic Arabidopsis and WT plants pot grown for 4 weeks under normal treatment with water (control) and 2 weeks under drought stress after 2 weeks of normal treatment, respectively. (A) Transcript levels of JA biosynthesis genes. (B) Transcript levels of JA signaling pathway genes. (C) Transcript levels of ROS-scavenging system genes. * and ** indicate significant differences from WT at P < 0.05 and P < 0.01, respectively, according to the Student’s t-test.

Discussion

IbMYB116 Enhances Drought Tolerance

It has been shown that several MYB TFs play crucial roles in the response to drought stress as positive stress response TFs (Rusconi et al., 2013; Lee et al., 2014; Yuan et al., 2015; Butt et al., 2017; Wang et al., 2017b). To date, the role of MYB116 in plants is still unknown. In this study, we cloned the IbMYB116 gene from the drought-tolerant sweetpotato line Xushu55-2 and found that the IbMYB116 protein belonged to R2R3-MYB TFs (Figure 1) (Jia et al., 2004; He et al., 2016). This gene was strongly induced by PEG6000 and MeJA, and its overexpression significantly improved the drought tolerance of the transgenic Arabidopsis plants (Figures 47). This study reveals, for the first time, the crucial role of IbMYB116 in the drought tolerance of plants.

IbMYB116 Upregulates JA Signaling Pathway Genes

JAs are naturally occurring signaling compounds that regulate plant responses to abiotic stresses, such as drought, salt, and ozone exposure (Rojo et al., 2003; Ahmad et al., 2016; Dhakarey et al., 2017). Rohwer and Erwin (2008) found that JA and JA-induced protein levels were increased in sorbitol-treated barley leaves, which confirmed the role of JAs in osmotic stress. MeJA enhanced drought tolerance by improving the water status of wheat plants (Ma et al., 2004) or increasing antioxidant activities in soybean plants (Anjum et al., 2011). In Arabidopsis, four 13-LOX forms (AtLOX2, 3, 4, and 6) contributed to JA formation in the stress response (Caldelari et al., 2011; Chauvin et al., 2013). The upregulation of OsLOX, OsAOS2, and OsOPR7 led to massive accumulation of endogenous JA in the rice rim1 mutant (Yoshii et al., 2010). The tolerance to drought as well as osmotic and salinity changes were increased in the Arabidopsis plants overexpressing CaLOX1 from pepper (Lim et al., 2015). The TaAOC1-overexpressing wheat and Arabidopsis plants accumulated more JA and exhibited enhanced tolerance to changes in salinity, which indicated that JA is related to the plant salinity response (Zhao et al., 2014). The expression of OsOPR7 was induced by drought stress and wounding, and the increase in OsOPR7 expression led to an elevated endogenous JA level (Tani et al., 2008).

The JA signaling pathway plays an important role in regulating the plant response to drought stress (Liu et al., 2015; Ahmad et al., 2016). As components of the core JA signaling pathway, COI1 participates in removing repressors of JA transduction (Xie et al., 1998; Ahmad et al., 2016); JAZs are transcription repressors of JA-responsive genes (Chini et al., 2007), and MYC2 acts as a positive regulator of JA signals (Zhang et al., 2015b). The overexpression of AtMYC2 in Arabidopsis improved osmotic stress tolerance (Abe et al., 2003). The OsMYC2-overexpressing rice exhibited increased resistance against Xoo (Uji et al., 2016).

Our results showed that overexpression of IbMYB116 in Arabidopsis systematically upregulated the JA biosynthesis genes, including AtLOX, AtAOS, AtAOC, AtOPR, AtOPCL, AtCOX3, AtfadA, and AtACAA1, and the MeJA content increased under drought stress conditions (Figures 7, 8). AtCOI1 and AtJAZ were downregulated, and AtMYC2 was upregulated in the transgenic Arabidopsis plants under drought stress conditions (Figure 8). These findings suggest that IbMYB116 enhances drought tolerance through the JA signaling pathway in transgenic Arabidopsis (Figure 9).

FIGURE 9
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Figure 9 Diagram showing a proposed model for the regulation of IbMYB116 in drought tolerance for transgenic Arabidopsis. ↑, ↓and ∣ indicate upregulation, downregulation, and no obvious change of expression for genes coding these enzymes, respectively.

IbMYB116 Activates the ROS-Scavenging System

In plants, ROS cause damage to the structure and function of biomolecules, which leads to oxidative stress. H2O2, as one of the prominent ROS, is considered to be an important signaling molecule in plant cells (Wang et al., 2017a). The ROS-scavenging system can detoxify ROS to reduce oxidative damage in plant cells (Gill and Tuteja, 2010; Liu et al., 2014). It has been shown that JA can activate the ROS-scavenging system in plants. The overexpression of CaLOX1 in Arabidopsis systematically upregulated the ROS-scavenging system genes, which resulted in the reduced H2O2 level under drought and salt stress conditions (Lim et al., 2015). The JA-deficient tomato mutant def-1 showed higher ROS levels than the WT under salt stress conditions (Abouelsaad and Renault, 2018). JA influenced oxidative stress through its direct effect on the activities of ROS-scavenging enzymes in raspberry and strawberry (Wang, 1999; Ghasemnezhad and Javaherdashti, 2008). Reduced levels of JA led to more GLN18:3-induced ROS production in Arabidopsis and tomato (Block et al., 2018).

The results of this study demonstrated that ROS-scavenging system genes, including AtSOD, AtGPX, and AtPOD, were upregulated and that the H2O2 level was decreased in the IbMYB116-overexpressing Arabidopsis plants under drought stress conditions (Figures 7, 8). These results suggest that IbMYB116 might enhance drought tolerance by activating the ROS-scavenging system through the JA signaling pathway in transgenic Arabidopsis (Figure 9).

Conclusion

We found a crucial role for IbMYB116 in the drought tolerance of plants. The results suggest that the overexpression of IbMYB116 might enhance drought tolerance by activating the ROS-scavenging system through the JA signaling pathway in transgenic Arabidopsis. This gene has the potential to be used for improving the drought tolerance of sweetpotato and other plants.

Author Contributions

QL and YZ conceived and designed the experiments. YZ and HZu performed the experiments. YZ, SH, and HZa analyzed the data. QL, NZ, SX, and ZW contributed reagents, materials, and analysis tools. QL and YZ wrote the paper. All authors read and approved the final manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (31461143017) and the China Agriculture Research System (CARS-10, Sweetpotato).

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2019.01025/full#supplementary-material

References

Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K., Yamaguchi-Shinozaki, K. (2003). Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15, 63–78. doi: 10.1105/tpc.006130

PubMed Abstract | CrossRef Full Text | Google Scholar

Abouelsaad, I., Renault, S. (2018). Enhanced oxidative stress in the jasmonic acid-deficient tomato mutant def-1 exposed to NaCl stress. J. Plant Physiol. 226, 136–144. doi: 10.1016/j.jplph.2018.04.009

PubMed Abstract | CrossRef Full Text | Google Scholar

Ahmad, P., Rasool, S., Gul, A., Sheikh, S. A., Akram, N. A., Ashraf, M., et al. (2016). Jasmonates: multifunctional roles in stress tolerance. Front. Plant Sci. 7, 813–827. doi: 10.3389/fpls.2016.00813

PubMed Abstract | CrossRef Full Text | Google Scholar

Anjum, S., Xie, X. Y., Wang, L. C., Saleem, M. F., Man, C., Wang, L. (2011). Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agri. Res. 6, 2026–2032. doi: 10.5897/AJAR10.027

CrossRef Full Text | Google Scholar

Aoyagi, L. N., Lopes-Caitar, V. S., de Carvalho, M., Darben, L. M., Polizel-Podanosqui, A., Kuwahara, M. K., et al. (2014). Genomic and transcriptomic characterization of the transcription factor family R2R3-MYB in soybean and its involvement in the resistance responses to Phakopsora pachyrhizi. Plant Sci. 229, 32–42. doi: 10.1016/j.plantsci.2014.08.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Berger, S. (2002). Jasmonate-related mutants of Arabidopsis as tools for studying stress signaling. Planta 214, 497–504. doi: 10.1007/s00425-001-0688-y

PubMed Abstract | CrossRef Full Text | Google Scholar

Block, A., Christensen, S. A., Hunter, C. T., Alborn, H. T. (2018). Herbivore-derived fatty-acid amides elicit reactive oxygen species burst in plants. J. Exp. Bot. 69, 1235–1245. doi: 10.1093/jxb/erx449

PubMed Abstract | CrossRef Full Text | Google Scholar

Bohnert, H. J., Nelson, D. E., Jensen, R. G. (1995). Adaptations to environmental stresses. Plant Cell 7, 1099–1111. doi: 10.1105/tpc.7.7.1099

PubMed Abstract | CrossRef Full Text | Google Scholar

Boyer, J. S., Byrne, P., Cassman, K. G., Cooper, M., Delmer, D., Greene, T., et al. (2013). The US drought of 2012 in perspective: a call to action. Glob. Food Secur-Agr. 2, 139–143. doi: 10.1016/j.gfs.2013.08.002

CrossRef Full Text | Google Scholar

Butt, H. I., Yang, Z., Gong, Q., Chen, E., Wang, X., Zhao, G., et al. (2017). GaMYB85, an R2R3 MYB gene, in transgenic Arabidopsis plays an important role in drought tolerance. BMC Plant Biol. 17, 142–158. doi: 10.1186/s12870-017-1078-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Caldelari, D., Wang, G., Farmer, E. E., Dong, X. (2011). Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol. Biol. 75, 25–33. doi: 10.1007/s11103-010-9701-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Chauvin, A., Caldelari, D., Wolfender, J. L., Farmer, E. E. (2013). Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol. 197, 566–575. doi: 10.1111/nph.12029

PubMed Abstract | CrossRef Full Text | Google Scholar

Chen, Y. H., Zhang, X. B., Wu, W., Chen, Z. L., Gu, H. Y., Qu, L. J., et al. (2006). Overexpression of the wounding-responsive gene AtMYB15 activates the shikimate pathway in Arabidopsis. J. Integr Plant Biol. 48, 1084–1095. doi: 10.1111/j.1744-7909.2006.00311.x

CrossRef Full Text | Google Scholar

Chini, A., Fonseca, S., Fernandez, G., Adie, B., Chico, J. M., Lorenzo, O., et al. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671. doi: 10.1038/nature06006

PubMed Abstract | CrossRef Full Text | Google Scholar

Denekamp, M., Smeekens, S. C. (2003). Integration of wounding and osmotic stress signals determines the expression of the AtMYB102 transcription factor gene. Plant Physiol. 132, 1415–1423. doi: 10.1104/pp.102.019273

PubMed Abstract | CrossRef Full Text | Google Scholar

Dhakarey, R., Raorane, M. L., Treumann, A., Peethambaran, P. K., Schendel, R. R., Sahi, V. P., et al. (2017). Physiological and proteomic analysis of the rice mutant cpm2 suggests a negative regulatory role of jasmonic acid in drought tolerance. Front. Plant Sci. 8, 1903–1919. doi: 10.3389/fpls.2017.01903

PubMed Abstract | CrossRef Full Text | Google Scholar

Dong, Y. P., Fan, G. Q., Zhao, Z. L., Deng, M. J. (2014). Compatible solute, transporter protein, transcription factor, and hormone-related gene expression provides an indicator of drought stress in Paulownia fortunei. Funct. Integr. Genomic 14, 479–491. doi: 10.1007/s10142-014-0373-4

CrossRef Full Text | Google Scholar

Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., Lepiniec, L. (2010). MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573–581. doi: 10.1016/j.tplants.2010.06.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Fan, W. J., Wang, H. X., Wu, Y. L., Yang, N., Yang, J., Zhang, P. (2017). H (+) -pyrophosphatase IbVP1 promotes efficient iron use in sweetpotato [Ipomoea batatas (L.) Lam.]. Plant Biotechnol. J. 15, 698–712. doi: 10.1111/pbi.12667

PubMed Abstract | CrossRef Full Text | Google Scholar

Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M. M., Seki, M., et al. (2005). AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17, 3470–3488. doi: 10.1105/tpc.105.035659

PubMed Abstract | CrossRef Full Text | Google Scholar

Ghasemnezhad, M., Javaherdashti, M. (2008). Effect of methyl jasmonate treatment on antioxidant capacity internal quality and postharvest life of raspberry on antioxidant capacity internal quality and postharvest life of raspberry fruit. Caspian J. Environ. Sci. 6, 73–78.

Google Scholar

Gill, S. S., Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909–930. doi: 10.1016/j.plaphy.2010.08.016

PubMed Abstract | CrossRef Full Text | Google Scholar

Hajiebrahimi, A., Owji, H., Hemmati, S. (2017). Genome-wide identification, functional prediction, and evolutionary analysis of the R2R3-MYB superfamily in Brassica napus. Genome 60, 797–814. doi: 10.1139/gen-2017-0059

PubMed Abstract | CrossRef Full Text | Google Scholar

He, Q., Jones, D. C., Li, W., Xie, F., Ma, J., Sun, R., et al. (2016). Genome-wide identification of R2R3-MYB genes and expression analyses during abiotic stress in Gossypium raimondii. Sci. Rep. 6, 22980–22993. doi: 10.1038/srep22980

PubMed Abstract | CrossRef Full Text | Google Scholar

Jia, L., Clegg, M. T., Jiang, T. (2004). Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol. 134, 575–585. doi: 10.1104/pp.103.027201

PubMed Abstract | CrossRef Full Text | Google Scholar

Jiang, X. Q., Zhang, C. Q., Lu, P. T., Jiang, G. M., Liu, X. W., Dai, F. W., et al. (2014). RhNAC3, a stress-associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress-related genes in rose petals. Plant Biotechnol. J. 12, 38–48. doi: 10.1111/pbi.12114

PubMed Abstract | CrossRef Full Text | Google Scholar

Jin, Y., Zheng, H. Y., Jin, X. J., Zhang, Y. X., Ren, C. Y. (2016). Effect of ABA, SA and JA on soybean growth under drought stress and re-watering. Soybean Sci. s565, 1. doi: 10.11861/j.issn.1000-9841

CrossRef Full Text | Google Scholar

Jung, C., Seo, J. S., Han, S. W., Koo, Y. J., Kim, C. H., Song, S. I., et al. (2008). Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiol. 146, 623–635. doi: 10.1104/pp.107.110981

PubMed Abstract | CrossRef Full Text | Google Scholar

Kang, C., He, S. Z., Zhai, H., Li, R. J., Zhao, N., Liu, Q. C. (2018b). A sweetpotato auxin response factor gene (IbARF5) is involved in carotenoid biosynthesis and salt and drought tolerance in transgenic Arabidopsis. Front. Plant Sci. 9, 1307. doi: 10.3389/fpls.2018.01307

PubMed Abstract | CrossRef Full Text | Google Scholar

Kang, C., Zhai, H., Xue, L. Y., Zhao, N., He, S. Z., Liu, Q. C. (2018a). A lycopene β-cyclase gene, IbLCYB2, enhances carotenoid contents and abiotic stress tolerance in transgenic sweetpotato. Plant Sci. 272, 243–254. doi: 10.1016/j.plantsci.2018.05.005

PubMed Abstract | CrossRef Full Text | Google Scholar

Kim, H. S., Ji, C. Y., Lee, C. J., Kim, S. E., Park, S. C., Kwak, S. S. (2018). Orange: a target gene for regulating carotenoid homeostasis and increasing plant tolerance to environmental stress in marginal lands. J. Exp. Bot. 69, 3393–3400. doi: 10.1093/jxb/ery023

PubMed Abstract | CrossRef Full Text | Google Scholar

Lee, S. B., Kim, H., Kim, R. J., Suh, M. C. (2014). Overexpression of Arabidopsis MYB96 confers drought resistance in Camelina sativa via cuticular wax accumulation. Plant Cell Rep. 33, 1535–1546. doi: 10.1007/s00299-014-1636-1

PubMed Abstract | CrossRef Full Text | Google Scholar

Li, Y., Wang, Y. N., Zhang, H., Zhang, Q., Zhai, H., Liu, Q. C., et al. (2017). The plasma membrane-localized sucrose transporter IbSWEET10 contributes to the resistance of sweet potato to Fusarium oxysporum. Front. Plant Sci. 8, 197–211. doi: 10.3389/fpls.2017.00197

PubMed Abstract | CrossRef Full Text | Google Scholar

Liang, Y. K., Dubos, C., Dodd, I. C., Holroyd, G. H., Hetherington, A. M., Campbell, M. M. (2005). AtMYB61, an R2R3-MYB transcription factor controlling stomatal aperture in Arabidopsis thaliana. Curr. Biol. 15, 1201–1206. doi: 10.1016/j.cub.2005.06.041

PubMed Abstract | CrossRef Full Text | Google Scholar

Lim, C. W., Han, S. W., Hwang, I. S., Kim, D. S., Hwang, B. K., Lee, S. C. (2015). The pepper lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant Cell Physiol. 56, 930–942. doi: 10.1093/pcp/pcv020

PubMed Abstract | CrossRef Full Text | Google Scholar

Liu, D. G., He, S. Z., Zhai, H., Wang, L. J., Zhao, Y., Wang, B., et al. (2014). Overexpression of IbP5CR enhances salt tolerance in transgenic sweetpotato. Plant Cell Tiss. Org. Cult. 117, 1–16. doi: 10.1007/s11240-013-0415-y

CrossRef Full Text | Google Scholar

Liu, N., Avramova, Z. (2016). Molecular mechanism of the priming by jasmonic acid of specific dehydration stress response genes in Arabidopsis. Epigenet. Chromatin 9, 8–30. doi: 10.1186/s13072-016-0057-5

CrossRef Full Text | Google Scholar

Liu, Z., Zhang, S. M., Sun, N., Liu, H. Y., Zhao, Y. H., Liang, Y. L., et al. (2015). Functional diversity of jasmonates in rice. Rice (N Y) 8, 42–54. doi: 10.1186/s12284-015-0042-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Lorenzo, O., Piqueras, R., Sanchez-Serrano, J. J., Solano, R. (2003). ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15, 165–178. doi: 10.1105/tpc.007468

PubMed Abstract | CrossRef Full Text | Google Scholar

Ma, C., Wang, Z. Q., Zhang, L. T., Sun, M. M., Lin, T. B. (2004). Photosynthetic responses of wheat (Triticum aestivum L.) to combined effects of drought and exogenous methyl jasmonate. Photosynthetica 3, 377–385. doi: 10.1007/s11099-014-0041-x

CrossRef Full Text | Google Scholar

Mueller, M. J. (1997). Enzymes involved in jasmonic acid biosynthesis. Physiol. Plant 100:, 653–663. doi: 10.1111/j.1399-3054.1997.tb03072.x

CrossRef Full Text | Google Scholar

Overmyer, K., Tuominen, H., Kettunen, R., Betz, C., Langebartels, C., Sandermann, H. J., et al. (2000). Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12, 1849–1862. doi: 10.1105/tpc.12.10.1849

PubMed Abstract | CrossRef Full Text | Google Scholar

Park, S. C., Kim, Y. H., Jeong, J. C., Kim, C. Y., Lee, H. S., Bang, J. W., et al. (2011). Sweetpotato late embryogenesis abundant 14 (IbLEA14) gene influences lignification and increases osmotic- and salt stress-tolerance of transgenic calli. Planta 233, 621–634. doi: 10.1007/s00425-010-1326-3

PubMed Abstract | CrossRef Full Text | Google Scholar

Paz-Ares, J., Ghosal, D., Wienand, U., Peterson, P. A., Saedler, H. (1987). The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J. 6, 3558–3558. doi: 10.1002/j.1460-2075.1987.tb02684.x

CrossRef Full Text | Google Scholar

Riechmann, J. L., Heard, J., Martin, G., Reuber, L., Jiang, C. Z., Keddie, J., et al. (2000). Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110. doi: 10.1126/science.290.5499.2105

PubMed Abstract | CrossRef Full Text | Google Scholar

Rohwer, C. L., Erwin, J. E. (2008). Horticultural applications of jasmonates. J. Hortic. Sci. Biotechnol. 83, 283–304. doi: 10.1016/j.biotechadv.2013.09.009

CrossRef Full Text | Google Scholar

Rojo, E., Solano, R., Sanchez-Serrano, J. J. (2003). Interactions between signaling compounds involved in plant defense. J. Plant Growth Reg. 22, 82–98. doi: 10.1007/s00344-003-0027-6

CrossRef Full Text | Google Scholar

Rusconi, F., Simeoni, F., Francia, P., Cominelli, E., Conti, L., Riboni, M., et al. (2013). The Arabidopsis thaliana MYB60 promoter provides a tool for the spatio-temporal control of gene expression in stomatal guard cells. J. Exp. Bot. 64, 3361–3371. doi: 10.1093/jxb/ert180

PubMed Abstract | CrossRef Full Text | Google Scholar

Schmittgen, T. D., Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C-T method. Nat. Protoc. 3, 1101–1108. doi: 10.1038/nprot.2008.73

PubMed Abstract | CrossRef Full Text | Google Scholar

Shiriga, K., Sharma, R., Kumar, K., Yadav, S. K., Hossain, F., Thirunavukkarasu, N. (2014). Genome-wide identification and expression pattern of drought-responsive members of the NAC family in Maize. Meta Gene. 2, 407–417. doi: 10.1016/j.mgene.2014.05.001

PubMed Abstract | CrossRef Full Text | Google Scholar

Smita, S., Katiyar, A., Chinnusamy, V., Pandey, D. M., Bansal, K. C. (2015). Transcriptional regulatory network analysis of MYB transcription factor family genes in rice. Front. Plant Sci. 6, 1157–1175. doi: 10.3389/fpls.2015.01157

PubMed Abstract | CrossRef Full Text | Google Scholar

Strasser, R., Singh, J., Bondili, J. S., Schoberer, J., Svoboda, B., Liebminger, E., et al. (2007). Enzymatic properties and subcellular localization of Arabidopsisβ-N-acetylhexosaminidases. Plant Physiol. 145, 5–16. doi: 10.1104/pp.107.101162

PubMed Abstract | CrossRef Full Text | Google Scholar

Su, L. T., Li, J. W., Liu, D. Q., Zhai, Y., Zhang, H. J., Li, X. W., et al. (2014). A novel MYB transcription factor, GmMYBJ1, from soybean confers drought and cold tolerance in Arabidopsis thaliana. Gene 538, 46–55. doi: 10.1016/j.gene.2014.01.024

PubMed Abstract | CrossRef Full Text | Google Scholar

Su, L. T., Wang, Y., Liu, D. Q., Li, X. W., Zhai, Y., Sun, X., et al. (2015). The soybean gene, GmMYBJ2, encodes a R2R3-type transcription factor involved in drought stress tolerance in Arabidopsis thaliana. Acta Physiol Plant. 37, 155–157. doi: 10.1007/s00192-015-2823-5

CrossRef Full Text | Google Scholar

Tani, T., Sobajima, H., Okada, K., Chujo, T., Arimura, S., Tsutsumi, N., et al. (2008). Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 227, 517–526. doi: 10.1007/s00425-007-0635-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Tester, M., Langridge, P. (2010). Breeding technologies to increase crop production in a changing world. Science 327, 818–822. doi: 10.1126/science.1183700

PubMed Abstract | CrossRef Full Text | Google Scholar

Turner, J. G., Ellis, C., Devoto, A. (2002). The jasmonate signal pathway. Plant Cell 14 Suppl, S153–S164. doi: 10.1105/tpc.000679

PubMed Abstract | CrossRef Full Text | Google Scholar

Uji, Y., Taniguchi, S., Tamaoki, D., Shishido, H., Akimitsu, K., Gomi, K. (2016). Overexpression of OsMYC2 results in the up-regulation of early JA-responsive genes and bacterial blight resistance in rice. Plant Cell Physiol. 57, 1814–1827. doi: 10.1093/pcp/pcw101

PubMed Abstract | CrossRef Full Text | Google Scholar

Vargas, L., Santa, B. A., Mota, F. J., de Carvalho, T. G., Rojas, C. A., Vaneechoutte, D., et al. (2014). Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PLoS One 9, e114744. doi: 10.1371/journal.pone.0114744

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, F. B., Tong, W. J., Zhu, H., Kong, W. L., Peng, R. H., Liu, Q. C., et al. (2016b). A novel Cys2/His2 zinc finger protein gene from sweetpotato, IbZFP1, is involved in salt and drought tolerance in transgenic Arabidopsis. Planta 243, 783–797. doi: 10.1007/s00425-015-2443-9

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, F., Chen, H. W., Li, Q. T., Wei, W., Li, W., Zhang, W. K., et al. (2015). GmWRKY27 interacts with GmMYB174 to reduce expression of GmNAC29 for stress tolerance in soybean plants. Plant J. 83, 224–236. doi: 10.1111/tpj.12879

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, L. Q., Li, Z., Lu, M. Z., Wang, Y. C. (2017a). ThNAC13, a NAC transcription factor from Tamarix hispida, confers salt and osmotic stress tolerance to transgenic Tamarix and Arabidopsis. Front. Plant Sci. 8, 635–647. doi: 10.3389/fpls.2017.00635

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, N., Zhang, W. X., Qin, M. Y., Li, S., Qiao, M., Liu, Z. H., et al. (2017b). Drought tolerance conferred in soybean (Glycine max. L) by GmMYB84, a novel R2R3-MYB transcription factor. Plant Cell Physiol. 58, 1764–1776. doi: 10.1093/pcp/pcx111

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, R. K., Cao, Z. H., Hao, Y. J. (2014). Overexpression of a R2R3 MYB gene MdSIMYB1 increases tolerance to multiple stresses in transgenic tobacco and apples. Physiol. Plant 150, 76–87. doi: 10.1111/ppl.12069

PubMed Abstract | CrossRef Full Text | Google Scholar

Wang, S. Y. (1999). Methyl jasmonate reduces water stress in strawberry. J. Plant Growth Reg. 18, 127–134. doi: 10.1007/PL00007060

CrossRef Full Text | Google Scholar

Wang, Z., Wang, F., Hong, Y., Huang, J., Shi, H., Zhu, J. K. (2016a). Two chloroplast proteins suppress drought resistance by affecting ROS production in guard cells. Plant Physiol. 172, 2491–2503. doi: 10.1104/pp.16.00889

PubMed Abstract | CrossRef Full Text | Google Scholar

Wasternack, C., Hause, B. (2013). Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 111, 1021–1058. doi: 10.1093/aob/mct067

PubMed Abstract | CrossRef Full Text | Google Scholar

Wasternack, C., Stenzel, I., Hause, B., Hause, G., Kutter, C., Maucher, H., et al. (2006). The wound response in tomato-role of jasmonic acid. J. Plant Physiol. 163, 297–306. doi: 10.1016/j.jplph.2005.10.014

PubMed Abstract | CrossRef Full Text | Google Scholar

Xie, D. X., Feys, B. F., James, S., Nieto-Rostro, M., Turner, J. G. (1998). COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091–1094. doi: 10.1126/science.280.5366.1091

PubMed Abstract | CrossRef Full Text | Google Scholar

Xu, Y., Burgess, P., Huang, B. (2017). Transcriptional regulation of hormone-synthesis and signaling pathways by overexpressing cytokinin-synthesis contributes to improved drought tolerance in creeping bentgrass. Physiol. Plant 161, 235–256. doi: 10.1111/ppl.12588

PubMed Abstract | CrossRef Full Text | Google Scholar

Yang, A., Dai, X., Zhang, W. H. (2012). A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J. Exp. Bot. 63, 2541–2556. doi: 10.1093/jxb/err431

PubMed Abstract | CrossRef Full Text | Google Scholar

Yang, S. J., Vanderbeld, B., Wan, J. X., Huang, Y. F. (2010). Narrowing down the targets: towards successful genetic engineering of drought-tolerant crop. Mol. Plant. 3, 469–490. doi: 10.1093/mp/ssq016

PubMed Abstract | CrossRef Full Text | Google Scholar

Yoshii, M., Yamazaki, M., Rakwal, R., Kishi-Kaboshi, M., Miyao, A., Hirochika, H. (2010). The NAC transcription factor RIM1 of rice is a new regulator of jasmonate signaling. Plant J. 61, 804–815. doi: 10.1111/j.1365-313X.2009.04107.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Yu, H., Chen, X., Hong, Y. Y., Wang, Y., Xu, P., Ke, S. D., et al. (2008). Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20, 1134–1151. doi: 10.1105/tpc.108.058263

PubMed Abstract | CrossRef Full Text | Google Scholar

Yuan, Y., Qi, L. J., Yang, J., Wu, C., Liu, Y. J., Huang, L. Q. (2015). A Scutellaria baicalensis R2R3-MYB gene, SbMYB8, regulates flavonoid biosynthesis and improves drought stress tolerance in transgenic tobacco. Plant Cell Tiss. Org. Cult. 120, 973–973. doi: 10.1007/s11240-014-0650-x

CrossRef Full Text | Google Scholar

Zhang, C., Zhang, L., Zhang, S., Zhu, S., Wu, P., Chen, Y., et al. (2015a). Global analysis of gene expression profiles in physic nut (Jatropha curcas L.) seedlings exposed to drought stress. BMC Plant Biol. 15, 17–30. doi: 10.1186/s12870-014-0397-x

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhang, F., Yao, J., Ke, J. Y., Zhang, L., Lam, V. Q., Xin, X. F., et al. (2015b). Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling. Nature 525, 269–273. doi: 10.1038/nature14661

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhang, H., Zhang, Q., Zhai, H., Li, Y., Wang, X. F., Liu, Q. C., et al. (2017). Transcript profile analysis reveals important roles of jasmonic acid signalling pathway in the response of sweet potato to salt stress. Sci. Rep. 7, 40819–40830. doi: 10.1038/srep40819

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhao, Y., Dong, W., Zhang, N. B., Ai, X. H., Wang, M. C., Huang, Z. G., et al. (2014). A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiol. 164, 1068–1076. doi: 10.1104/pp.113.227595

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhu, H., Zhou, Y. Y., Zhai, H., He, S. Z., Zhao, N., Liu, Q. C. (2018). Transcriptome profiling reveals insights into the molecular mechanism of drought tolerance in sweetpotato. J. Inter. Agri. 17, 60345–60347. doi: 10.1016/S2095-3119(18)61934-3

CrossRef Full Text | Google Scholar

Zhu, J. K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant. Biol. 53, 247–273. doi: 10.1146/annurev.arplant.53.091401.143329

PubMed Abstract | CrossRef Full Text | Google Scholar

Zhu, J. K. (2016). Abiotic stress signaling and responses in plants. Cell 167, 313–324. doi: 10.1016/j.cell.2016.08.029

PubMed Abstract | CrossRef Full Text | Google Scholar

Zong, W., Tang, N., Yang, J., Peng, L., Ma, S. Q., Xu, Y., et al. (2016). Feedback regulation of ABA signaling and biosybthesis by a bZIP transcription factor of targets drought-resistance-related genes. Plant Physiol. 171, 2810–2825. doi: 10.1104/pp.16.00469

PubMed Abstract | CrossRef Full Text | Google Scholar

Keywords: sweetpotato, IbMYB116, Arabidopsis, drought tolerance, JA signaling pathway

Citation: Zhou Y, Zhu H, He S, Zhai H, Zhao N, Xing S, Wei Z and Liu Q (2019) A Novel Sweetpotato Transcription Factor Gene IbMYB116 Enhances Drought Tolerance in Transgenic Arabidopsis. Front. Plant Sci. 10:1025. doi: 10.3389/fpls.2019.01025

Received: 10 December 2018; Accepted: 22 July 2019;
Published: 15 August 2019.

Edited by:

Susanne Berger, Julius Maximilian University of Würzburg, Germany

Reviewed by:

Ratna Karan, University of Florida, United States
Eric Ruelland, Centre National de la Recherche Scientifique (CNRS), France

Copyright © 2019 Zhou, Zhu, He, Zhai, Zhao, Xing, Wei and Liu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Qingchang Liu, liuqc@cau.edu.cn