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A WD40-Repeat Protein From the Recretohalophyte Limonium bicolor Enhances Trichome Formation and Salt Tolerance in Arabidopsis.

ABSTRACT: The Arabidopsis thaliana WD40-repeat protein TRANSPARENT TESTA GLABRA1 (TTG1) controls epidermis development, playing opposite roles in trichome differentiation and root hair formation. We isolated and characterized LbTTG1 (encoding a WD40-repeat protein with high sequence similarity to TTG1) from the recretohalophyte Limonium bicolor, which actively excretes absorbed salt via a salt gland. The complete open reading frame of LbTTG1 was 1,095 bp, encoding a protein of 364 amino acids, and showed highest expression during the salt gland initiation stage. We heterologously expressed LbTTG1 in wild type and ttg1-13 Arabidopsis plants to verify the protein's function, and the copies of LbTTG1 were identified in transgenic strains using southern blotting. Trichomes were extremely induced on the first true leaves of plants heterologously expressing LbTTG1, whereas no trichomes were produced by ttg1-13 plants. Conversely, plants heterologously expressing LbTTG1 produced fewer root hairs than ttg1-13 plants. In plants heterologously expressing LbTTG1 compared to controls, epidermis differentiation genes (GLABRA1 and GLABRA3) were up-regulated while genes encoding negative regulators of trichome development (TRIPTYCHON and CAPRICE) were down-regulated. Under increased NaCl concentrations, both of the transgenic lines showed enhanced germination and root length, and accumulated less malondialdehyde (MDA) and Na+ and produced more proline, soluble sugar, and higher glutathione S-transferase activity, compared with the ttg1-13 mutant. These results indicate that LbTTG1 participates in epidermis development in Arabidopsis, similarly to other WD40-repeat proteins, and specifically increases salt tolerance of transgenic Arabidopsis by reducing ion accumulation and increasing osmolyte levels.

SUBMITTER: Yuan F

PROVIDER: S-EPMC6861380 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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A WD40-Repeat Protein From the Recretohalophyte Limonium bicolor Enhances Trichome Formation and Salt Tolerance in Arabidopsis.

Yuan Fang F Leng Bingying B Zhang Haonan H Wang Xi X Han Guoliang G Wang Baoshan B

Frontiers in plant science 20191112

The Arabidopsis thaliana WD40-repeat protein TRANSPARENT TESTA GLABRA1 (TTG1) controls epidermis development, playing opposite roles in trichome differentiation and root hair formation. We isolated and characterized LbTTG1 (encoding a WD40-repeat protein with high sequence similarity to TTG1) from the recretohalophyte Limonium bicolor, which actively excretes absorbed salt via a salt gland. The complete open reading frame of LbTTG1 was 1,095 bp, e ...[more]

PMID: 31781150

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Project description:AimsTo elucidate the genetics underlying salt tolerance in recretohalophytes and assess its relevance to non-halophytes, we cloned the Limonium bicolor homolog of Arabidopsis thaliana (Arabidopsis) SUPER SENSITIVE TO ABA AND DROUGHT2 (AtSAD2) and named it LbSAD2, an importin-β gene associated with trichome initiation and reduced abscisic acid (ABA) sensitivity, and then we assessed the heterologously expressed LbSAD2 in Arabidopsis.MethodsWe examined LbSAD2 expression and assessed the effect of heterologous LbSAD2 expression in Arabidopsis on root hair/trichome induction; the expression levels of possible related genes in trichome/root hair development; some physiological parameters involved in salt tolerance including germination rate, root length, and contents of Na+, proline, and malondialdehyde; and the response of ABA at the germination stage.ResultsThe LbSAD2 gene is highly expressed in the salt gland development stage and salt treatment, especially located in the salt gland by in situ hybridization, and the LbSAD2 protein contains some special domains compared with AtSAD2, which may suggest the involvement of LbSAD2 in salt tolerance. Compared with the SAD2/GL1 mutant CS65878, which lacks trichomes, CS65878-35S:LbSAD2 had higher trichome abundance but lower root hair abundance. Under 100 mM NaCl treatment, CS65878-35S:LbSAD2 showed enhanced germination and root lengths; improved physiological parameters, including high proline and low contents of Na+ and malondialdehyde; higher expression of the salt-tolerance genes Δ1-PYRROLINE-5-CARBOXYLATE SYNTHETASE 1 (P5CS1) and GST CLASS TAU 5 (GSTU5); reduced ABA sensitivity; and increased expression of the ABA signaling genes RESPONSIVE TO ABA 18 (RAB18) and SNF1-RELATED PROTEIN KINASE 2 (SRK2E), but not of the ABA biosynthesis gene 9-CIS-EPOXYCAROTENOID DIOXYGENASE 3 (NCED3).ConclusionLbSAD2 enhances salt tolerance in Arabidopsis by specifically reducing root hair development, Na+ accumulation, and ABA sensitivity.

Project description:BackgroundSoil salinization is becoming an increasingly serious problem worldwide, resulting in cultivated land loss and desertification, as well as having a serious impact on agriculture and the economy. The indoleamine melatonin (N-acetyl-5-methoxytryptamine) has a wide array of biological roles in plants, including acting as an auxin analog and an antioxidant. Previous studies have shown that exogenous melatonin application alleviates the salt-induced growth inhibition in non-halophyte plants; however, to our knowledge, melatonin effects have not been examined on halophytes, and it is unclear whether melatonin provides similar protection to salt-exposed halophytic plants.ResultsWe exposed the halophyte Limonium bicolor to salt stress (300 mM) and concomitantly treated the plants with 5 μM melatonin to examine the effect of melatonin on salt tolerance. Exogenous melatonin treatment promoted the growth of L. bicolor under salt stress, as reflected by increasing its fresh weight and leaf area. This increased growth was caused by an increase in net photosynthetic rate and water use efficiency. Treatment of salt-stressed L. bicolor seedlings with 5 μM melatonin also enhanced the activities of antioxidants (superoxide dismutase [SOD], peroxidase [POD], catalase [CAT], and ascorbate peroxidase [APX]), while significantly decreasing the contents of hydrogen peroxide (H2O2), superoxide anion (O2•-), and malondialdehyde (MDA). To screen for L. bicolor genes involved in the above physiological processes, high-throughput RNA sequencing was conducted. A gene ontology enrichment analysis indicated that genes related to photosynthesis, reactive oxygen species scavenging, the auxin-dependent signaling pathway and mitogen-activated protein kinase (MAPK) were highly expressed under melatonin treatment. These data indicated that melatonin improved photosynthesis, decreased reactive oxygen species (ROS) and activated MAPK-mediated antioxidant responses, triggering a downstream MAPK cascade that upregulated the expression of antioxidant-related genes. Thus, melatonin improves the salt tolerance of L. bicolor by increasing photosynthesis and improving cellular redox homeostasis under salt stress.ConclusionsOur results showed that melatonin can upregulate the expression of genes related to photosynthesis, reactive oxygen species scavenging and mitogen-activated protein kinase (MAPK) of L. bicolor under salt stress, which can improve photosynthesis and antioxidant enzyme activities. Thus melatonin can promote the growth of the species and maintain the homeostasis of reactive oxygen species to alleviate salt stress.

Project description:BACKGROUND:Salt, a common environmental stress factor, inhibits plant growth and reduces yields. Melatonin is a pleiotropic molecule that regulates plant growth and can alleviate environmental stress in plants. All previous research on this topic has focused on the use of melatonin to improve the relatively low salt tolerance of glycophytes by promoting growth and enhancing antioxidant ability. It is unclear whether exogenous melatonin can increase the salt tolerance of halophytes, particularly recretohalophytes, by enhancing salt secretion from the salt glands. RESULTS:To examine the mechanisms of melatonin-mediated salt tolerance, we explored the effects of exogenous applications of melatonin on the secretion of salt from the salt glands of Limonium bicolor (a kind of recretohalophyte) seedlings and on the expression of associated genes. A pretreatment with 5??M melatonin significantly improved the growth of L. bicolor seedlings under 300?mM NaCl. Furthermore, exogenous melatonin significantly increased the dry weight and endogenous melatonin content of L. bicolor. In addition, this treatment reduced the content of Na+ and Cl- in leaves, but increased the K+ content. Both the salt secretion rate of the salt glands and the expression level of genes encoding ion transporters (LbHTK1, LbSOS1, LbPMA, and LbNHX1) and vesicular transport proteins (LbVAMP721, LbVAP27, and LbVAMP12) were significantly increased by exogenous melatonin treatment. These results indicate that melatonin improves the salt tolerance of the recretohalophyte L. bicolor via the upregulation of salt secretion by the salt glands. CONCLUSIONS:Our results showed that melatonin can upregulate the expression of genes encoding ion transporters and vesicle transport proteins to enhance salt secretion from the salt glands. Combining the results of the current study with previous research, we formulated a novel mechanism by which melatonin increases salt secretion in L. bicolor. Ions in mesophyll cells are transported to the salt glands through ion transporters located at the plasma membrane. After the ions enter the salt glands, they are transported to the collecting chamber adjacent to the secretory pore through vesicle transport and ions transporter and then are secreted from the secretory pore of salt glands, which maintain ionic homeostasis in the cells and alleviate NaCl-induced growth inhibition.

Dataset Information

A WD40-Repeat Protein From the Recretohalophyte Limonium bicolor Enhances Trichome Formation and Salt Tolerance in Arabidopsis.

Publications

A WD40-Repeat Protein From the Recretohalophyte <i>Limonium bicolor</i> Enhances Trichome Formation and Salt Tolerance in <i>Arabidopsis</i>.

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