Crosstalk between GABA and ALA to improve antioxidation and cell expansion of tomato seedling under cold stress
Introduction
Plant cell membrane is a flowing structure; however, cold stress reduces its fluidity and increases its hardness (Ding et al., 2019). Plants can sense cold signals through the changes in cell membrane fluidity, subsequently inducing downstream signalling substances, including plant hormones, reactive oxygen species (ROS), nitric oxide (NO) and mitogen-activated protein kinases (Lv et al., 2018; Zhu, 2016). These substances regulate downstream transcription factors, such as C-repeat binding factors (CBFs), to induce COR expression, thereby improving plant cold resistance (Boudsocq and Sheen, 2013; Lv et al., 2018). However, persistent or severe cold stress causes excessive accumulation of intracellular ROS, resulting in membrane lipid peroxidation (Ding et al., 2019; Megha et al., 2018). This damage in turn causes metabolic plant disorders that affect normal growth and development (Baier et al., 2019; Wang et al., 2019; Willems et al., 2016). Therefore, maintaining the integrity and stability of the cell membrane structure is particularly important for the normal growth and development of plants. Plants can regulate cell membrane stability through external (e.g. cell wall) and internal (e.g. antioxidant) factors.
Cell wall, as the external structure of the cell membrane, is the first barrier for plants perceiving changes in the external environment (Yan et al., 2019). The highly dynamic structure of cell wall provides the foundation and mechanical support for plant growth and development and resistance to adversity (Vaahtera et al., 2019). Cell wall formation includes cell wall expansion and reconstruction and cell wall component synthesis, assembly and deposition; among them, cell wall expansion is an important part (Reiter, 2002). Cell enlargement caused by plant cell wall expansion increases the leaf area and affects the looseness of the leaf tissue structure, thereby enhancing photosynthesis and promoting plant tissue growth (Clemente-Moreno et al., 2019). The regulators of cell wall expansion include xyloglucan endotransglucosylase/hydrolases (XTHs), glycoside hydrolase, expansin and hydroxyl radical (Tenhaken, 2015). Among them, XTHs play important roles (Han et al., 2013; Rui and Dinneny, 2019). Studies have shown that the increase in XTH transcription may play a role in the positive regulation of plant salt and drought tolerance by enhancing the strength and thickness of plant cells, ensuring structural integrity (Han et al., 2017) and adjusting the structure and size of the mesophyll cell (Han et al., 2013). However, whether XTHs regulate plant cold tolerance by regulating cell remodelling and integrity is still unclear.
In addition, cell wall integrity signalling is transduced and stimulates downstream signals, including ROS which is produced by NADPH oxidases, and phytohormones, such as jasmonate, ethylene and salicylic acid (Wolf et al., 2012). These signals can ultimately stimulate cytoplasmic antioxidation to regulate redox balance and maintain the structural integrity of cells (Liu et al., 2019a, 2019b). Appropriate ROS, like XTHs, can also regulate cell wall expansion. A close relationship between cell wall expansion and redox balance/ antioxidants exists in plants under stress (Tenhaken, 2015).
Tomatoes are important thermophile vegetables widely cultivated worldwide. Low-temperature stress (mainly cold stress) often occurs in protected cultivations in China, inhibiting plant growth and ultimately affecting yield formation (Liu et al., 2018). Cell expansion increased plant leaf area can enhance the total photosynthetic capacity, promote plant growth and improve plant stress resistance (Clemente-Moreno et al., 2019). Therefore, exploring the methods to regulate tomato cell wall expansion and redox balance/ antioxidants is very important for alleviating cold inhibition in plant growth.
Exogenous 5-aminolevulinic acid (ALA) is known as a new, green plant growth regulator that play key roles in enhancing plant stress tolerance (Akram and Ashraf, 2013; An et al., 2019; Anwar et al., 2018). Our previous research showed that exogenous 5-aminolevulinic acid (ALA) can directly participate in chlorophyll synthesis to regulate photosynthesis, and enhance tomato cold stress resistance by increasing antioxidation and endogenous hormone levels (Liu et al., 2018, 2019b). ALA is formatted from glutamate (Glu) catalysed by glutamate-tRNA synthetase, glutamate-tRNA reductase and glutamate-1-semialdehyde aminotransferase (Tripathy and Pattanayak, 2012). Glu is also a precursor of gamma-aminobutyric acid (GABA) catalysed by glutamate decarboxylase (GAD), which is the main pathway for GABA synthesis in plants (Bao et al., 2015). Numerous studies have shown that exogenous GABA could also improve plant stress tolerance by regulating antioxidant capacity, the substance levels in osmotic adjustment and ion balance (Guo et al., 2020; Jin et al., 2019). Thus, ALA and GABA may be closely related or synergistic in regulating plant metabolism and cold stress tolerance. This study aimed to explore the roles of ALA and GABA, and their internal relationship in regulating antioxidation and cell morphological changes related to tomato plant growth and cold tolerance.
Section snippets
Plant growth conditions and treatments
Solanum lycopersicum Jinpeng No. 1 cultivars (cold sensitive) was used in this work. Seedlings were cultivated in accordance with our previous methods (Liu et al., 2018). Seeds were germinated and sown in 50-well plates filled with substrate containing peat, vermiculite and perlite (2:1:1, v/v/v). After the fourth true leaf was expanded, they were transplanted individually into a plastic pot (10 cm × 10 cm), and still cultivated in climate chambers with normal conditions (25 °C/18 °C,
Exogenous ALA and GABA regulated mutual transformation of endogenous ALA and GABA in tomato under low temperatures
Transcriptome and RT-qPCR analysis showed that ALA treatment significantly up-regulated the SlGAD4 expression under cold stress (Fig. S1). Thus, the effects of exogenous ALA and GABA on the endogenous ALA and GABA levels were further explored (Fig. 1, Fig. 2). Under normal condition, the exogenous ALA or GABA treatments had no significant influence on the endogenous Glu and GABA contents, whereas cold treatment dramatically increased their contents compared with the control plants (Fig. 1).
Discussion
Cold stress inhibited crop growth and yield formation, causing serious yield losses (Barrero-Gil et al., 2016; Duan et al., 2012). Our previous studies showed that exogenous ALA increases endogenous ALA content which may mostly participate in chlorophyll synthesis under cold stress, and enhanced the antioxidation of tomato by regulating the H2O2→NO signal pathway (Liu et al., 2019b). GABA application could also improve plant cold stress tolerance by increasing endogenous GABA, which is involved
Authors contribution
T.L., X.H., H.Q., and J.L. designed the experiments and wrote the manuscript. T.L., X.J., S.Y., X.Y., and Z.Z. performed the experiments. T.L., and X.H. analyzed the data. All authors have read and approved the final version of the manuscript.
Declaration of Competing Interest
The authors declare that they have no competing interests.
Acknowledgements
This work was supported by grants from National Key R & D Program of China (2019YFD1001902), the National Natural Science Foundation of China (32002116), the China Agriculture Research System (CARS-23-C-05, CARS-23-C-07), and the Research Start Funding of Shenyang Agricultural University (880419015).
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