Research articleEthylene promotes germination of Arabidopsis seed under salinity by decreasing reactive oxygen species: Evidence for the involvement of nitric oxide simulated by sodium nitroprusside
Introduction
In many areas of the world increasing salinity of cropland has become a major constraint to agricultural production [1], [2]. Seed germination is a key ecological and agronomic trait, which plays a critical role affecting the subsequent growth and production of higher plants. Germination is highly regulated by both internal and external cues that determine the dormancy status of the seed and the potential for germination [3]. Salinity decreases the rate of germination and the proportion of seed germinating and thus impairs seedling establishment in many species [4], [5], [6]. Therefore, understanding the underlying mechanisms that regulate seed germination under salinity is of vital importance for agriculture.
Reactive oxygen species (ROS) play an important role in the regulation of germination under both normal and stress conditions. Accumulation of ROS is required for breaking dormancy and seed germination in many plant species [8], [9], [10], [11]. However, under conditions such as salinity the rate of production of ROS is dramatically elevated, causing oxidative stress [7]. It is established that H2O2, a representative ROS, accumulates more in germinating seeds under saline conditions than in non-saline conditions, which correlates with markedly delayed germination [12], [13]. In addition, H2O2 is involved in mediating the interaction between abscisic acid (ABA) and gibberellic acid (GA) during alleviation of dormancy and seed germination in Arabidopsis [14], indicating that ROS are good candidates for mediating hormone interactions [11]. Therefore, it is important to understand the regulatory networks involving ROS in plant responses to abiotic stress during various development stages, such as seed germination under salinity stress.
Ethylene is involved in many abiotic stress responses and has long been recognized as a stress hormone [15]. The biosynthetic pathway of ethylene involves the conversion of S-adenosyl methionine to ACC by ACC synthase (ACS) and then of ACC to ethylene by ACC oxidase (ACO) [16]. ACC synthesis is generally the rate-limiting step for ethylene production during vegetative growth [17]. In seedlings an increase in ACS protein increases ethylene synthesis [11] and also phosphorylation of ACS2 by stress-responsive MAPKs might increase ethylene synthesis [17], [18], [19]. Generally, seed germination is subject to tight hormonal control [20]. It has been found that ethylene can alleviate germination inhibition induced by salinity in many seeds [13], [21], [22] but ethylene is not the only factor controlling this process: ethylene promotes germination under salinity by modulating ROS production [13]. Little is known about how ethylene interacts with other signals to regulate seed germination under salinity.
Nitric oxide (NO) is a signalling molecule which is involved in the control and regulation of a variety of plant responses to environmental stresses, such as drought, cold, salinity stress and disease resistance in almost all stages of development [23], [24], [25], [26], [27], [28]. Tolerance of plants to salinity can be enhanced by increasing NO content by expressing rat neuronal NO synthase in Arabidopsis thaliana [29]. Nitric oxide stimulates germination of seeds by breaking dormancy [9], [30], [31]. Notably, NO often exerts its regulatory activity in tight coordination with other molecules, such as ROS, thereby stimulating germination [9], [26]. The antioxidant function of NO, by inducing superoxide dismutase or by directly scavenging superoxide in response to stress stimuli, has been reported in plant models [32]. The underlying mechanisms by which ROS and NO participate in germination under salinity, and the potential interaction between them during germination, are still unclear.
Recently, the interaction between ethylene and NO has been well studied. NO can stimulate ethylene production under various conditions such as ozone stress and ion deficiency and when dormancy is breaking and germination is initiated [20], [33], [34], [35]. The potential for analysing the mechanisms of action and interaction of ethylene and NO by use of mutants altered in ethylene signalling as well as their effects in regulating seed germination under salinity has not been exploited. In the present study, we use seed of the ethylene insensitive mutant (ein3-1) and wild-type Col-0 of Arabidopsis to investigate the regulatory network between ethylene and NO and elucidate the physiological mechanisms of ethylene and NO in increasing germination under salinity. The results indicate that both ethylene and NO production increased under salinity in germinating seeds; and that each one influenced the production of the other. The increased ethylene biosynthesis then decreased hydrogen peroxide level induced by salinity and ultimately increased seed germination rate.
Section snippets
Seed germination in Col-0 and ein3-1 plants was affected by salinity
Salinity (NaCl) significantly delayed or inhibited seed germination rate of wild-type Arabidopsis Col-0, compared to the control (without NaCl): with 100 mM NaCl about 82% germinated 3 days after transfer to light compared to almost 100% in the control and with 150 and 200 mM NaCl seed germination rate was severely inhibited (Fig. 1A). Seed germination of ein3-1 was delayed compared to that of Col-0 particularly with increasing salinity. Under mild salinity (50 mM NaCl), after 2 days only 17%
Discussion
It is commonly accepted that ethylene plays a crucial role in overcoming seed dormancy [36], and its production increases during dormancy release and germination in many plants [9], [20]. Under salinity the production of ethylene increased in rice, wheat, maize and soybean during germination [6], indicating strong involvement of ethylene in germination of seeds. Our previous studies showed that ethylene antagonizes the inhibition of germination in Arabidopsis induced by salinity by decreasing
Plant materials and growth conditions
Wild type Columbia ecotype (Col-0) and ein3-1 [44] seeds were surface sterilized by incubating for 10 min in 70% ethanol containing 0.05% Triton X-100 (Solar Bio, Beijing, China), and rinsed thoroughly with ethanol for 1 min, then washed with sterilized water. The sterilized seeds were sown on 1/2 MS medium containing MS basal salt mixture (Sigma–Aldrich, St Louis, MO, USA), 1% sucrose, 0.8% agar, pH 5.7. After stratification at 4 °C in the dark for 48 h, the seeds were then cultivated at 23 °C
Acknowledgements
The authors thank Prof Guo Hongwei (Peking University, China) for providing Arabidopsis seeds used in this report. We also wish to thank two anonymous reviewers for their valuable comments on the work and Prof David Lawlor (Rothamsted Research, UK) for critical reading of the manuscript. This study was supported by National Natural Science Foundation of China (31370007 and 31000176) and the Fundamental Research Funds for the Central Universities (DL12CA02).
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