Research articlePhotochemistry and proteomics of ginger (Zingiber officinale Roscoe) under drought and shading
Introduction
Increasing global atmospheric CO2 concentrations are associated with reductions in average precipitation in mid-latitude and subtropical regions (Zandalinas et al., 2018). Drought-induced fires are expected to further increase atmospheric CO2 concentrations (Aragão et al., 2018), resulting in a vicious cycle. Drought can affect the normal growth of crops by inhibiting root development (Hasibeder et al., 2015), reducing stomatal opening (Martin StPaul et al., 2017), altering water use efficiency (Yang et al., 2016), producing superoxide anions (Anjum et al., 2017), degrading key enzymes (Carmo-Silva et al., 2010) and, in severe cases, damaging the photosynthetic apparatus (Silva et al., 2003). Drought is an ecological problem that must be confronted without delay.
As an important industrial crop in China, ginger has important applications in food, industry and other fields. China is the world's main producer of ginger, but statistics from the China Meteorological Administration (http://www.cma.gov.cn) indicate that annual precipitation in the important ginger-producing regions of Shandong and Henan has been less than 1000 mm/year on average for the past five years, causing ginger to experience drought stress frequently.
Photosynthesis is the main process by which carbohydrates are assimilated and accumulated, and the effects of drought stress on crops are first reflected in photosynthesis. Early in drought stress, leaves initiate a stress response by closing their stomata (Anjum et al., 2011; Ji et al., 2018) to reduce transpirational water loss (Miyashita et al., 2005), and the resulting decline in CO2 uptake leads to a decline in photosynthetic rate, mainly as a result of stomatal limitation (Liu et al., 2017). As drought stress increases, the activity of photosynthetic enzymes decreases (Dias and Brüggemann, 2010), as do photophosphorylation and ATP synthesis (Ji et al., 2012), leading to further decreases in CO2 assimilation due to non-stomatal limitation (Ji et al., 2012). Under severe drought, superoxide anions are produced in large quantities (Tian et al., 2012), causing damage to the photosynthetic system (Yan et al., 2010). The degradation of the D1 protein of photosystem II (PSII) directly abolishes photosynthetic electron transport (Batra et al., 2014), ultimately leading to crop death. However, a series of protective mechanisms also exist to mitigate photosynthetic damage, including the Mehler reaction for scavenging superoxide anions (Mehler, 1951; Carvalho, 2018), and photorespiration and xanthophyll cycle for the dissipation of excess light energy (Wang et al., 2010; Voss et al., 2013; Zhou et al., 2015b).
Under drought stress, plants may reduce photochemical damage by the natural folding of their leaves, and the resultant shading can reduce damage by lowering photon flux density (Thomas and Turner, 2001). Shading can mitigate the adverse effects of drought stress, especially for crops, such as ginger, that have low light saturation points. On the other hand, shading is ineffective for crops, such as coffee, that have higher light saturation points (Cavatte et al., 2012). The alleviation of drought stress by shading arises mainly from decreased stomatal limitation, reduced photochemical inactivation of the photosystems, maintenance of higher water use efficiency, and, as a result, higher photosynthetic electron transfer efficiency (Montanaro et al., 2009). Shading can also protect the antioxidant enzyme activities in ginger, underscoring the necessity of shade in cultivation under dry, sunny conditions during the spring and summer (Zhang et al., 2013).
Proteomics provides insights into gene regulation and has been widely used to study plant responses to drought stress (Budak et al., 2013; Rollins et al., 2013; Alvarez et al., 2014; Jedmowski et al., 2014; Lyon et al., 2016; Wu et al., 2019). The proteins that are differentially expressed in response to drought stress are involved in many cellular functions and differ among plant organs. For example, proteins related to osmotic regulation, defense signals and programmed cell death play an important role in the drought adaptation of roots (Alam et al., 2010; Faghani et al., 2015; Hao et al., 2015), while proteins related to cell wall biosynthesis and photosynthesis are differentially expressed in response to drought in leaves (Faghani et al., 2015; Hao et al., 2015). Comparative proteomics has also been used to demonstrate increases in metabolism-related proteins and decreases in energy- and translation-related proteins under drought and to identify methionine synthetase as a drought response protein (Mohammadi et al., 2012). Comparative proteomics at the cellular level demonstrated that drought stress induced ribosome-related functions and upregulated an oxidative phosphorylation protein. Furthermore, an endocytosis protein was also significantly enriched under drought, consistent with an increase in active transport and circulation of membrane proteins under abiotic stress (Alqurashi et al., 2018). When combined with plant genetic transformation, proteomics can also provide insights into protein interactions (Meng et al., 2019).
Although the physiological responses of ginger to drought stress have been studied, the molecular mechanisms by which ginger responds to drought and shading remain unclear. Therefore, it is particularly important to characterize the expression and metabolic pathways of proteins whose abundance changes in response to drought and shading. Ours is the first study to use an iTRAQ tandem mass spectrometry approach to analyze the response of ginger proteins to drought and shading. In particular, the molecular mechanisms of drought and shading response were investigated by measuring protein levels of photosynthetic electron transport chain components. This work lays a foundation for further studies of photosynthetic electron transport under stress in ginger and provides a theoretical basis for the alleviation of drought stress during ginger production.
Section snippets
Methods and materials
Experiments were performed at the experiment centre of Shandong Agricultural University (36°160′N, 117°156′E) in China. A soil-free culture system was used in order to minimize the effects of extraneous variables. The ginger cultivar ‘Shannong 1’ was sown in pots (25 cm diameter, 30 cm height) filled with acid-cleaned quartz sand on 10 May 2018, and Hoagland's nutrient solution (Sarwar et al., 2018) was added once every three days. When seedlings had five or six leaves and three branches, four
Analysis of H2O–CO2 exchange parameters
Abiotic stress can inhibit photosynthetic electron transport, resulting in a lower photosynthetic rate (Berla et al., 2015; Zhang and Liu, 2016) due to stomatal and/or non-stomatal limitations (Chandra et al., 2018). In a previous study, the photosynthetic rate of ginger decreased significantly under high tetracycline concentration, and measurements of stomatal conductance and intercellular CO2 suggested that the decrease resulted primarily from non-stomatal limitation (Liu et al., 2018). This
Conclusion
In conclusion, our data suggest that ginger alleviates drought-related damage by increasing CEF around PSI at the cost of reduced electron transfer efficiency and photosynthetic rate. Heat dissipation is also increased under drought stress. Shading significantly improves photosynthetic electron transport efficiency, enhances the photosynthesis of ginger leaves, and alleviates some of the effects of drought, further highlighting the necessity of shade in the cultivation of ginger under the dry,
Declaration of competing interest
The authors declare that they have no conflict of interest.
Acknowledgement
We appreciate the linguistic assistance provided by TopEdit (www.topeditsci.com) during the preparation of this manuscript. This study was supported by China Agricultural Research System (Grant No. CARS-24-A-09), Taishan Industrial Experts Programme, China (Grant No. tscy20190105), and Shandong Province's Dual-class Discipline Construction Project, China (Grant No. SYL2017YSTD06).
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