A novel ethylene responsive factor CitERF13 plays a role in photosynthesis regulation
Introduction
Photosynthesis is the basic manufacturing process required for the existence of life in this planet, it can increase carbon gain thus improve the crop yield and quality. It is greately regulated by diverse signals, including environmental stresses such as drought, chilling, heavy metals [1], [2], [3], [4], as well as phytohormones, which are effective in regulating photosynthesis in different biochemical, physiological situations and molecular mechanisms [5]. In recent years, phytohormones have been reported to be involved in protecting and alleviating stress by modulating metabolic processes in plants. Gibberellic acid (GA) has been reported to improve photosynthetic efficiency and stomatal conductance in wheat, mustard and linseed [6], [7], [8]. Brassinosteroid (BR) enhanced photosynthesis by inducing expressions of photosynthetic genes and enhancing the activation state of Rubisco [9], [10]. Interestingly, BR-induced hydrogen peroxide (H2O2) accumulation in the apoplast of mesophyll cells plays a role in this process [11]. Abscisic acid (ABA) is considered to protect the photosynthetic apparatus in stress conditions. ABA has been reported to alleviate the salt stress-induced decline in the efficiency of photosystem II (PSII) photochemistry and enhance PSII efficiency and non-photochemical quenching (NPQ) [12]. Reports on the influence of ethylene on stomatal and photosynthetic behavior are, however, contradictory. Ethylene decreased stomatal aperture in carnation, tomato and Arabidopsis [13], [14], increased stomatal conductance (Gs) in mustard [15], however it had no effect on Gs in Aglaonema [16]. Moreover, ethylene could also increased maximal quantum efficiency of PSII, net photosynthetic rate (Pn) and Rubisco activity in mustard [17]. There has been very little research on the role of ethylene in stomatal and photosynthetic regulation in other crops, especially in fruit trees.
Ethylene responsive factor (ERF) genes encode plant-specific transcription factors which act downstream of ethylene perception [18]. ERFs are one of the largest transcription factor families, with diverse functions in plants. They are associated with plant developmental and growth processes, including seed germination, root initiation, leaf emergence, floral development, fruit ripening and organ senescence [19], [20]. Moreover, they are involved in a diverse range of responses, such as cold stress related Hv-CBF2A in barley [21], drought related TaERF3 in wheat [22], salt tolerance related OsERF922 in rice [23], pathogen Phytophthora sojae related GmERF5 in soybean [24], and hypoxia responses related DkERF9 and DkERF10 in persimmon [25]. However, many aspects of transcriptional regulation of perennial fruit trees by ERF genes remain to be explored.
Recently, a few ERF genes have been shown to promote chlorophyll degradation during senescence, such as CBF2 [26], AtERF4 and AtERF8 [27]. Chlorophyll is essential for light harvesting for photosynthesis. Previous results suggested that ERF may play a role in regulation of photosynthesis [26], [27]. However, the regulation of photosynthesis by ERFs has not been reported. Our previous study has identified an ethylene-inducible ERF, CitERF13 in citrus. Overexpression of CitERF13 resulted in chlorophyll degradation and accumulation of Pheide a and reactive oxygen species (ROS) [28]. Here, we carried out experiments to determine the impacts of over-expressing CitERF13 on photosynthesis and chlorophyll fluorescence parameters in citrus and tobacco leaves.
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Plant materials
Tobacco (Nicotiana tabacum) seeds were sown in a growth medium of peat, plant ash, vermiculite, and perlite (5:1:1:1, v/v/v/v) in a glasshouse. The growth conditions of plant materials were as follows: a CO2 concentration of 300 μl l−1 and a photosynthetic photon flux density (PPFD) of 300 μmol m−2 s−1 in 16 h of light/8 h dark condition at 25 °C.
Transient over-expression analysis in citrus and tobacco leaf
The CitERF13 gene was isolated as in our previous reports [28], [29], [30]. Full length CitERF13 was inserted into pGreen II 0029 62-SK vector (empty vector),
CitERF13 transient over-expression in tobacco leaves
In our previous experiments, transient over-expression of CitERF13 in tobacco led to a remarkable degradation of green color near the injection point within 5 days [28]. In order to verify the mechanism of degreening and study effects on photosynthesis, we transiently over-expressed CitERF13 in tobacco leaves with CitERF13 expression level of 21–56 folders than empty vector (Fig. S1). CitERF13 over-expression caused the modulation of photosynthetic performance in tobacco leaves, as shown by the
Discussion
Because of the known involvement of ethylene in chlorophyll degradation and CitERF13 in fruit degreening in citrus [28], it was logical to look at the possibility of ERFs regulating photosynthesis and chlorophyll fluorescence response in these tissues. Due to the shortage of stable transformation systems in perennial fruit, transient expression systems have been developed in fruit tree material, such as apple skin [40], persimmon leaves [25] and papaya leaves [41]. Here, using a transient
Conclusions
In conclusion, given that overexpression of CitERF13 inhibits photosynthesis and chlorophyll fluorescence in both citrus and tobacco leaves, it is likely that CitERF13 has a role in the down-regulation of photosynthesis observed during chlorophyll degradation or senescence. CitERF13 was showed direct regulation on chlorophyll degradation related genes [28], but regulation of CitERF13 on photosynthesis-related target promoters requires further investigation.
Acknowledgements
The authors would like to thank Prof. Donald Grierson (University of Nottingham, UK) for critical reading and revision of the manuscript. This research was supported by the National Key Research and Development Program (2016YFD0400100), the Program of International Science and Technology Cooperation (2011DFB31580), and the National Basic Research Program of China (2011CB100602).
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These authors contributed equally to this manuscript.