Contrasting Responses of Photosynthesis to Salt Stress in the Glycophyte Arabidopsis and the Halophyte Thellungiella: Role of the Plastid Terminal Oxidase as an Alternative Electron Sink

Abstract

The effects of short-term salt stress on gas exchange and the regulation of photosynthetic electron transport were examined in Arabidopsis (Arabidopsis thaliana) and its salt-tolerant close relative Thellungiella (Thellungiella halophila). Plants cultivated on soil were challenged for 2 weeks with NaCl. Arabidopsis showed a much higher sensitivity to salt than Thellungiella; while Arabidopsis plants were unable to survive exposure to greater than 150 mM salt, Thellugiella could tolerate concentrations as high as 500 mM with only minimal effects on gas exchange. Exposure of Arabidopsis to sublethal salt concentrations resulted in stomatal closure and inhibition of CO 2 fixation. This lead to an inhibition of electron transport though photosystem II (PSII), an increase in cyclic electron flow involving only PSI, and increased nonphotochemical quenching of chlorophyll fluorescence. In contrast, in Thellungiella, although gas exchange was marginally inhibited by high salt and PSI was unaffected, there was a large increase in electron flow involving PSII. This additional electron transport activity is oxygen dependent and sensitive to the alternative oxidase inhibitor n-propyl gallate. PSII electron transport in Thellungiella showed a reduced sensitivity to 2#-iodo-6-isopropyl-3-methyl-2#,4,4#-trinitrodiphenylether, an inhibitor of the cytochrome b 6 f complex. At the same time, we observed a substantial up-regulation of a protein reacting with antibodies raised against the plastid terminal oxidase. No such up-regulation was seen in Arabidopsis. We conclude that in salt-stressed Thellungiella, plastid terminal oxidase acts as an alternative electron sink, accounting for up to 30% of total PSII electron flow.

The integration of activity in saline environments: problems and perspectives

“…In some cases, such as wheat and barley under drought stress, photorespiration plays the major role in dissipation of excess energy (Noctor et al 2002), but this is not uniformly the case. In both A. thaliana and T. salsuginea, photorespiratory O 2 fixation was unaffected by salinity (Stepien and Johnson 2009). In A. thaliana, increased cyclic electron flow around PSI accompanied salinisation, whereas in T. salsuginea, electrons were dissipated instead by a plastid terminal oxidase (PTOX) (Stepien and Johnson 2009).…”

“…In both A. thaliana and T. salsuginea, photorespiratory O 2 fixation was unaffected by salinity (Stepien and Johnson 2009). In A. thaliana, increased cyclic electron flow around PSI accompanied salinisation, whereas in T. salsuginea, electrons were dissipated instead by a plastid terminal oxidase (PTOX) (Stepien and Johnson 2009).…”

“…on the light dependent and independent reactions (Chaves et al 2009(Chaves et al , 2011. Stepien and Johnson (2009) detailed many of these in a comparative study of Thellungiella salsuginea (halophila) growing successfully at salinities up to 500 mM NaCl and A. thaliana failing to thrive at 100 and 150 mM NaCl. Over a period of 2 weeks, both net assimilation and stomatal conductance declined in A. thaliana, but showed little if any change in T. salsuginea.…”

Plant Responses to Salt Stress: Adaptive Mechanisms

“…Depending on the ability of plants to grow in saline environments, they are classified as either glycophytes or euhalophytes, and their response to salt stress differs in terms of toxic ion uptake, ion compartmentation and/or exclusion, osmotic regulation, CO2 assimilation, photosynthetic electron transport, chlorophyll content and fluorescence, reactive oxygen species (ROS) generation, and antioxidant defences [11][12][13][14]. Most salinity adaptive mechanisms in plants are accompanied by certain morphological and anatomical changes [15].…”

Thylakoid Terminal Oxidases Are Essential for the CyanobacteriumSynechocystissp. PCC 6803 to Survive Rapidly Changing Light Intensities

“…High light, continuous illumination, and/or low temperature were all observed to increase the proportion of closed PSII reaction centers and, therefore, the excitation pressure in the mutant and led to impaired thylakoid membrane biogenesis (Rosso et al, 2009). In several plant species, up-regulation of PTOX has been observed in response to adverse conditions, such as exposure to high-light stress in low or elevated temperature environments (Streb et al, 2005) or under salt stress (Stepien and Johnson, 2009). Deletion of the PTOX2 gene in Chlamydomonas reinhardtii, encoding PTOX, confirmed a role in preventing overreduction of the plastoquinone pool in the light (Houille-Vernes et al, 2011).…”