Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis

Abstract

The high mountain plant species Ranunculus glacialis has a low antioxidative scavenging capacity and a low activity of thermal dissipation of excess light energy despite its growth under conditions of frequent light and cold stress. In order to examine whether this species is protected from over-reduction by matching photosystem II (PSII) electron transport (ETR) and carbon assimilation, both were analysed simultaneously at various temperatures and light intensities using infrared gas absorption coupled with chlorophyll fluorescence. ETR exceeded electron consumption by carbon assimilation at higher light intensities and at all temperatures tested, necessitating alternative electron sinks. As photorespiration might consume the majority of excess electrons, photorespiration was inhibited by either high internal leaf CO 2 molar ratio (C i ), low oxygen partial pressure (0.5% oxygen), or both. At 0.5% oxygen ETR was significantly lower than at 21% oxygen. At 21% oxygen, however, ETR still exceeded carbon assimilation at high C i , suggesting that excess electrons are transferred to another oxygen consuming reaction when photorespiration is blocked. Nevertheless, photorespiration does contribute to electron consumption. While the activity of the waterwater cycle to electron consumption is not known in leaves of R. glacialis , indirect evidence such as the high sensitivity to oxidative stress and the low initial NADP-malate dehydrogenase (NADP-MDH) activity suggests only a minor contribution as an alternative electron sink. Alternatively, the plastid terminal oxidase (PTOX) may transfer excess electrons to oxygen. This enzyme is highly abundant in R. glacialis leaves and exceeds the PTOX content of every other plant species so far examined, including those of transgenic tomato leaves overexpressing the PTOX protein. Finally, PTOX contents strongly declined during deacclimation of R. glacialis plants, suggesting their important role in photoprotection. Ranunculus glacialis is the first reported plant species with such a high PTOX protein content.

Photosynthetic Redox Imbalance Governs Leaf Sectoring in theArabidopsis thalianaVariegation Mutantsimmutans,spotty,var1, andvar2

“…Furthermore, Stepien and Johnson (2009) reported that PTOX acts as an alternative electron sink in the salt-stressed halophyte Thellungiella. These effects were accompanied by a significant increase in the relative abundance of PTOX in R. glacialis (Streb et al, 2005) and Thellungiella but not in Arabidopsis (Stepien and Johnson, 2009). These data support the role of IM/PTOX as an alternative electron sink in alleviating overreduction of the PQ pool under unfavorable environmental conditions where PSI is limited on the acceptor side.…”

“…Consequently, excitation pressure should be sensitive to both irradiance and temperature (Dietz et al, 1985;Hü ner et al, 1998Hü ner et al, , 2003Wilson et al, 2006). Since IM is considered to be a plastid terminal oxidase capable of oxidizing the intersystem PQ pool (Joë t et al, 2002;Josse et al, 2003, Aluru andStreb et al, 2005;Stepien and Johnson, 2009), we examined the effects of either changes in measuring irradiance or measuring temperature on excitation pressure in im seedlings. The data in Figure 5A illustrate the light response curves for excitation pressure in fully expanded leaves of im seedlings grown at 25/50, which results in an all green phenotype.…”

“…Under stress conditions when the PET chain becomes overly reduced, IM may act as an alternative electron sink that, by consuming excess photosynthetically generated electrons, would minimize the formation of ROS (Niyogi, 2000). PTOX has been reported to reduce oxygen and was suggested to play an important photoprotective role in the high alpine plant species Ranunculus glacialis acclimated to low temperature (Streb et al, 2005). Furthermore, Stepien and Johnson (2009) reported that PTOX acts as an alternative electron sink in the salt-stressed halophyte Thellungiella.…”

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).…”

An original adaptation of photosynthesis in the marine green alga Ostreococcus

“…Later, it was established that oxygen reduction can take place either downstream of PSI [leading to the so-called ''Mehler reaction'' (24)] or between PSII and PSI. The latter reaction is driven by the plastoquinol terminal oxidase (PTOX) (25), an enzyme that catalyzes electron flow from reduced plastoquinol to O 2 during the so-called chlororespiratory process (reviewed in ref. 26).…”