Coordination of Cyclic Electron Flow and Water–Water Cycle Facilitates Photoprotection under Fluctuating Light and Temperature Stress in the Epiphytic Orchid Dendrobium officinale

Abstract

Photosystem I (PSI) is the primary target of photoinhibition under fluctuating light (FL). Photosynthetic organisms employ alternative electron flows to protect PSI under FL. However, the understanding of the coordination of alternative electron flows under FL at temperature stresses is limited. To address this question, we measured the chlorophyll fluorescence, P700 redox state, and electrochromic shift signal in leaves of Dendrobium officinale exposed to FL at 42 °C, 25 °C, and 4 °C. Upon a sudden increase in illumination at 42 °C and 25 °C, the water–water cycle (WWC) consumed a significant fraction of the extra reducing power, and thus avoided an over-reduction of PSI. However, WWC was inactivated at 4 °C, leading to an over-reduction of PSI within the first seconds after light increased. Therefore, the role of WWC under FL is largely dependent on temperature conditions. After an abrupt increase in light intensity, cyclic electron flow (CEF) around PSI was stimulated at any temperature. Therefore, CEF and WWC showed different temperature responses under FL. Furthermore, the enhancement of CEF and WWC at 42 °C quickly generated a sufficient trans-thylakoid proton gradient (ΔpH). The inactivation of WWC at 4 °C was partially compensated for by an increased CEF activity. These findings indicate that CEF and WWC coordinate to protect PSI under FL at temperature stresses.

Changes in Light Energy Utilization in Photosystem II and Reactive Oxygen Species Generation in Potato Leaves by the Pinworm Tuta absoluta

“…The absorbed light energy (as photons) by the light-harvesting complexes (LHCs) is transferred to the reaction centers (RCs) where, through charge separation, the electrons flow from photosystem II (PSII) to photosystem I (PSI), resulting on the one hand in the generation of a proton gradient (ΔpH) that drives ATP synthesis and on the other hand in the reduction of NADP + by the electrons transferred [ 21 , 22 , 23 , 24 ]. However, under most biotic or abiotic stresses the absorbed light energy exceeds the level that can be used, resulting in an increased formation of reactive oxygen species (ROS), such as superoxide anion radical (O 2 • − ), hydrogen peroxide (H 2 O 2 ), and singlet oxygen ( 1 O 2 ) [ 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 ]. Singlet oxygen ( 1 O 2 ) is formed when unquenched singlet excited states of chlorophyll ( 1 Chl*) undergo intersystem crossing and the resulting triplets ( 3 Chl*) react with oxygen (O 2 ) [ 34 , 35 , 36 , 37 , 38 ].…”

“…•− ), hydrogen peroxide (H 2 O 2 ), and singlet oxygen ( 1 O 2 ) [25][26][27][28][29][30][31][32][33]. Singlet oxygen ( 1 O 2 ) is formed when unquenched singlet excited states of chlorophyll ( 1 Chl*) undergo intersystem crossing and the resulting triplets ( 3 Chl*) react with oxygen (O 2 ) [34][35][36][37][38].…”

Regulation of Leaf Angle Protects Photosystem I under Fluctuating Light in Tobacco Young Leaves

“…In the other regulatory mechanism (acceptor-side regulation of PSI), the electron sink downstream of PSI consumes the excess electrons and thus alleviates PSI overreduction. This regulation involves CO 2 assimilation [ 61 , 63 ] and photorespiration (data not shown), the operation of O 2 photoreduction mediated by flavodiiron proteins [ 30 , 31 , 34 , 64 ] and the water–water cycle [ 11 , 54 , 65 ]. Flavodiiron proteins do not exist in angiosperms [ 28 ], and transient PSI overreduction indicates that the activity of the water–water cycle in tobacco is negligible [ 54 ].…”

Leaf Age-Dependent Photosystem II Photochemistry and Oxidative Stress Responses to Drought Stress in Arabidopsis thaliana Are Modulated by Flavonoid Accumulation

“…Under most environmental stresses, the absorbed light energy exceeds what it can be used, resulting in ROS generation, such as superoxide anion radical (O 2 • − ), hydrogen peroxide (H 2 O 2 ) and 1 O 2 [ 38 , 41 , 61 , 62 , 63 , 64 , 65 , 66 ]. When ROS production is not counterbalanced by the antioxidant defense network, photo-oxidative stress occurs [ 24 , 41 , 61 , 62 ].…”

“…•− ), hydrogen peroxide (H 2 O 2 ) and 1 O 2 [38,41,[61][62][63][64][65][66]. When ROS production is not counterbalanced by the antioxidant defense network, photo-oxidative stress occurs [24,41,61,62].…”