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

Hu Sun,Shi-Bao Zhang,Qi Shi,Wei Huang

doi:10.3390/plants10030606

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.

Highlights

Photosynthetic organisms usually experience dynamic fluctuations of light intensity under natural field conditions [1]
We first examined the changes in redox kinetics of the Photosystem I (PSI) primary electron donor (P700) upon transition from dark to actinic light (AL; 1,455 μmol photons m−2 s−1) at 42 ◦C, 25 ◦C, and 4 ◦C (Figure 1)
We first examined the changes in redox kinetics of the PSI primary electron d3oonfo1r5 (P700) upon transition from dark to actinic light (AL; 1,455 μmol photons m−2 s−1) at 42 °C, 25 °C, and 4 °C (Figure 1)

Summary

Introduction

Photosynthetic organisms usually experience dynamic fluctuations of light intensity under natural field conditions [1]. During fluctuating light (FL), a sudden increase in light intensity leads to a rapid increase in electron flow from photosystem II (PSII) to PSI [2]. The excited states in PSI cannot be immediately consumed by the dark reactions because CO2 fixation has a much slower kinetics [3], generating the imbalance between electron supply and nicotinamide adenine dinucleotide phosphate (NADPH) consumption [4]. Once PSI is damaged, the CO2 assimilation rate significantly decreases, impairing plant growth [8,9,10,11,12,13,14]. Plants have evolved several effective mechanisms to protect PSI against photo-oxidative damage under FL [15,16,17]. Two alternative electron flows, cyclic electron flow (CEF) around PSI and water–water cycle (WWC), have the potential to fine-tune the redox state of PSI under FL [6,18,19,20]

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