Elsevier

Plant Science

Volume 303, February 2021, 110795
Plant Science

Research article
Photosystem I is tolerant to fluctuating light under moderate heat stress in two orchids Dendrobium officinale and Bletilla striata

https://doi.org/10.1016/j.plantsci.2020.110795Get rights and content

Highlights

  • We examine responses of PSI and PSII to FL at 42 °C in D. officinale and B. striata.

  • FL at 42 °C induces selective photoinhibition of PSII in these two orchids.

  • The water-water cycle protects PSI in FL at 42 °C in D. officinale.

  • Heat-induced PSII photoinhibition protects PSI in FL at 42 °C in B. striata.

  • WWC and PSII photoinhibition are important strategies to cope with FL at 42 °C.

Abstract

Under natural field conditions, plants usually experience fluctuating light (FL) under moderate heat stress in summer. However, responses of photosystems I and II (PSI and PSII) to such combined stresses are not well known. Furthermore, the role of water-water cycle (WWC) in photoprotection in FL under moderate heat stress is poorly understood. In this study, we examined chlorophyll fluorescence and P700 redox state in FL at 42 °C in two orchids, Dendrobium officinale (with high WWC activity) and Bletilla striata (with low WWC activity). After FL treatment at 42 °C, PSI activity maintained stable while PSII activity decreased significantly in these two orchids. In D. officinale, the WWC could rapidly consume the excess excitation energy in PSI and thus avoided an over-reduction of PSI upon any increase in illumination. Therefore, in D. officinale, WWC likely protected PSI in FL at 42 °C. In B. striata, heat-induced PSII photoinhibition down-regulated electron flow from PSII and thus prevented an over-reduction of PSI after transition from low to high light. Consequently, in B. striata moderate PSII photoinhibition could protected PSI in FL at 42 °C. We conclude that, in addition to cyclic electron flow, WWC and PSII photoinhibition-repair cycle are two important strategies for preventing PSI photoinhibition in FL under moderate heat stress.

Introduction

Under the circumstance of natural field, leaves are usually exposed to fluctuating light (FL) in daytime [[1], [2], [3]]. Upon a sudden increase in illumination, light absorption increases immediately. However, leaves cannot generate an enough trans-thylakoid proton gradient (ΔpH) to finely control electron flow at cytochrome (Cyt) b6/f [[4], [5], [6]]. The resulting excess electron flow from PSII to PSI induces the over-reduction of PSI, leading to the production of reactive oxygen species (ROS) within PSI. Because antioxidant enzymes cannot scavenge ROS immediately [7], FL can induce preferential photodamage to PSI, even in wild-type angiosperms [[8], [9], [10]]. In summer, leaves undergo FL associated with moderate heat stress in tropical and subtropical areas. Recent studies indicated that FL associated with moderate heat stress caused selective photoinhibition of PSI in tobacco [11,12]. However, photosynthetic responses to FL under moderate heat stress in other angiosperms are still poorly understood.

Due to the important roles of PSI in determining CO2 assimilation and photoprotection [[13], [14], [15]], plants have evolved several pathways to protect PSI against photoinhibition in FL. For instance, in nonflowering plants, flavodiiron proteins are the main player protecting PSI in FL [[16], [17], [18], [19], [20]]. In angiosperms, flavodiiron proteins are lost during evolution [21]. Alternatively, angiosperms use cyclic electron flow (CEF) around PSI to alleviate PSI photoinhibition [9,[22], [23], [24]]. In CEF mutants, ΔpH formation under high light is largely impaired [[25], [26], [27]], leading to the over-reduction of PSI and severe photoinhibition of PSI when exposed to high light [10,22,25,28]. When tobacco leaves were exposed to FL under moderate heat stress, the stimulation of CEF favored photoprotection for PSI [12]. Recently, some studies reported that water-water cycle (WWC) had a potential to protect PSI in FL [5,6,29]. Comparing with CEF, the activity of WWC is relatively species dependent [30,31]. Upon a sudden increase in irradiance, WWC rapidly consumed the excess excitation energy in PSI and thus prevented the over-reduction of PSI electron carriers in Camellia species [5,29]. In addition, down-regulation of PSII activity can rescue the lethal phenotype of pgr5 plant in FL [32]. In the shade-establishing plant Paris polyphylla, the relatively low PSII activity prevented PSI photoinhibition in FL [33]. These previous studies suggested that plants might use different strategies for protecting PSI against photoinhibition in FL.

Some recent studies also found that WWC was more effective in protecting PSI in FL at room temperature than CEF [5,6,29]. In angiosperms with low WWC activity, PSI was usually over-reduced within the first seconds after a sudden increase in light intensity. By comparison, in angiosperms with high WWC activity, the operation of WWC rapidly accepted electrons from PSI to O2, consuming a significant fraction of the extra excitation energy. Thus, WWC can avoid an over-reduction of PSI upon any increase in light intensity. Under moderate heat stress, an increased thylakoid proton conductivity decreased the ΔpH formation [12,34,35], which increased the risk of PSI over-reduction in FL. Owing to the low WWC activity, FL under moderate heat stress induced preferential photodamage to PSI and accelerated PSI photoinhibition in FL for tobacco young leaves (Tan et al. 2020a, b). However, whether WWC has the potential to protect PSI against photoinhibition in FL under moderate heat stress remains uncertain.

As we know, moderate heat stress can cause photoinhibition to PSI in heat-sensitive plants such as wheat [36,37]. In addition, heat stress induces damage to oxygen-evolving complex (OEC) and thus causes photoinhibition of PSII [[38], [39], [40], [41]]. Once PSII photoinhibition occurs, electron flow from PSII to PSI is depressed [28,42]. As a result, PSII photoinhibition protected PSI under high light in pgr5 mutant [28]. Although pgr5 mutant died at the seedling stage when grown under FL [22], the minimal PSII activity rescued the lethal phenotype of pgr5 in FL [32]. Therefore, PSII photoinhibition-repair cycle has the potential to protect PSI against photoinhibition in FL under moderate heat stress.

Dendrobium officinale and Bletilla striata are two orchids that are native to subtropical areas and can grow under high light. In summer, they usually experience FL under moderate heat stress. However, their photosynthetic responses to FL under moderate heat stress are little known. In this study, we measured chlorophyll fluorescence and P700 signal in FL at 42 °C. We found that FL at 42 °C caused selective photodamage to PSII in both species, which was large different from the phenotype of tobacco. In D. officinale, the high WWC activity avoided an over-reduction of PSI upon any increase in illumination and thus protected PSI against FL at 42 °C. By comparison, the heat-induced photoinhibition of PSII in B. striata decreased the electron flow from PSII and thus prevented PSI photoinhibition in FL at 42 °C. Therefore, in addition to CEF, WWC and PSII photoinhibition-repair cycle are two important strategies used by angiosperms to cope with FL under moderate heat stress.

Section snippets

Plant materials

In this study, we used two orchids Dendrobium officinale and Bletilla striata for experiments. Plants were cultivated in a greenhouse with 60 %–70 % relative air humidity and day/night temperatures of 30/19 °C. Non-woven shade was used to control light condition to be 40 % of full sunlight. In summer, the maximum irradiance at midday is approximately 1200 μmol photons m−2 s−1. No water or nutrition stress occurred during cultivation. The fully expanded leaves without senescence were used for

Redox kinetics of P700 upon dark-to-light transition at 42 °C

After dark adaptation for 60 min, the redox kinetics of P700 were measured at 42 °C during 15 s long illumination at a high light of 1455 μmol photons m−2 s−1. The results showed that D. officinale displayed a rapid P700 re-oxidation in 4 s (Fig. 1). However, such rapid re-oxidation of P700 was not observed in B. striata, similar to the phenotype of A. thaliana [21]. Recent studies have documented that this rapid re-oxidation of P700 was attributed to the photo-reduction of O2 [21,29,30].

FL under moderate heat stress causes preferential photodamage of PSII in D. Officinale and B. striata

Under natural field conditions, FL is a typical light stress in daytime, owing to changes in leaf angle, cloud cover, and canopy cover [1,2,50]. In nonflowering plants, the rapid photo-reduction of O2 mediated by flavodiiron proteins prevents an over-reduction of PSI upon any abrupt increase in light intensity, making PSI tolerant to FL in them [[16], [17], [18], [19], [20]]. However, flavodiiron proteins are not conserved in angiosperms [21,51]. Upon a sudden increase in illumination, the

Conclusions

In this study, we studied photosynthetic regulation in FL under moderate heat stress in two orchids D. officinale and B. striata. We found that PSI activity maintained stable but PSII activity significantly decreased after FL treatment at 42 °C in both species. Taking into consideration the phenotype of tobacco in FL at 42 °C, the effects of FL under moderate heat stress on PSI and PSII activities are species dependent. Upon a sudden increase in irradiance at 42 °C, both species showed highly

Declaration of Competing Interest

The authors have no conflicts of interest to declare.

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grant 31971412), the Key Research and Development Plan of Yunnan Province (2018BB010), Digitalization, Development and Application of Biotic Resource (202002AA100007) and Beijing DR PLANT Biotechnology Co., Ltd.

References (61)

  • H. Sun et al.

    The water-water cycle is more effective in regulating redox state of photosystem I under fluctuating light than cyclic electron transport

    Biochim. Biophys. Acta - Bioenerg.

    (2020)
  • M. Suorsa et al.

    PGR5-PGRL1-dependent cyclic electron transport modulates linear electron transport rate in Arabidopsis thaliana

    Mol. Plant

    (2016)
  • H. Sun et al.

    Decreased photosystem II activity facilitates acclimation to fluctuating light in the understory plant Paris polyphylla

    Biochim. Biophys. Acta - Bioenerg.

    (2020)
  • X. Wen et al.

    Heat stress induces an inhibition of excitation energy transfer from phycobilisomes to photosystem II but not to photosystem I in a cyanobacterium Spirulina platensis

    Plant Physiol. Biochem.

    (2005)
  • P. Li et al.

    Heterogeneous behavior of PSII in soybean (Glycine max) leaves with identical PSII photochemistry efficiency under different high temperature treatments

    J. Plant Physiol.

    (2009)
  • Y.-J. Yang et al.

    Stimulation of cyclic electron flow around photosystem I upon a sudden transition from low to high light in two angiosperms Arabidopsis thaliana and Bletilla striata

    Plant Sci.

    (2019)
  • W. Huang et al.

    In vivo regulation of proton motive force during photosynthetic induction

    Environ. Exp. Bot.

    (2018)
  • S.-L. Tan et al.

    Balancing light use efficiency and photoprotection in tobacco leaves grown at different light regimes

    Environ. Exp. Bot.

    (2020)
  • W. Huang et al.

    Responses of photosystem I compared with photosystem II to fluctuating light in the shade-establishing Tropical tree species psychotria henryi

    Front. Plant Sci.

    (2016)
  • M. Tikkanen et al.

    Integrative regulatory network of plant thylakoid energy transduction

    Trends Plant Sci.

    (2014)
  • T. Shikanai et al.

    Contribution of cyclic and pseudo-cyclic electron transport to the formation of proton motive force in chloroplasts

    Mol. Plant

    (2017)
  • Y.J. Yang et al.

    The water-water cycle facilitates photosynthetic regulation under fluctuating light in the epiphytic orchid Dendrobium officinale

    Environ. Exp. Bot.

    (2020)
  • H. Kimura et al.

    Improved stomatal opening enhances photosynthetic rate and biomass production in fluctuating light

    J. Exp. Bot.

    (2020)
  • W. Yamori et al.

    Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice

    Plant Cell Environ.

    (2020)
  • R.A. Slattery et al.

    The impacts of fluctuating light on crop performance

    Plant Physiol.

    (2018)
  • D. Takagi et al.

    Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition

    Plant Physiol.

    (2016)
  • M. Kono et al.

    Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana

    Plant Cell Physiol.

    (2014)
  • H. Yamamoto et al.

    PGR5-dependent cyclic electron flow protects photosystem I under fluctuating light at donor and acceptor sides

    Plant Physiol.

    (2019)
  • S.-L. Tan et al.

    Moderate heat stress accelerates photoinhibition of photosystem I under fluctuating light in tobacco young leaves

    Photosynth. Res.

    (2020)
  • M. Zivcak et al.

    Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves

    Photosynth. Res.

    (2015)
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