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