Dynamics And Triggering Mechanisms Of Photoinactivation Of Oxygen-evolving Complex In Seagrasses

As a foundation species of coastal ecosystems,seagrasses provide important ecosystem services.However,seagrasses are facing a serious decline crisis in recent years,becoming one of the most threatened ecosystems on the planet.At this stage,the decline of seagrasses is mainly attributed to global climate change and habitat fragmentation,eutrophication,pollution,and biological invasion directly related to human activities,while less attention has been paid to the intrinsic biological vulnerability of seagrasses.Our previous studies found that the representative northern seagrass-Zostera marina oxygen-evolving complex（OEC）is prone to photoinactivation,clearly distinguishing it from terrestrial plants and seaweeds.Therefore,to gain a deeper understanding of the photoinactivation regularity and triggering factors of seagrass OEC and its intrinsic linkage with seagrass decline,this paper takes Phyllospadix iwatensis,a representative vulnerable seagrass in northern China,and Zostera marina with complete genome sequencing as the research objects,systematically investigated the photoinactivation dynamics and triggering mechanisms of OEC through laboratory simulation experiments and in situ measurements in the field,combined with physiological,transcriptomic,and metabolomic methods.The main results are as follows:1.Characteristics of OEC photoinactivationPhyllospadix iwatensis,a typical species of seagrass in a blue carbon ecosystem,has been recognized to be a vulnerable seagrass.Its degradation has previously been reported to be associated with environmental changes and human activities,while there has been a limited number of studies on its inherent characteristics.In this study,both the physiological and molecular biological data indicated that the OEC of P.iwatensis is prone to photoinactivation,which exhibits the light-dependent trait.When exposed to laboratory light intensities similar to typical midday conditions,<10%of the OEC was photoinactivated,and the remaining active OEC was sufficient to maintain normal photosynthetic activity.Moreover,the photoinactivated OEC could fully recover within the same day.However,under harsh light conditions,e.g.,light intensities that simulated cloudless sunny neap tide days and continual sunny days,the OEC suffered irreversible photoinactivation,which subsequently resulted in damage to the photosystem II reaction centers and a reduction in the rate of O₂evolution.Furthermore,in situ measurements on a cloudless sunny neap tide day revealed both poor resilience and irreversible photoinactivation of the OEC.Based on these findings,we postulated that the OEC dysfunction induced by ambient harsh light conditions could be an important inherent reason for the degradation of P.iwatensis.2.Triggering mechanism of OEC photoinactivationIn order to reveal the mechanism of OEC photoinactivation,the light screening function of seagrass was investigated in this paper.Zostera marina,a representative northern seagrass with complete genome sequencing,was selected as the research subject to explore the photosensitivity and inducement of OEC by examining the inactivation spectrum of OEC and the differences in photoresponse pathways following exposure to different spectrums.The OEC inactivation was spectral-dependent.High-energy light significantly reduced the PSII performance,OEC peripheral protein expression,and photosynthetic O₂release capacity.The increased synthesis of carotenoids under blue light with severe OEC damage implied its weak photoprotection property in Z.marina.However,anthocyanins key synthetic genes were lowly expressed with inefficient accumulation under high-energy light.Furthermore,targeted metabolome results showed that the acylation modifications of anthocyanins,especially aromatic acylation modifications were insufficient,leading to poor stability and light absorption of anthocyanins.Based on the role of blue light receptors in regulating the synthesis of anthocyanins in vascular plant,we hypothesized that the absence of blue light receptor CRY2 in Z.marina causes the insufficient synthesis of anthocyanins and acyl modifications,reducing the shielding against high-energy light,subsequently causing OEC photoinactivation.In summary,the following conclusions can be drawn:the absence of photoreceptor in seagrass led to the insufficient synthesis of anthocyanins and reduced the level of aromatic acylated modification of anthocyanins,which makes the high-energy light rich in marine ecosystems reach chloroplasts easily,leading to OEC inactivation;furthermore,the irreversible photoinactivation of OEC under harsh light conditions in the wild,can reduce the photosynthetic performance and even damage the photosynthetic apparatus,which will threaten the survival of seagrasses and may trigger the decline of seagrass populations in the long run.This study not only re-examines seagrass decline in terms of intrinsic biological vulnerability of seagrasses but also provides new ideas for the restoration of seagrass beds,i.e.to modify the photoreceptors of seagrasses through gene-editing techniques to provide healthy seagrass populations and improve the ability of seagrasses to cope with environmental changes,thus slowing down the decline of seagrass populations.The results bear significance for maintaining the sustainable use of resources in coastal seagrass beds ecosystems.