ABSTRACT
Seagrass meadows play pivotal roles in coastal biochemical cycles, with nitrogen fixation being a well-established process associated with living seagrass. Here, we tested the hypothesis that nitrogen fixation is also associated with seagrass debris in Danish coastal waters. We conducted a 52-day in situ experiment to investigate nitrogen fixation (proxied by acetylene reduction) and dynamics of the microbial community (16S rRNA gene amplicon sequencing) and the nitrogen fixing community (nifH DNA/RNA amplicon sequencing) associated with decomposing Zostera marina leaves. The leaves harboured distinct microbial communities, including distinct nitrogen fixers, relative to the surrounding seawater and sediment throughout the experiment. Nitrogen fixation rates were measurable on most days, but highest on days 3 (dark, 334.8 nmol N g-1 dw h-1) and 15 (light, 194.6 nmol N g-1 dw h-1). Nitrogen fixation rates were not correlated with the concentration of inorganic nutrients in the surrounding seawater or with carbon:nitrogen ratios in the leaves. The composition of nitrogen fixers shifted from cyanobacterial Sphaerospermopsis to heterotrophic genera like Desulfopila over the decomposition period. On the days with highest fixation, nifH RNA gene transcripts were mainly accounted for by cyanobacteria, in particular by Sphaerospermopsis and an unknown taxon (order Nostocales), alongside Proteobacteria. Our study shows that seagrass debris in temperate coastal waters harbours substantial nitrogen fixation carried out by cyanobacteria and heterotrophic bacteria that are distinct relative to the surrounding seawater and sediments. This suggests that seagrass debris constitutes a selective environment where degradation is affected by the import of nitrogen via nitrogen fixation.
Subject(s)
Microbiota , Nitrogen Fixation , Plant Leaves , Seawater , Zosteraceae , Plant Leaves/microbiology , Seawater/microbiology , Seawater/chemistry , Zosteraceae/microbiology , Zosteraceae/metabolism , Nitrogen/metabolism , Nitrogen/analysis , RNA, Ribosomal, 16S/genetics , Bacteria/classification , Bacteria/genetics , Bacteria/metabolism , Bacteria/isolation & purification , Denmark , Cyanobacteria/metabolism , Cyanobacteria/genetics , Cyanobacteria/classification , Cyanobacteria/isolation & purificationABSTRACT
Microplastics are fast-emerging as another potential threat to already globally declining seagrass ecosystems, but there is a paucity of in situ surveys showing their accumulations. Here, we surveyed multiple Zostera marina L. meadows in 2020 and 2021 across Massachusetts, USA, for microplastic contamination, as well as identified factors related to patterns of accumulation. We found that microplastics were ubiquitous throughout all sites regardless of proximity to human development, with fibers being the most common microplastic type. In addition, we showed that accumulation of microplastics within seagrass meadows was related to epiphytic cover on leaves, plant morphology, and bulk-density in sediments. The results of this study provide the first in situ baseline microplastic concentrations on Z. marina plants and sediments for the temperate western North Atlantic. Additionally, we identify specific biotic and abiotic factors related to patterns of microplastic accumulation in these ecosystems.
Subject(s)
Environmental Monitoring , Microplastics , Water Pollutants, Chemical , Zosteraceae , Zosteraceae/metabolism , Massachusetts , Water Pollutants, Chemical/analysis , Microplastics/analysis , Geologic Sediments/chemistry , EcosystemABSTRACT
KEY MESSAGE: Multiple regulatory pathways of Zostera japonica to salt stress were identified through growth, physiological, transcriptomic and metabolomic analyses. Seagrasses are marine higher submerged plants that evolved from terrestrial monocotyledons and have fully adapted to the high saline seawater environment during the long evolutionary process. As one of the seagrasses growing in the intertidal zone, Zostera japonica not only has the ability to quickly adapt to short-term salt stress but can also survive at salinities ranging from the lower salinity of the Yellow River estuary to the higher salinity of the bay, making it a good natural model for studying the mechanism underlying the adaptation of plants to salt stress. In this work, we screened the growth, physiological, metabolomic, and transcriptomic changes of Z. japonica after a 5-day exposure to different salinities. We found that high salinity treatment impeded the growth of Z. japonica, hindered its photosynthesis, and elicited oxidative damage, while Z. japonica increased antioxidant enzyme activity. At the transcriptomic level, hypersaline stress greatly reduced the expression levels of photosynthesis-related genes while increasing the expression of genes associated with flavonoid biosynthesis. Meanwhile, the expression of candidate genes involved in ion transport and cell wall remodeling was dramatically changed under hypersaline stress. Moreover, transcription factors signaling pathways such as mitogen-activated protein kinase (MAPK) were also significantly influenced by salt stress. At the metabolomic level, Z. japonica displayed an accumulation of osmolytes and TCA mediators under hypersaline stress. In conclusion, our results revealed a complex regulatory mechanism in Z. japonica under salt stress, and the findings will provide important guidance for improving salt resistance in crops.
Subject(s)
Gene Expression Regulation, Plant , Metabolomics , Salt Stress , Signal Transduction , Zosteraceae , Zosteraceae/genetics , Zosteraceae/physiology , Zosteraceae/metabolism , Salt Stress/genetics , Signal Transduction/genetics , Salt Tolerance/genetics , Gene Expression Profiling , Transcriptome/genetics , Salinity , Photosynthesis/genetics , Photosynthesis/drug effects , Metabolome/geneticsABSTRACT
Zostera marina, a critical keystone marine angiosperm species in coastal seagrass meadows, possesses a photosensitive oxygen evolving complex (OEC). In harsh environments, the photoinactivation of the Z. marina OEC may lead to population declines. However, the factors underlying this photosensitivity remain unclear. Therefore, this study was undertaken to elucidate the elements contributing to Z. marina OEC photosensitivity. Our results demonstrated a gradual decrease in photosystem II performance towards shorter wavelengths, especially blue light and ultraviolet radiation. This phenomenon was characterized by a reduction in Fv/Fm and the rate of O2 evolution, as well as increased fluorescence at 0.3 ms on the OJIP curve. Furthermore, exposure to shorter light wavelengths and longer exposure durations significantly reduced the relative abundance of the OEC peripheral proteins, indicating OEC inactivation. Analyses of light-screening substances revealed that carotenoids, which increased most notably under 420 nm light, might primarily serve as thermal dissipators instead of efficient light filters. In contrast, anthocyanins reacted least to short-wavelength light, in terms of changes to both their content and the expression of genes related to their biosynthesis. Additionally, the levels of aromatically acylated anthocyanins remained consistent across blue-, white-, and red-light treatments. These findings suggest that OEC photoinactivation in Z. marina may be linked to inadequate protection against short-wavelength light, a consequence of insufficient synthesis and aromatic acylation modification of anthocyanins.
Subject(s)
Light , Oxygen , Photosystem II Protein Complex , Zosteraceae , Zosteraceae/metabolism , Photosystem II Protein Complex/metabolism , Oxygen/metabolism , Anthocyanins/metabolism , Carotenoids/metabolismABSTRACT
Eelgrass meadows have attracted much attention not only for their ability to maintain marine ecosystems as feeding grounds for marine organisms but also for their potential to store atmospheric and dissolved CO2 as blue carbon. This study comprehensively evaluated the bacterial and chemical data obtained from eelgrass sediments of different scales along the Japanese coast to investigate the effect on the acclimatization of eelgrass. Regardless of the eelgrass habitat, approximately 1% Anaerolineales, Babeliales, Cytophagales, and Phycisphaerales was present in the bottom sediment. Sulfate-reducing bacteria (SRB) were present at 3.69% in eelgrass sediment compared to 1.70% in bare sediment. Sulfur-oxidizing bacteria (SOB) were present at 2.81% and 1.10% in the eelgrass and bare sediment, respectively. Bacterial composition analysis and linear discriminant analysis revealed that SOB detoxified H2S in the eelgrass meadows and that the larger-scale eelgrass meadows had a higher diversity of SOB. Our result indicated that there were regional differences in the system that detoxifies H2S in eelgrass meadows, either microbial oxidation mediated by SOB or O2 permeation via the physical diffusion of benthos. However, since bacterial flora and phylogenetic analyses cannot show bias and/or causality due to PCR, future kinetic studies on microbial metabolism are expected.
Subject(s)
Geologic Sediments , Zosteraceae , Zosteraceae/microbiology , Zosteraceae/metabolism , Geologic Sediments/microbiology , Phylogeny , Bacteria/metabolism , Bacteria/classification , Hydrogen Sulfide/metabolism , Ecosystem , Oxidation-ReductionABSTRACT
Seagrass meadows act as filters for nitrogen in coastal areas, but whether they are a source or sink for N2O has been still controversy. Additionally, the production pathways of N2O as well as the microbial driving mechanism in seagrass meadows are seldom reported. In this study, the air-sea fluxes, sediment release potential, and production pathway of N2O in a temperate Zostera marina and Z. japonica mixed meadow were investigated by using gas chromatography and 15N isotopic tracing methods. The qPCR and metagenome sequencing were used to compare the difference in functional gene abundance and expression between seagrass vegetated and non-grass sediments. The results showed that the N2O air-sea fluxes in the meadow ranged from -1.97 to -1.77 nmol mâ»2 hâ»1, which was slightly lower in the seagrass region than in the adjacent bare region. Seagrass sediment N2O release potential dramatically increased after warming and nitrogen enrichment treatments. Heterotrophic nitrification was firstly investigated in seagrass meadows, and the process (26.80%-62.41%) and denitrification (37.55%-72.83%) contributed significantly to N2O production in the meadow, affected deeply by sediment organic content, while the contribution of autotrophic nitrification can be neglected. Compared with the bare sediments, the ammonia monooxygenase genes amoA, amoB and amoC, and nitrite oxidoreductase genes nxrA and nxrB, as well as nitrite reductase gene nirS and nitric oxide reductase gene norB were down-regulated, while the nitrous oxide reductase gene nosZ was up-regulated in the seagrass sediments, explaining less N2O emission in seagrass regions from the perspective of molecular. The nosZII-bearing bacteria like Bacteroidia, Polyangia, Anaerolineae, and Verrucomicrobiae could play important roles in N2O reduction in the seagrass meadow. The result is of great significance for highlighting the ability of seagrass meadows to mitigate climate changes.
Subject(s)
Nitrous Oxide , Zosteraceae , Zosteraceae/metabolism , Zosteraceae/genetics , Nitrous Oxide/metabolism , Nitrous Oxide/analysis , Environmental Monitoring , Geologic Sediments/microbiology , Denitrification , Nitrification , Air Pollutants/analysis , Nitrogen/metabolismABSTRACT
Frame Transplantation System (FTS) is considered an efficient method for seagrass restoration, but the effect of the rusting of iron frame on seagrass restoration remains unclear. We transplanted Zostera marina plants using iron FTS treated with fluorocarbon paint (painted treatment, PT) and traditional unpainted iron FTS (unpainted treatment, UT) under controlled mesocosm conditions for 24 days. Our results showed that the survival rate of Z. marina under the UT was significantly 31.2 % lower than that of the plants under the PT. Soluble sugar content in Z. marina rhizomes under the UT was significantly 2.19 times higher than that of the plants under the PT. Transcriptome analysis revealed differentially expressed genes (DEGs) involved in photosynthesis, metabolism and signal transduction functions. The results provide valuable data that could prove helpful in the development of efficient restoration techniques for Z. marina beds.
Subject(s)
Zosteraceae , Zosteraceae/metabolism , Gene Expression Profiling , Ecology , Plants , PhotosynthesisABSTRACT
Sulfide poisoning, hypoxia events, and reduced light availability pose threats to marine ecosystems such as seagrass meadows. These threats are projected to intensify globally, largely due to accelerating eutrophication of estuaries and coastal environments. Despite the urgency, our current comprehension of the metabolic pathways that underlie the deleterious effects of sulfide toxicity and hypoxia on seagrasses remains inadequate. To address this knowledge gap, I conducted metabolomic analyses to investigate the impact of sulfide poisoning under dark-hypoxia in vitro conditions on Zostera marina, a vital habitat-forming marine plant. During the initial 45 minutes of dark-hypoxia exposure, I detected an acclimation phase characterized by the activation of anaerobic metabolic pathways and specific biochemical routes that mitigated hypoxia and sulfide toxicity. These pathways served to offset energy imbalances, cytosolic acidosis, and sulfide toxicity. Notably, one such route facilitated the transformation of toxic sulfide into non-toxic organic sulfur compounds, including cysteine and glutathione. However, this sulfide tolerance mechanism exhibited exhaustion post the initial 45-minute acclimation phase. Consequently, after 60 minutes of continuous sulfide exposure, the sulfide toxicity began to inhibit the hypoxia-mitigating pathways, culminating in leaf senescence and tissue degradation. Utilizing metabolomic approaches, I elucidated the intricate metabolic responses of seagrasses to sulfide toxicity under in vitro dark-hypoxic conditions. My findings suggest that future increases in coastal eutrophication will compromise the resilience of seagrass ecosystems to hypoxia, primarily due to the exacerbating influence of sulfide.
Subject(s)
Ecosystem , Zosteraceae , Zosteraceae/metabolism , Environment , Sulfides/toxicity , Sulfides/metabolism , HypoxiaABSTRACT
Seagrasses, which are considered among the most ecologically valuable and endangered coastal ecosystems, have a narrowly limited distribution in the south-east Pacific, where Zostera chilensis is the only remaining relict. Due to water scarcity, desalination industry has grown in the last decades in the central-north coasts of Chile, which may be relevant to address in terms of potential impacts on benthic communities due to their associated high-salinity brine discharges to subtidal ecosystems. In this work, we assessed ecophysiological and cellular responses to desalination-extrapolable hypersalinity conditions on Z. chilensis. Mesocosms experiments were performed for 10 days, where plants were exposed to 3 different salinity treatments: 34 psu (control), 37 psu and 40 psu. Photosynthetic performance, H2O2 accumulation, and ascorbate content (reduced and oxidized) were measured, as well as relative gene expression of enzymes related to osmotic regulation and oxidative stress; these, at 1, 3, 6 and 10 days. Z. chilensis showed a decrease in photosynthetic parameters such as electron transport rate (ETRmax) and saturation irradiance (EkETR) under hypersalinity treatments, while non-photochemical quenching (NPQmax) presented an initial increment and a subsequent decline at 40 psu. H2O2 levels increased with hypersalinity, while ascorbate and dehydroascorbate only increased under 37 psu, although decreased along the experimental period. Increased salinities also triggered the expression of genes related to ion transport and osmolyte syntheses, but salinity-dependent up-regulated genes were mostly those related to the reactive oxygen species metabolism. The relict seagrass Z. chilensis has shown to withstand increased salinities that may be extrapolable to desalination effects in the short-term. As the latter is not fully clear in the long-term, and considering the restricted distribution and ecological importance, direct brine discharges to Z. chilensis meadows may not be recommended.
Subject(s)
Magnoliopsida , Zosteraceae , Ecosystem , Zosteraceae/metabolism , Chile , Magnoliopsida/metabolism , Hydrogen Peroxide/metabolism , Pacific Ocean , Ascorbic Acid , Risk Assessment , SalinityABSTRACT
Seagrasses are important marine ecosystem engineers but anthropogenic impacts and climate change have led to numerous population declines globally. In South Africa, Zostera capensis is endangered due to fragmented populations and heavy anthropogenic pressures on estuarine ecosystems that house the core of the populations. Addressing questions of how pressures such as climate change affect foundational species, including Z. capensis are crucial to supporting their conservation and underpin restoration efforts. Here we use ecological transcriptomics to study key functional responses of Z. capensis through quantification of gene expression after thermal stress and present the first reference transcriptome of Z. capensis. Four de novo reference assemblies (Trinity, IDBA-tran, RNAspades, SOAPdenovo) filtered through the EvidentialGene pipeline resulted in 153,755 transcripts with a BUSCO score of 66.1% for completeness. Differential expression analysis between heat stressed (32 °C for three days) and pre-warming plants identified genes involved in photosynthesis, oxidative stress, translation, metabolic and biosynthetic processes in the Z. capensis thermal stress response. This reference transcriptome is a significant contribution to the limited available genomic resources for Z. capensis and represents a vital tool for addressing questions around the species restoration and potential functional responses to warming marine environments.
Subject(s)
Zosteraceae , Zosteraceae/genetics , Zosteraceae/metabolism , Transcriptome , Ecosystem , Genomics , Climate ChangeABSTRACT
Seagrass beds are recognized as critical and among the most vulnerable habitats on the planet; seagrass colonize the coastal waters where heavy metal pollution is a serious problem. In this study, the toxic effects of copper and cadmium in the eelgrass Zostera marina L. were observed at the individual, subcellular, physiologically biochemical, and molecular levels. Both Cu and Cd stress significantly inhibited the growth and the maximal quantum yield of photosystem II (Fv/Fm); and high temperature increased the degree of heavy metal damage, while low temperatures inhibited damage. The half-effect concentration (EC50) of eelgrass was 28.9 µM for Cu and 2246.8 µM for Cd, indicating Cu was much more toxic to eelgrass than Cd. The effect of Cu and Cd on photosynthesis was synergistic. After 14 days of enrichment, the concentration of Cu in leaves and roots of Z. marina was 48 and 37 times higher than that in leaf sheath, and 14 and 11 times higher than that in rhizome; and the order of Cd concentration in the organs was root > leaf > rhizome > sheath. Heavy metal uptake mainly occurred in the organelles, and Cd enrichment also occurred to a certain extent in the cytoplasm. Transcriptome results showed that a number of photosynthesis-related KEGG enrichment pathways and GO terms were significantly down-regulated under Cd stress, suggesting that the photosynthetic system of eelgrass was severely damaged at the transcriptome level, which was consistent with the significant inhibition of Fv/Fm and leaf yellowing. Under Cu stress, the genes related to glutathione metabolic pathway were significantly up-regulated, together with the increased autioxidant enzyme activity of GSH-PX. In addition, the results of recovery experiment indicated that the damage caused by short-term Cd and Cu stress under EC50 was reversible. These results provide heavy metal toxic effects at multiple levels and information relating to the heavy metal resistance strategies evolved by Z. marina to absorb and isolate heavy metals, and highlight the phytoremediation potential of this species especially for Cd.
Subject(s)
Metals, Heavy , Zosteraceae , Cadmium/metabolism , Copper/metabolism , Metals, Heavy/metabolism , Metals, Heavy/toxicity , Photosynthesis , Zosteraceae/metabolismABSTRACT
Zostera marina, a widespread seagrass, evolved from a freshwater ancestor of terrestrial monocots and successfully transitioned into a completely submerged seagrass. We found that its oxygen-evolving complex (OEC) was partially inactivated in response to light exposure, as evidenced by both the increment of the relative variable fluorescence at the K-step and the downregulation of the OEC genes and proteins. This photosynthetic regulation was further addressed at both proteome and physiology levels by an in vivo study. The unchanged content of the ΔpH sensor PsbS protein and the non-photochemical quenching induction dynamics, described by a single exponential function, verified the absence of the fast qE component. Contents and activities of chlororespiration, Mehler reaction, malic acid synthesis, and photorespiration key enzymes were not upregulated, suggesting that alternative electron flows remained unactivated. Furthermore, neither significant production of singlet oxygen nor increment of total antioxidative capacity indicated that reactive oxygen species were not produced during light exposure. In summary, these low electron consumptions may allow Z. marina to efficiently use the limited electrons caused by partial OEC photoinactivation to maintain a normal carbon assimilation level.
Subject(s)
Photosynthesis , Zosteraceae/metabolism , Antioxidants/chemistry , Antioxidants/metabolism , Carbon/chemistry , Carbon/metabolism , Chlorophyll/chemistry , Electron Transport , Energy Metabolism , Light , Oxygen/metabolism , Photosynthesis/radiation effects , Photosystem II Protein Complex/metabolism , Plant Leaves/metabolism , Principal Component Analysis , Proteome/analysis , Singlet Oxygen/metabolismABSTRACT
Non-photochemical quenching (NPQ) of photosystem II (PSII) fluorescence is one of the most important protective mechanisms enabling the survival of phototropic organisms under high-light conditions. A low-efficiency NPQ, characterized by weak NPQ induction capacity and a low level of protective NPQ, was observed in the marine angiosperm Zostera marina, which inhabits the shallow water regions. Furthermore, chlorophyll fluorescence and Western blot analysis verified that the fast-inducted component of NPQ, i.e., the energy-dependent quenching (qE), was not present in this species. In contrast with the lack of PSII antenna quenching sites for qE induction in brown algae and the lack of functional XC in Ulvophyceae belonging to green algae, all the antenna proteins and the functional XC are present in Z. marina. A novel underlying mechanism was observed that the limited construction of the trans-thylakoid proton gradient (ΔpH) caused by photoinactivation of the oxygen evolving complex (OEC) did not induce protonation of PsbS, thus explaining the inability to form quenching sites for qE induction. Although the ΔpH established under light exposure activated violaxanthin (V) de-epoxidase enzyme to catalyze conversion of V via antheraxanthin (A) and then to zeaxanthin (Z), the quenching capacity of de-epoxidized pigment was weak in Z. marina. We suggest that the low-efficiency NPQ was conducive to efficiently utilize the limited electrons to perform photosynthesis, resisting the adverse effect of OEC photoinactivation on the photosynthetic rate.
Subject(s)
Adaptation, Ocular/physiology , Aquatic Organisms/metabolism , Chlorophyll/metabolism , Light-Harvesting Protein Complexes/metabolism , Oxygen/metabolism , Photosystem II Protein Complex/metabolism , Zosteraceae/metabolismABSTRACT
After HSP70 binds to the J domain of the substrate and co-chaperone protein, ATP is hydrolyzed to ADP, and the nucleotide exchange factors (NEFs) promote the release of ADP. Under physiological conditions, the nucleotide exchange step is the rate-limiting step, which is accelerated by NEFs. In this study, the promoter of nucleotide exchange factor ZjFes1 was cloned, and its expression in tissues and under heat stress was studied to understand the regulatory mechanism of ZjFes1 and provide the molecular basis to study heat tolerance mechanism of seagrass. It was found that the promoter has common cis-acting elements in promoter and enhancer regions CAAT-box, as well as light response elements AE-box, Box 4 and TCCC-motif, a cis-acting regulatory element essential for the anaerobic induction of ARE, hormone response elements CGTCA-motif and TGACG-motif (MeJA response element), GARE-motif (gibberellin response element), TGA-element (auxin response element), a cis-acting regulatory element related to meristem expression CAT-box, and a cis-acting element involved in defense and stress responsiveness of TC-rich repeats. Two-week-old seedlings exhibited weak GUS activities in their cotyledons. In addition, the AtFes1A promoter was constitutively active in the anthers. After exposure to 38 °C for 2 h, the root tips of two-week-old seedlings were stained a strong blue. Heat-inducible activities of GUS were also observed in the cotyledons, roots, leaves, anthers, sepals and siliques.
Subject(s)
Plant Proteins/genetics , Plant Proteins/metabolism , Zosteraceae/metabolism , Base Sequence , Cloning, Molecular , Gene Expression Regulation, Plant , Promoter Regions, Genetic , Response Elements , Zosteraceae/geneticsABSTRACT
Eutrophication leads to epiphyte blooms on seagrass leaves that strongly affect plant health, yet the actual mechanisms of such epiphyte-induced plant stress remain poorly understood. We used magnetic optical sensor nanoparticles in combination with luminescence lifetime imaging to map the O2 concentration and dynamics in the heterogeneous seagrass phyllosphere under changing light conditions. By incorporating magnetite into the sensor nanoparticles, it was possible to image the spatial O2 distribution under flow over seagrass leaf segments in the presence of a strong magnetic field. Local microniches with low leaf surface O2 concentrations were found under thick epiphytic biofilms, often leading to anoxic microhabitats in darkness. High irradiance led to O2 supersaturation across most of the seagrass phyllosphere, whereas leaf microenvironments with reduced O2 conditions were found under epiphytic biofilms at low irradiance, probably driven by self-shading. Horizontal micro-profiles extracted from the O2 images revealed pronounced heterogeneities in local O2 concentration over the base of the epiphytic biofilm, with up to 52% reduction in O2 concentrations in areas with relatively thick (>2 mm), compared with thin (≤1 mm), epiphyte layers in darkness. We also present evidence of enhanced relative internal O2 transport within leaves with epiphyte overgrowth, compared with bare seagrass leaves, in light as a result of limited mass transfer across thick outward diffusion pathways. The local availability of O2 was still markedly reduced in the epiphyte-covered leaves, however. The leaf phyllosphere is thus characterized by a complex microlandscape of O2 availability that strongly affects microbial processes occurring within the epiphytic biofilm, which may have implications for seagrass health, as anoxic microhabitats have been shown to promote the microbiological production of reduced toxic compounds, such as nitric oxide.
Subject(s)
Aquatic Organisms/metabolism , Hydrobiology , Magnetite Nanoparticles , Optical Devices , Oxygen/metabolism , Plant Leaves/metabolism , Eutrophication , Seaweed/metabolism , Zosteraceae/metabolismABSTRACT
As an alternative electron sink, chlororespiration, comprising the NAD(P)H dehydrogenase complex and plastid terminal plastoquinone oxidase, may play a significant role in sustaining the redox equilibrium between stroma and thylakoid membrane. This study identified a distinct role for chlororespiration in the marine angiosperm Zostera marina, whose oxygen-evolving complex (OEC) is prone to photo-inactivation as a result of its inherent susceptibility to excess irradiation. The strong connectivity between OEC peripheral proteins and key chlororespiratory enzymes, as demonstrated in the interaction network of differentially expressed genes, suggested that the recovery of photo-inactivated OEC was connected with chlororespiration. Chlorophyll fluorescence, transcriptome and Western blot data verified a new physiological role for chlororespiration to function as photoprotection and generate a proton gradient across the thylakoid membrane for the recovery of photo-inactivated OEC. Chlororespiration was only activated in darkness following excess irradiation exposure, which might be related to electron deficiency in the electron transport chain because of the continuous impairment of the OEC. The activation of chlororespiration in Z. marina was prone to proactivity, which was also supported by the further activation of the oxidative pentose-phosphate pathway synthesizing NADPH to meet the demand of chlororespiration during darkness. This phenomenon is distinct from the common assumption that chlororespiration is prone to consuming redundant reducing power during the short transition phase from light to dark.
Subject(s)
Light , Magnoliopsida/metabolism , Magnoliopsida/radiation effects , Electron Transport/radiation effects , Oxidation-Reduction , Oxygen , Photosynthesis/radiation effects , Photosystem II Protein Complex , Thylakoids/metabolism , Zosteraceae/metabolism , Zosteraceae/radiation effectsABSTRACT
Zostera marina, a fully submerged marine angiosperm with a unique evolutionary history associated with its terrestrial origin, has distinct photochemical characteristics caused by its oxygen-evolving complex (OEC) being prone to deactivation in visible light. Based on the present phylogenetic analysis, the chloroplast NADPH dehydrogenase-like (NDH) complex was found to be completed in of Z. marina, unlike other marine plants, suggesting its crucial role. Thus, the responses of electron transport to irradiation were investigated through multiple chlorophyll fluorescence techniques and Western blot analysis. Moreover, the respective contribution of the two photosystem I cyclic electron flow (PSI-CEF) pathways to the generation of trans-thylakoid proton gradient (∆pH) was also examined using inhibitors. The contributions of the two PSI-CEF pathways to ∆pH were similar; furthermore, there was a trade-off between the two pathways under excess irradiation: the PGR5/L1-dependent PSI-CEF decreased gradually following its activation during the initial illumination, while NDH-dependent PSI-CEF was activated gradually with exposure duration. OEC inactivation was continuously under excess irradiation, which exhibits a positive linear correlation with the activation of NDH-dependent PSI-CEF. We suggest that PGR5/L1-dependent PSI-CEF was preferentially activated to handle the excess electron caused by the operation of OEC during the initial illumination. Subsequently, the increasing OEC inactivation with exposure duration resulted in a deficit of electrons. Limited electrons from PSI might preferentially synthesize NADPH, which could support the function of NDH-dependent PSI-CEF to generate ∆pH and ATP via reducing ferredoxin, thereby maintaining OEC stability.
Subject(s)
Arabidopsis Proteins/metabolism , Magnoliopsida/metabolism , Photosystem I Protein Complex/metabolism , Photosystem II Protein Complex/metabolism , Plant Proteins/metabolism , Zosteraceae/metabolism , Arabidopsis Proteins/genetics , Electrons , Magnoliopsida/genetics , Photosystem I Protein Complex/genetics , Photosystem II Protein Complex/genetics , Plant Proteins/genetics , Zosteraceae/geneticsABSTRACT
Nucleotide exchange factors (NEFs) play an important role in plant abiotic stress response, but their characteristics and functions in seagrass have not been studied. Zostera japonica (Z. japonica) is one of the most widely distributed seagrass species in China and are distributed in subtropical and temperate coastal areas. Z. japonica is intertidal seagrass, which often undergoes heat stress during summer when the tide ebbs. Overexpression of ZjFes1 in Arabidopsis results in an increase in heat tolerance. We found that ZjFes1 associates with ZjHsp70 in vivo by yeast two-hybrid and bimolecular fluorescence complementarity (BiFC). Overexpression of ZjFes1 leads to selective reduction of Hsp70 transcription and an increase in Hsp101. In conclusion, our results suggest that ZjFes1 may be an active regulator of heat tolerance.
Subject(s)
Arabidopsis/metabolism , Plants, Genetically Modified/metabolism , Arabidopsis/genetics , HSP70 Heat-Shock Proteins/genetics , HSP70 Heat-Shock Proteins/metabolism , Heat-Shock Response , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically Modified/genetics , Transcription Factors/genetics , Transcription Factors/metabolism , Zosteraceae/genetics , Zosteraceae/metabolismABSTRACT
Through respiration and photosynthesis, seagrass meadows contribute greatly to carbon and oxygen fluxes in shallow coastal waters. There is increasing concern about how shallow-water primary producers will react to a near-future climate scenario with increased temperature variation. When modelling primary productivity under high temperature variability, Q10 values are commonly used to predict rate changes depending on biophysical factors. Q10 values are often assumed to be constant and around 2.0 (i.e. a doubling of the rate with a temperature increase of 10 °C). We aimed to establish how the gas exchange of seagrass (Zostera marina) tissues at various maturity stages would respond over a broad range of temperatures. Seagrass shoot maturity stage clearly affected respiration and apparent photosynthesis, and the Q10 results indicated a skewed balance between the two processes, with a higher photosynthetic Q10 during periods of elevated temperatures. When estimating whole-plant Q10 in a realistic maximal temperature range, we found that the overall response of a seagrass plant's net O2 exchange balance can be as much as three to four times higher than under ambient temperatures. Our findings indicate that plant tissue age and temperature should be considered when assessing and modelling carbon and oxygen fluctuations in vegetated coastal areas.
Subject(s)
Temperature , Zosteraceae/growth & development , Zosteraceae/metabolism , Analysis of Variance , Cell Respiration , Photosynthesis , Plant Leaves/metabolism , Plant Shoots/metabolismABSTRACT
Although seagrasses can incorporate heavy metals from the marine environment, few studies have been conducted on heavy metal uptake and phytoremediation potential by seagrass transplants in the heavy metal contaminated sediments. Zostera marina shoots were transplanted in two polluted bay systems on Korean coasts to evaluate the heavy metal contaminations in sediments and the possibility of using Z. marina transplants as a bioindicator and phytoremediation agent. The major concentrated metals in sediments were As, Cu, Fe, and Pb in Jaran Bay, and Cd, Co, Zn, and Hg in Onsan Bay. The Co, Zn, Pb, and Hg concentrations in Z. marina tissues reflected the sediment heavy metal concentrations, and thus the tissue heavy metal concentrations may be used as bio-indicators of the metal contaminations. Since Z. marina transplants accumulated a great amount of heavy metals in their tissues, they may have the phytoremediation potential for the heavy metal contaminated sediments.