Summary
Ligand‐receptor pairs play important roles in cell–cell communication for multicellular organisms in response to environmental cues. Recently, the emergence of single‐cell RNA‐sequencing ...(scRNA‐seq) provides unprecedented opportunities to investigate cellular communication based on ligand‐receptor expression. However, so far, no reliable ligand‐receptor interaction database is available for plant species. In this study, we developed PlantPhoneDB (https://jasonxu.shinyapps.io/PlantPhoneDB/), a pan‐plant database comprising a large number of high‐confidence ligand‐receptor pairs manually curated from seven resources. Also, we developed a PlantPhoneDB R package, which not only provided optional four scoring approaches that calculate interaction scores of ligand‐receptor pairs between cell types but also provided visualization functions to present analysis results. At the PlantPhoneDB web interface, the processed datasets and results can be searched, browsed, and downloaded. To uncover novel cell–cell communication events in plants, we applied the PlantPhoneDB R package on GSE121619 dataset to infer significant cell–cell interactions of heat‐shocked root cells in Arabidopsis thaliana. As a result, the PlantPhoneDB predicted the actively communicating AT1G28290‐AT2G14890 ligand‐receptor pair in atrichoblast–cortex cell pair in Arabidopsis thaliana. Importantly, the downstream target genes of this ligand‐receptor pair were significantly enriched in the ribosome pathway, which facilitated plants adapting to environmental changes. In conclusion, PlantPhoneDB provided researchers with integrated resources to infer cell–cell communication from scRNA‐seq datasets.
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BFBNIB, DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
Aquaporins (AQPs) play important roles in plant growth, development and tolerance to environmental stresses. To understand the role of AQPs in the mangrove plant Kandelia obovata, which has the ...ability to acquire water from seawater, we identified 34 AQPs in the K. obovata genome and analysed their structural features. Phylogenetic analysis revealed that KoAQPs are homologous to AQPs of Populus and Arabidopsis, which are evolutionarily conserved. The key amino acid residues were used to assess water‐transport ability. Analysis of cis‐acting elements in the promoters indicated that KoAQPs may be stress‐ and hormone‐responsive. Subcellular localization of KoAQPs in yeast showed most KoAQPs function in the membrane system. That transgenic yeast with increased cell volume showed that some KoAQPs have significant water‐transport activity, and the substrate sensitivity assay indicates that some KoAQPs can transport H2O2. The transcriptome data were used to analyze the expression patterns of KoAQPs in different tissues and developing fruits of K. obovata. In addition, real‐time quantitative PCR analyses combined transcriptome data showed that KoAQPs have complex responses to environmental factors, including salinity, flooding and cold. Collectively, the transport of water and solutes by KoAQPs contributed to the adaptation of K. obovata to the coastal intertidal environment.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Aquaporins (AQPs) regulate the transport of water and other substrates, aiding plants in adapting to stressful environments. However, the knowledge of AQPs in salt‐secreting and viviparous Avicennia ...marina is limited. In this study, 46 AmAQPs were identified in A. marina genome, and their subcellular localisation and function in transporting H2O2 and boron were assessed through bioinformatics analysis and yeast transformation. Through analysing their expression patterns via RNAseq and real‐time quantitative polymerase chain reaction, we found that most AmAQPs were downregulated in response to salt and tidal flooding. AmPIP (1;1, 1;7, 2;8, 2;9) and AmTIP (1;5, 1;6) as salt‐tolerant candidate genes may contribute to salt secretion together with Na+/H+ antiporters. AmPIP2;1 and AmTIP1;5 were upregulated during tidal flooding and may be regulated by anaerobic‐responsive element and ethylene‐responsive element cis‐elements, aiding in adaptation to tidal inundation. Additionally, we found that the loss of the seed desiccation and dormancy‐related TIP3 gene, and the loss of the seed dormancy regulator DOG1 gene, or DOG1 protein lack heme‐binding capacity, may be genetic factors contributing to vivipary. Our findings shed light on the role of AQPs in A. marina adaptation to intertidal environments and their relevance to salt secretion and vivipary.
Summary statement
AmAQPs respond to salinity and tidal inundation in Avicennia marina, some of which play a role in salt gland secretion and function as water effluxes. The absence of TIP3, an aquaporin isoform, and the loss of DOG1, or its ability to bind to heme, may be one of the causes of vivipary in mangrove plants.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Theory and experiments support that plant invasions largely impact aboveground biodiversity and function. Yet, much less is known on the influence of plant invasions on the structure and function of ...the soil microbiome of coastal wetlands, one of the largest major reservoirs of biodiversity and carbon on Earth. We studied the continental‐scale invasion of Spartina alterniflora across 2451 km of Chinese coastlines as our model‐system and found that S. alterniflora invasion can largely influence the soil microbiome (across six depths from 0 to 100 cm), compared with the most common microhabitat found before invasion (mudflats, Mud). In detail, S. alterniflora invasion was not only positively associated with bacterial richness but also resulted in important biotic homogenization of bacterial communities, suggesting that plant invasion can lead to important continental scale trade‐offs in the soil microbiome. We found that plant invasion changed the community composition of soil bacterial communities across the soil profile. Moreover, the bacterial communities associated with S. alterniflora invasions where less responsive to climatic changes than those in native Mud microhabitats, suggesting that these new microbial communities might become more dominant under climate change. Plant invasion also resulted in important reductions in the complexity and stability of microbial networks, decoupling the associations between microbes and carbon pools. Taken together, our results indicated that plant invasions can largely influence the microbiome of coastal wetlands at the scale of China, representing the first continental‐scale example on how plant invasions can reshuffle the soil microbiome, with consequences for the myriad of functions that they support.
The continental‐scale invasion of Spartina alterniflora across China’s coastline was used as our model‐system to study the impact of plant invasions on the soil microbiome of blue carbon ecosystems. Plant invasion led to important trade‐offs in the soil microbiome by promoting bacterial richness, while resulting in biotic homogenization of bacterial communities. Plant invasion was further associated with an important reduction in the complexity and stability of microbial networks, and resulted in an important decoupling between soil microbes and carbon pools.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Aegiceras corniculatum is a major mangrove plant species adapted to waterlogging and saline conditions, grows in the coastal intertidal zone of tropical and subtropical regions. Here, we present a ...chromosome‐level genome assembly of A. corniculatum by incorporating PacBio long‐read sequencing and Hi‐C technology. The results showed that the PacBio draft genome size is 906.63 Mb. Hi‐C scaffolding anchored 885.06 Mb contigs (97.62% of draft assembly) onto 24 pseudochromosomes. The contig N50 and scaffold N50 were 7.1 Mb and 37.74 Mb, respectively. Out of 40,727 protein‐coding genes predicted in the study, 89% have functional annotations in public databases. We also showed that of the 603.93 Mb repetitive sequences predicted in the assembled genome, long terminal repeat retrotransposons constitute 41.52%. The genome evolution analysis showed that the A. corniculatum genome experienced two whole‐genome duplication events and shared the ancient γ whole‐genome triplication event. A comparative genomic analysis revealed an incidence of expansion in 1,488 gene families associated with essential metabolism and biosynthetic pathways, including photosynthesis, oxidative phosphorylation, phenylalanine, glyoxylate, dicarboxylate metabolism, and DNA replication, which probably constitute adaptation traits that allow the A. corniculatum to survive in the intertidal zone. Also, the systematic characterization of genes associated with flavonoid biosynthesis pathway and the AcNHX gene family conducted in this study will provide insight into the adaptation mechanism of A. corniculatum to intertidal environments. The high‐quality genome reported here can provide historical insights into genomic transformations that support the survival of A. corniculatum under harsh intertidal habitats.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
•A. ilicifolius migrated to the intertidal habitats at 16.89 Mya.•Unique unigenes drives adaptation of A. ilicifolius to environment.•Positive selection of genes promotes A. ilicifolius growth in the ...intertidal habitats.
Acanthus is a unique genus covering both mangroves and terrestrial species, and thus is an ideal system to comparatively analyze the mechanisms of mangrove adaptation to intertidal habitats. We performed RNA sequencing of the mangrove plant Acanthus ilicifolius and its two terrestrial relatives, Acanthus leucostachyus and Acanthus mollis. A total of 91,125, 118,290, and 141,640 unigenes were obtained. Simple sequence repeats (SSR) analysis showed that A. ilicifolius had more SSRs, the highest frequency of distribution, and higher in polymorphism potential compared to the two terrestrial relatives. Phylogenetic analyses suggested a relatively recent split between A. ilicifolius and A. leucostachyus, i.e., about 16.76 million years ago (Mya), after their ancestor divergence with A. mollis (32.11 Mya), indicating that speciation of three Acanthus species occurred in the Early to Middle Miocene. Gene Ontology (GO) enrichment revealed that the unique unigenes in A. ilicifolius are predominantly related to rhythmic process, reproductive process and response to stimuli. The accelerated evolution and positive selection analyses indicated that the genus Acanthus migrated from terrestrial to intertidal habitats, where 311 pairs may be under positive selection. Functional enrichment analysis revealed that these genes associated with essential metabolism and biosynthetic pathways such as oxidative phosphorylation, plant hormone signal transduction, photosynthetic carbon fixation and arginine and proline metabolism, are related to the adaptation of A. ilicifolius to intertidal habitats, which are characterized by high salinity and hypoxia. Our results indicate the evolutionary processes and the mechanisms underlying the adaptability of Acanthus to various harsh environments from the arid terrestrial to intertidal habitats.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Brassinosteroid (BR) has been shown to modulate plant tolerance to various stresses. S‐nitrosoglutathione reductase (GSNOR) is involved in the plant response to environment stress by fine‐turning the ...level of nitric oxide (NO). However, whether GSNOR is involved in BR‐regulated Na+/K+ homeostasis to improve the salt tolerance in halophyte is unknown. Here, we firstly reported that high salinity increases the expression of BR‐biosynthesis genes and the endogenous levels of BR in mangrove Kandelia obovata. Then, salt‐induced BR triggers the activities and gene expressions of GSNOR and antioxidant enzymes, thereafter decrease the levels of malondialdehyde, hydrogen peroxide. Subsequently, BR‐mediated GSNOR negatively regulates NO contributions to the reduction of reactive oxygen species generation and induction of the gene expression related to Na+ and K+ transport, leading to the decrease of Na+/K+ ratio in the roots of K. obovata. Finally, the applications of exogenous BR, NO scavenger, BR biosynthetic inhibitor and GSNOR inhibitor further confirm the function of BR. Taken together, our result provides insight into the mechanism of BR in the response of mangrove K. obovata to high salinity via GSNOR and NO signaling pathway by reducing oxidative damage and modulating Na+/K+ homeostasis.
Summary Statement
Salinity increases brassinosteroid (BR)‐biosynthesis genes expression and endogenous BR in mangrove Kandelia obovata.
BR enhances the activity and gene expression of S‐nitrosoglutathione reductase that negatively regulates nitric oxide signaling and reactive oxygen species level, while, BR regulates antioxidant enzymes and Na+/K+ homeostasis.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
SUMMARY
Salicylic acid (SA) is known to enhance salt tolerance in plants. However, the mechanism of SA‐mediated response to high salinity in halophyte remains unclear. Using electrophysiological and ...molecular biological methods, we investigated the role of SA in response to high salinity in mangrove species, Kandelia obovata, a typical halophyte. Exposure of K. obovata roots to high salinity resulted in a rapid increase in endogenous SA produced by phenylalanine ammonia lyase pathway. The application of exogenous SA improved the salt tolerance of K. obovata, which depended on the NADPH oxidase‐mediated H2O2. Exogenous SA and H2O2 increased Na+ efflux and reduced K+ loss by regulating the transcription levels of Na+ and K+ transport‐related genes, thus reducing the Na+/K+ ratio in the salt‐treated K. obovata roots. In addition, exogenous SA‐enhanced antioxidant enzyme activity and its transcripts, and the expressions of four genes related to AsA‐GSH cycle as well, then alleviated oxidative damages in the salt‐treated K. obovata roots. However, the above effects of SA could be reversed by diphenyleneiodonium chloride (the NADPH oxidase inhibitor) and paclobutrazol (a SA biosynthesis inhibitor). Collectively, our results demonstrated that SA‐induced salt tolerance of K. obovata depends on NADPH oxidase‐generated H2O2 that affects Na+/K+ and redox homeostasis in response to high salinity.
Significance Statement
Our study further clarified the role of salicylic acid (SA) in the networks of salt tolerance in mangrove plants. The results are of great scientific significance in complementing the mechanism of SA in salt tolerance of halophyte.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Hydrogen sulfide (H2S) is considered to mediate plant growth and development. However, whether H2S regulates the adaptation of mangrove plant to intertidal flooding habitats is not well understood. ...In this study, sodium hydrosulfide (NaHS) was used as an H2S donor to investigate the effect of H2S on the responses of mangrove plant Avicennia marina to waterlogging. The results showed that 24‐h waterlogging increased reactive oxygen species (ROS) and cell death in roots. Excessive mitochondrial ROS accumulation is highly oxidative and leads to mitochondrial structural and functional damage. However, the application of NaHS counteracted the oxidative damage caused by waterlogging. The mitochondrial ROS production was reduced by H2S through increasing the expressions of the alternative oxidase genes and increasing the proportion of alternative respiratory pathway in the total mitochondrial respiration. Secondly, H2S enhanced the capacity of the antioxidant system. Meanwhile, H2S induced Ca2+ influx and activated the expression of intracellular Ca2+‐sensing‐related genes. In addition, the alleviating effect of H2S on waterlogging can be reversed by Ca2+ chelator and Ca2+ channel blockers. In conclusion, this study provides the first evidence to explain the role of H2S in waterlogging adaptation in mangrove plants from the mitochondrial aspect.
Summary statement
H2S reduces mitochondrial ROS production by increasing the expressions of the alternative oxidase gene (AOX) and increases the proportion of alternative respiratory pathway in the total respiration, while H2S alleviates the mitochondrial structural damages including loss of bilayer membranes and blurring of mitochondrial cristae, and functional damages such as decrease of mitochondrial membrane potential (ΔΨm), membrane permeability transition pores opening, Cyt c release and the blockage of electron transfer along the mitochondrial electron transport chain caused by waterlogging‐induced oxidative stress. Secondly, H2S enhances the capacity of the antioxidant system through upregulating the expression of SOD, CAT, and APX genes to scavenge excess ROS. Last, H2S induces Ca2+ influx in the roots under waterlogging. Our results provide the better understanding of the role of H2S in adaptation of mangrove plants to the coastal intertidal environment from the mitochondrial aspect.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Acanthus is a distinctive genus that covers three species with different ecological niches including Acanthus mollis (arid terrestrial), Acanthus leucostachyus (damp forest) and Acanthus ilicifolius ...(coastal intertidal). It is an intriguing question how these species evolved from terrestrial to coastal intertidal. In the present study, we assembled chloroplast genomes of A. ilicifolius, A. leucostachyus and A. mollis, which exhibited typical quadripartite structures. The sizes were 150,758, 154,686 and 150,339 bp that comprised a large single copy (LSC, 82,963, 86,461 and 82,612 bp), a small single copy (SSC, 17,191, 17,511 and 17,019 bp), and a pair of inverted repeats (IRs, 25,302, 25,357 and 25,354 bp), respectively. Gene annotation revealed that A. ilicifolius, A. leucostachyus and A. mollis contained 113, 112 and 108 unique genes, each of which contained 79, 79 and 74 protein-coding genes, 30, 29 and 30 tRNAs, and 4 rRNA genes, respectively. Differential gene analysis revealed plenty of ndhs gene deletions in the terrestrial plant A. mollis. Nucleotide diversity analysis showed that the psbK, ycf1, ndhG, and rpl22 have the highest nucleotide variability. Compared to A. leucostachyus and A. mollis, seven genes in A. ilicifolius underwent positive selection. Among them, the atpF gene showed a strong positive selection throughout terrestrial to marine evolution and was important for adaptation to coastal intertidal habitats. Phylogenetic analysis indicated that A. ilicifolius has a closer genetic relationship with A. leucostachyus than A. mollis which further confirmed the evolutionary direction of Acanthus going from terrestrial to coastal intertidal zones.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
