RÉSUMÉ
Mangroves perform a crucial ecological role along the tropical and subtropical coastal intertidal zone where salinity fluctuation occurs frequently. However, the differential responses of mangrove plant at the combined transcriptome and metabolome level to variable salinity are not well documented. In this study, we used Avicennia marina (Forssk.) Vierh., a pioneer species of mangrove wetlands and one of the most salt-tolerant mangroves, to investigate the differential salt tolerance mechanisms under low and high salinity using inductively coupled plasma-mass spectrometry, transcriptomic and metabolomic analysis. The results showed that HAK8 was up-regulated and transported K+ into the roots under low salinity. However, under high salinity, AKT1 and NHX2 were strongly induced, which indicated the transport of K+ and Na+ compartmentalization to maintain ion homeostasis. In addition, A. marina tolerates low salinity by up-regulating ABA signaling pathway and accumulating more mannitol, unsaturated fatty acids, amino acids' and L-ascorbic acid in the roots. Under high salinity, A. marina undergoes a more drastic metabolic network rearrangement in the roots, such as more L-ascorbic acid and oxiglutatione were up-regulated, while carbohydrates, lipids and amino acids were down-regulated in the roots, and, finally, glycolysis and TCA cycle were promoted to provide more energy to improve salt tolerance. Our findings suggest that the major salt tolerance traits in A. marina can be attributed to complex regulatory and signaling mechanisms, and show significant differences between low and high salinity.
Sujet(s)
Avicennia , Métabolome , Racines de plante , Salinité , Tolérance au sel , Plantes tolérantes au sel , Transcriptome , Avicennia/génétique , Avicennia/physiologie , Avicennia/métabolisme , Plantes tolérantes au sel/génétique , Plantes tolérantes au sel/métabolisme , Plantes tolérantes au sel/physiologie , Racines de plante/métabolisme , Racines de plante/génétique , Tolérance au sel/génétique , Régulation de l'expression des gènes végétauxRÉSUMÉ
Salt secretion is an important strategy used by the mangrove plant Aegiceras corniculatum to adapt to the coastal intertidal environment. However, the structural, developmental and functional analyses on the leaf salt glands, particularly the salt secretion mechanism, are not well documented. In this study, we investigated the structural, developmental and degenerative characteristics and the salt secretion mechanisms of salt glands to further elucidate the mechanisms of salt tolerance of A. corniculatum. The results showed that the salt gland cells have a large number of mitochondria and vesicles, and plenty of plasmodesmata as well, while chloroplasts were found in the collecting cells. The salt glands developed early and began to differentiate at the leaf primordium stage. We observed and defined three stages of salt gland degradation for the first time in A. corniculatum, where the secretory cells gradually twisted and wrinkled inward and collapsed downward as the salt gland degeneration increased and the intensity of salt gland autofluorescence gradually diminished. In addition, we found that the salt secretion rate of the salt glands increased when the treated concentration of NaCl increased, reaching the maximum at 400 mM NaCl. The salt-secreting capacity of the salt glands of the adaxial epidermis is significantly greater than that of the abaxial epidermis. The real-time quantitative PCR results indicate that SAD2, TTG1, GL2 and RBR1 may be involved in regulating the development of the salt glands of A. corniculatum. Moreover, Na+/H+ antiporter, H+-ATPase, K+ channel and Cl- channel may play important roles in the salt secretion of salt glands. In sum mary, this study strengthens the understanding of the structural, developmental and degenerative patterns of salt glands and salt secretion mechanisms in mangrove recretohalophyte A. corniculatum, providing an important reference for further studies at the molecular level.
Sujet(s)
Primulaceae , Glande à sel , Environnement , Feuilles de plante/métabolisme , Primulaceae/physiologie , Chlorure de sodium/métabolismeRÉSUMÉ
MAIN CONCLUSION: Transcriptional and metabolic regulation of lignin biosynthesis and lignification plays crucial roles in Avicennia marina pneumatophore development, facilitating its adaptation to coastal habitats. Avicennia marina is a pioneer mangrove species in coastal wetland. To cope with the periodic intertidal flooding and hypoxia environment, this species has developed a complex and extensive root system, with its most unique feature being a pneumatophore with a distinct above- and below-ground morphology and vascular structure. However, the characteristics of pneumatophore lignification remain unknown. Studies comparing the anatomy among above-ground pneumatophore, below-ground pneumatophore, and feeding root have suggested that vascular structure development in the pneumatophore is more like the development of a stem than of a root. Metabolome and transcriptome analysis illustrated that the accumulation of syringyl (S) and guaiacyl (G) units in the pneumatophore plays a critical role in lignification of the stem-like structure. Fourteen differentially accumulated metabolites (DAMs) and 10 differentially expressed genes involved in the lignin biosynthesis pathway were targeted. To identify genes significantly associated with lignification, we analyzed the correlation between 14 genes and 8 metabolites and further built a co-expression network between 10 transcription factors (TFs), including 5 for each of MYB and NAC, and 23 enzyme-coding genes involved in lignin biosynthesis. 4-Coumarate-CoA ligase, shikimate/quinate hydroxycinnamoyl transferase, cinnamyl alcohol dehydrogenase, caffeic acid 3-O-methyltransferase, phenylalanine ammonia-lyase, and peroxidase were identified to be strongly correlated with these TFs. Finally, we examined 9 key candidate genes through quantitative real-time PCR to validate the reliability of transcriptome data. Together, our metabolome and transcriptome findings reveal that lignin biosynthesis and lignification regulate pneumatophore development in the mangrove species A. marina and facilitate its adaptation to coastal habitats.
Sujet(s)
Avicennia , Avicennia/génétique , Avicennia/métabolisme , Lignine/métabolisme , Reproductibilité des résultats , Analyse de profil d'expression de gènes , Transcriptome/génétique , MétabolomeRÉSUMÉ
Hydrogen sulfide (H2 S) is considered to mediate plant growth and development. However, whether H2 S regulates the adaptation of mangrove plant to intertidal flooding habitats is not well understood. In this study, sodium hydrosulfide (NaHS) was used as an H2 S donor to investigate the effect of H2 S 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 H2 S through increasing the expressions of the alternative oxidase genes and increasing the proportion of alternative respiratory pathway in the total mitochondrial respiration. Secondly, H2 S enhanced the capacity of the antioxidant system. Meanwhile, H2 S induced Ca2+ influx and activated the expression of intracellular Ca2+ -sensing-related genes. In addition, the alleviating effect of H2 S 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 H2 S in waterlogging adaptation in mangrove plants from the mitochondrial aspect.
Sujet(s)
Avicennia , Sulfure d'hydrogène , Sulfure d'hydrogène/pharmacologie , Sulfure d'hydrogène/métabolisme , Calcium/métabolisme , Avicennia/métabolisme , Espèces réactives de l'oxygène/métabolisme , Stress oxydatifRÉSUMÉ
NAC (NAM, ATAF1/2, CUC2) transcription factors (TFs) constitute a plant-specific gene family. It is reported that NAC TFs play important roles in plant growth and developmental processes and in response to biotic/abiotic stresses. Nevertheless, little information is known about the functional and evolutionary characteristics of NAC TFs in mangrove plants, a group of species adapting coastal intertidal habitats. Thus, we conducted a comprehensive investigation for NAC TFs in Avicennia marina, one pioneer species of mangrove plants. We totally identified 142 NAC TFs from the genome of A. marina. Combined with NAC proteins having been functionally characterized in other organisms, we built a phylogenetic tree to infer the function of NAC TFs in A. marina. Gene structure and motif sequence analyses suggest the sequence conservation and transcription regulatory regions-mediated functional diversity. Whole-genome duplication serves as the driver force to the evolution of NAC gene family. Moreover, two pairs of NAC genes were identified as positively selected genes of which AmNAC010/040 may be imposed on less constraint toward neofunctionalization. Quite a few stress/hormone-related responsive elements were found in promoter regions indicating potential response to various external factors. Transcriptome data revealed some NAC TFs were involved in pneumatophore and leaf salt gland development and response to salt, flooding and Cd stresses. Gene co-expression analysis found a few NAC TFs participates in the special biological processes concerned with adaptation to intertidal environment. In summary, this study provides detailed functional and evolutionary information about NAC gene family in mangrove plant A. marina and new perspective for adaptation to intertidal habitats.
Sujet(s)
Avicennia , Avicennia/composition chimique , Avicennia/génétique , Avicennia/métabolisme , Phylogenèse , Facteurs de transcription/métabolisme , Gènes de plante , ÉcosystèmeRÉSUMÉ
Avicennia marina, a mangrove plant growing in coastal wetland habitats, is frequently affected by tidal salinity. To understand its salinity tolerance, the seedlings of A. marina were treated with 0, 200, 400 and 600 mM NaCl. We found the whole-plant dry weight and photosynthetic parameters increased at 200 mM NaCl but decreased over 400 mM NaCl. The maximum quantum yield of primary photochemistry (Fv/Fm) significantly decreased at 600 mM NaCl. Transmission electron microscopy observations showed high salinity caused the reduction in starch grain size, swelling of the thylakoids and separation of the granal stacks, and even destruction of the envelope. In addition, the dense protoplasm and abundant mitochondria in the secretory and stalk cells, and abundant plasmodesmata between salt gland cells were observed in the salt glands of the adaxial epidermis. At all salinities, Na+ content was higher in leaves than in stems and roots; however, Na+ content increased in the roots while it remained at a constant level in the leaves over 400 mM NaCl treatment, due to salt secretion from the salt glands. As a result, salt crystals on the leaf adaxial surface increased with salinity. On the other hand, salt treatment increased Na+ and K+ efflux and decreased H+ efflux from the salt glands by the non-invasive micro-test technology, although Na+ efflux reached the maximum at 400 mM NaCl. Further real-time quantitative PCR analysis indicated that the expression of Na+/H+ antiporter (SOS1 and NHX1), H+-ATPase (AHA1 and VHA-c1) and K+ channel (AKT1, HAK5 and GORK) were up-regulated, and only the only Na+ inward transporter (HKT1) was down-regulated in the salt glands enriched adaxial epidermis of the leaves under 400 mM NaCl treatment. In conclusion, salinity below 200 mM NaCl was beneficial to the growth of A. marina, and below 400 mM, the salt glands could excrete Na+ effectively, thus improving its salt tolerance.
Sujet(s)
Avicennia , Animaux , Tolérance au sel , Glande à sel/métabolisme , Sodium/métabolisme , Chlorure de sodium/pharmacologie , Chlorure de sodium/métabolisme , Homéostasie , Feuilles de plante/métabolisme , Racines de plante/métabolismeRÉSUMÉ
Hydrogen sulfide (H2S), is a crucial biological player in plants. Here, we primarily explored the interaction between sodium hydrosulfide (NaHS, a H2S donor) and the fluxes of Na+ and K+ from the salt glands of mangrove species Avicennia marina (Forsk.) Vierh. with non-invasive micro-test technology (NMT) and quantitative real-time PCR (qRT-PCR) approaches under salinity treatments. The results showed that under 400-mM NaCl treatment, the addition of 200-µM NaHS markedly increased the quantity of salt crystals in the adaxial epidermis of A. marina leaves, accompanied by an increase in the K+/Na+ ratio. Meanwhile, the endogenous content of H2S was dramatically elevated in this process. The NMT result revealed that the Na+ efflux was increased from salt glands, whereas K+ efflux was decreased with NaHS application. On the contrary, the effects of NaHS were reversed by H2S scavenger hypotaurine (HT), and DL-propargylglycine (PAG), an inhibitor of cystathionine-γ-lyase (CES, a H2S synthase). Moreover, enzymic assay revealed that NaHS increased the activities of plasma membrane and tonoplast H+-ATPase. qRT-PCR analysis revealed that NaHS significantly increased the genes transcript levels of tonoplast Na+/H+ antiporter (NHX1), plasma membrane Na+/H+ antiporter (SOS1), plasma membrane H+-ATPase (AHA1) and tonoplast H+-ATPase subunit c (VHA-c1), while suppressed above-mentioned gene expressions by the application of HT and PAG. Overall, H2S promotes Na+ secretion from the salt glands of A. marina by up-regulating the plasma membrane and tonoplast Na+/H+ antiporter and H+-ATPase.