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Low temperatures largely determine the geographic limits of plant species by reducing survival and growth. Inter-specific differences in the geographic distribution of mangrove species have been associated with cold tolerance, with exclusively tropical species being highly cold-sensitive and subtropical species being relatively cold-tolerant. To identify species-specific adaptations to low temperatures, we compared the chilling stress response of two widespread Indo-West Pacific mangrove species from Rhizophoraceae with differing latitudinal range limits-Bruguiera gymnorhiza (L.) Lam. ex Savigny (subtropical range limit) and Rhizophora apiculata Blume (tropical range limit). For both species, we measured the maximum photochemical efficiency of photosystem II (Fv/Fm) as a proxy for the physiological condition of the plants and examined gene expression profiles during chilling at 15 and 5 °C. At 15 °C, B. gymnorhiza maintained a significantly higher Fv/Fm than R. apiculata. However, at 5 °C, both species displayed equivalent Fv/Fm values. Thus, species-specific differences in chilling tolerance were only found at 15 °C, and both species were sensitive to chilling at 5 °C. At 15 °C, B. gymnorhiza downregulated genes related to the light reactions of photosynthesis and upregulated a gene involved in cyclic electron flow regulation, whereas R. apiculata downregulated more RuBisCo-related genes. At 5 °C, both species repressed genes related to CO2 assimilation. The downregulation of genes related to light absorption and upregulation of genes related to cyclic electron flow regulation are photoprotective mechanisms that likely contributed to the greater photosystem II photochemical efficiency of B. gymnorhiza at 15 °C. The results of this study provide evidence that the distributional range limits and potentially the expansion rates of plant species are associated with differences in the regulation of photosynthesis and photoprotective mechanisms under low temperatures., (© The Author(s) 2024. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com.)

The process of plastids developing into chloroplasts is critical for plants to survive. However, this process in woody plants is less understood. Kandelia obovata Sheue, Liu & Yong is a viviparous mangrove species; the seeds germinate on the maternal tree, and the hypocotyls continue to develop into mature propagules. We identified rare albino propagules through field observation among normal green and brown ones. Toward unveiling the propagule plastid development mechanism, albino propagule leaves only have etioplasts, low photosynthesis rates, and drastically reduced chlorophyll a/b and carotenoid contents, but with increased superoxide dismutase activities. To identify candidate genes controlling propagule plastid development, a genome-wide association study (GWAS) was performed between the albino and green propagules. Twenty-five significant single nucleotide polymorphisms (SNPs) were associated with albino propagule plastid development, the most significant SNPs being located on chromosomes 1 and 5. Significant differentially expressed genes were identified in porphyrin and chlorophyll metabolisms, carotenoid and flavonoid biosynthesis by combining transcriptome and GWAS data. In particular, KoDELLAs, encoding a transcription factor and KoCHS, encoding chalcone synthase, may be essential to regulate the albino propagules plastid development through weakened chlorophyll and flavonoid biosynthesis pathways while promoting chlorophyll degradation. Our results provide insights into genetic mechanisms regulating propagule plastid development in woody plants., (© The Author(s) 2022. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com.)

To explore the adaptation mechanisms of Kandelia candel (L.) Druce in response to daily flooding, a large-scale quantitative lysine acetylome was carried out using immunoaffinity enrichment of Lys-acetylated peptides and liquid chromatography linked to tandem mass spectrometry. A total of 1041 lysine acetylation (LysAc) sites, 1021 Lys-acetylated peptides and 617 Lys-acetylated proteins were identified. Six conserved sequence motifs of the LysAc sites, including a new motif KxxxxK, were detected. Among these proteins, 260 were differentially acetylated in response to flooding, which were preferentially predicted to participate in carbon metabolism and photosynthesis pathways based on KEGG pathway category enrichment analysis. Consistently, the transcriptional level of acetyltransferase and the consumption of acetyl-CoA were up-regulated under flooding conditions. Most of physiological parameters and mRNA expression levels related to carbon metabolism and photosynthesis were found to be insignificantly affected by flooding. Taken together, reversible protein LysAc is likely to be a post-translational mechanism contributing to the mangrove K. candel's adaptation to daily flooding.

Using 3-month-old seedlings of Bruguiera gymnorrhiza (L.) Savigny and Kandelia candel (L.) Druce, we compared species differences in ionic homeostasis control between the two non-secretor mangrove species. A high salinity (400 mM NaCl, 4 weeks) resulted in a decline of the K(+)/Na(+) ratio in root and leaf tissues, and the reduction was more pronounced in K. candel (41-66%) as compared with B. gymnorrhiza (5-36%). Salt-altered flux profiles of Na(+), K(+), H(+) and Ca(2+) in roots and effects of exogenous hydrogen peroxide (H(2)O(2)), nitric oxide (NO) and Ca(2+) on root ion fluxes were examined in seedlings that were hydroponically treated short term with 100 mM NaCl (ST, 24 h) and long term with 200 mM NaCl (LT, 7 days). Short term and LT salinity resulted in Na(+) efflux and a correspondingly increased H(+) influx in roots of both species, although a more pronounced effect was observed in B. gymnorrhiza. The salt-enhanced exchange of Na(+) with H(+) was obviously inhibited by amiloride (a Na(+)/H(+) antiporter inhibitor) or sodium orthovanadate (a plasma membrane H(+)-ATPase inhibitor), indicating that the Na(+) efflux resulted from active Na(+) exclusion across the plasma membrane. Short term and LT salinity accelerated K(+) efflux in the two species, but K. candel exhibited a higher flux rate. The salt-induced K(+) efflux was markedly restricted by the K(+) channel blocker, tetraethylammonium chloride, indicating that the K(+) efflux is mediated by depolarization-activated channels, e.g., KORCs (outward rectifying K(+) channels) and NSCCs (non-selective cation channels). Exogenous H(2)O(2) application (10 mM) markedly increased the apparent Na(+) efflux and limited K(+) efflux in ST-treated roots, although H(2)O(2) caused a higher Na(+) efflux in B. gymnorrhiza roots. CaCl(2) (10 mM) reduced the efflux of K(+) in salinized roots of the two mangroves, but its enhancement of Na(+) efflux was found only in B. gymnorrhiza. Under ST treatment, sodium nitroprusside (SNP) (100 ∝M, an NO donor) increased Na(+) efflux at the root apex of the two species; however, its inhibition of K(+) loss was seen only in K. candel. Of note, NaCl caused an obvious influx of Ca(2+) in B. gymnorrhiza roots, which was enhanced by H(2)O(2) (10 mM). Therefore, the salt-induced Ca(2+) benefits B. gymnorrhiza in maintaining K(+)/Na(+) homeostasis under high external salinity.

Salinity is a major abiotic stress that is responsible for growth reduction in most higher plants. Bruguiera gymnorrhiza (L.) Lam., a mangrove plant, is a halophyte and is one of the most salt-tolerant plant species. Physiological and proteomic characteristics of B. gymnorrhiza were investigated under three NaCl concentrations (0, 200 and 500 mM) in this study. Maximum seedling growth occurred at 200 mM NaCl. Leaf osmotic potential was more negative as salt levels increased further. Physiological results revealed that inorganic ions (especially Na(+) and Cl(-)) played a key role in osmotic adjustment of B. gymnorrhiza leaves under salinity treatments. Comparative proteomic analysis revealed 23 salt-responsive proteins in B. gymnorrhiza leaves, which were differentially expressed under salt treatment compared with control. Ten protein spots were analyzed by liquid chromatography-tandem mass spectrometry, leading to identification of proteins involved in photosynthesis, antioxidation, protein folding, cell organization and metabolism. Salt-responsive mechanism was different between 200 and 500 mM NaCl-treated plants on the basis of the physiological and proteomic analyses. Salt tolerance under 200 mM NaCl treatment was due to effective osmotic adjustment, accumulation of inorganic ions (especially Na(+) and Cl(-)) as well as increased expression of photosynthesis-related proteins and antioxidant enzymes, which improved the salt tolerance of B. gymnorrhiza, and furthermore promoted plant growth. On the other hand, 500 mM NaCl reduced the growth of B. gymnorrhiza, which appears to have been caused by the accumulation of NaCl (ionic effect) and energy consumption by organic solute synthesis. Moreover, the repressed expression of photosynthesis-related proteins and antioxidant enzymes led to the reduction of growth. Protein folding and degradation-related proteins and cell organization-related protein were up-regulated and played important roles in salt tolerance of B. gymnorrhiza under severe salt stress.

Root anatomy, radial oxygen loss (ROL), and tolerances to ferrous (Fe(2+)), sulphide (S(2-)), and zinc (Zn(2+)) ions were investigated in seedlings of eight species of mangrove, including three pioneer species, three rhizophoraceous and two landward semi-mangrove species. The results showed an interesting co-tolerance to Fe(2+), S(2-), and Zn(2+). The three rhizophoraceous species (Bruguiera gymnorrhiza, Kandelia obovata and Rhizophora stylosa), which possessed the thickest lignified exodermis and the 'tightest barrier' in ROL spatial pattern, consistently exhibited the highest tolerance to Fe(2+), S(2-), and Zn(2+). B. gymnorrhiza could directly reduce ROL by increasing lignification within the exodermis. Such an induced barrier to ROL is a probable defence response to prevent further invasion and spread of toxins within plants. The data also indicated that, in B. gymnorrhiza, Fe(2+) or S(2-), or both, induced a lignified exodermis that delayed the entry of Zn(2+) into the roots and thereby contributed to a higher tolerance to Zn(2+). This study provides new evidence of exclusive strategies of mangrove seedling roots in dealing with contaminations. The information is also important in the selection and cultivation of tolerant species for the bioremediation of contaminated waters or soils.

Rhizophora mangle L. trees of Biscayne National Park (Florida, USA) have two distinct growth forms: tall trees (5-10 m) growing along the coast and dwarf trees (1 m or less) growing in the adjacent inland zone. Sharp decreases in salinity and thus increases in soil water potential from surface soil to about a depth of 1 m were found at the dwarf mangrove site but not at the tall mangrove site. Consistent with our prediction, hydraulic redistribution detected by reverse sap flow in shallow prop roots was observed during nighttime, early morning and late afternoon in dwarf trees, but not in tall trees. In addition, hydraulic redistribution was observed throughout the 24-h period during a low temperature spell. Dwarf trees had significantly lower sapwood-specific hydraulic conductivity, smaller stem vessel diameter, lower leaf area to sapwood area ratio (LA/SA), smaller leaf size and higher leaf mass per area. Leaves of dwarf trees had lower CO(2) assimilation rate and lower stomatal conductance compared to tall trees. Leaf water potentials at midday were more negative in tall trees that are consistent with their substantially higher stomatal conductance and LA/SA. The substantially lower water transport efficiency and the more conservative water use of dwarf trees may be due to a combination of factors such as high salinity in the surface soil, particularly during dry periods, and substantial reverse sap flow in shallow roots that make upper soil layers with high salinity a competing sink of water to the transpiring leaves. There may also be a benefit for the dwarf trees in having hydraulic redistribution because the reverse flow and the release of water to upper soil layers should lead to dilution of the high salinity in the rhizosphere and thus relieve its potential harm to dwarf R. mangle trees.

To identify key proteins in the regulation of salt tolerance in the mangrove plant Bruguiera gymnorhiza, proteome analysis of samples grown under conditions of salt stress was performed. Comparative two-dimensional electrophoresis revealed that two, three and one protein were differentially expressed in the main root, lateral root and leaf, respectively, in response to salt stress. Among these, three proteins were identified by internal peptide sequence analysis: fructose-1,6-bisphosphate (FBP) aldolase and a novel protein in the main root, and osmotin in the lateral root. These results suggest that FBP aldolase and osmotin play roles in salt tolerance mechanisms common to both glycophytes and mangrove plants. Osmotin was abundant at early time points following salt treatment and seems to play a role in initial osmotic adaptation in lateral roots of B. gymnorhiza under salt stress, but does not contribute towards adaptation to prolonged or continuous exposure to salt stress. The amounts of these proteins were not correlated with those of the respective mRNAs, as determined by microarray analysis. A novel salt-responsive protein, not previously detected by expressed sequence tag analysis or transcriptome analysis, was also identified in this proteomic approach, and may provide insight into the salt tolerance mechanism of the mangrove plant. This is the first report of proteome analysis with detailed analysis of main and lateral roots of mangrove plants under salt stress conditions.

Root respiration uses a significant proportion of photosynthetically fixed carbon (C) and is a globally important source of C liberated from soils. Mangroves, which are an important and productive forest resource in many tropical and subtropical countries, sustain a high ratio of root to shoot biomass which may indicate that root respiration is a particularly important component in mangrove forest carbon budgets. Mangroves are often exposed to nutrient pollution from coastal waters. Here we assessed the magnitude of fine root respiration in mangrove forests in Belize and investigated how root respiration is influenced by nutrient additions. Respiration rates of excised fine roots of the mangrove, Rhizophora mangle L., were low (4.01 +/- 0.16 nmol CO(2) g(-1) s(-1)) compared to those measured in temperate tree species at similar temperatures. In an experiment where trees where fertilized with nitrogen (N) or phosphorus (P) in low productivity dwarf forests (1-2 m height) and more productive, taller (4- 7 m height) seaward fringing forests, respiration of fine roots did not vary consistently with fertilization treatments or with forest stature. Fine roots of taller fringe trees had higher concentrations of both N and P compared to dwarf trees. Fertilization with P enhanced fine root P concentrations in both dwarf and fringe trees, but reduced root N concentrations compared to controls. Fertilization with N had no effect on root N or P concentrations. Unlike photosynthetic C gain and growth, which is strongly limited by P availability in dwarf forests at this site, fine root respiration (expressed on a mass basis) was variable, but showed no significant enhancements with nutrient additions. Variation in fine root production and standing biomass are, therefore, likely to be more important factors determining C efflux from mangrove sediments than variations in fine root respiration per unit mass.

We determined how different hydroperiods affected leaf gas exchange characteristics of greenhouse-grown seedlings (2002) and saplings (2003) of the mangrove species Avicennia germinans (L.) Stearn., Laguncularia racemosa (L.) Gaertn. f., and Rhizophora mangle L. Hydroperiod treatments included no flooding (unflooded), intermittent flooding (intermittent), and permanent flooding (flooded). Plants in the intermittent treatment were measured under both flooded and drained states and compared separately. In the greenhouse study, plants of all species maintained different leaf areas in the contrasting hydroperiods during both years. Assimilation-light response curves indicated that the different hydroperiods had little effect on leaf gas exchange characteristics in either seedlings or saplings. However, short-term intermittent flooding for between 6 and 22 days caused a 20% reduction in maximum leaf-level carbon assimilation rate, a 51% lower light requirement to attain 50% of maximum assimilation, and a 38% higher demand from dark respiration. Although interspecific differences were evident for nearly all measured parameters in both years, there was little consistency in ranking of the interspecific responses. Species by hydroperiod interactions were significant only for sapling leaf area. In a field study, R. mangle saplings along the Shark River in the Everglades National Park either demonstrated no significant effect or slight enhancement of carbon assimilation and water-use efficiency while flooded. We obtained little evidence that contrasting hydroperiods affect leaf gas exchange characteristics of mangrove seedlings or saplings over long time intervals; however, intermittent flooding may cause short-term depressions in leaf gas exchange. The resilience of mangrove systems to flooding, as demonstrated in the permanently flooded treatments, will likely promote photosynthetic and morphological adjustment to slight hydroperiod shifts in many settings.

While H2O2 has been implicated in numerous plant environmental responses, normal levels and variabilities are poorly established, and estimates of leaf tissue concentrations span more than three orders of magnitude, even in a single species under similar conditions. Here, leaf tissue H2O2 contents under natural conditions are reported after determining (i) that H2O2 in extracts was stable with time, (ii) that H2O2 added to the extract was recovered quantitatively, and (iii) that the H2O2 calibration curve was unaffected (or quantifiably affected) by the extract. The broad applicability of the protocol and variability in leaf concentrations were demonstrated using tissue collected from several habitats in association with three, more extensive, experiments. The first involved nychthemeral studies of the mangrove, Rhizophora mangle L. Lowest H2O2 levels occurred in the early morning and near sunset, with higher levels both at midday and at night. Second, using five temperate species in Spring, concentrations were compared on a warm, sunny day and a cool, cloudy day. Higher concentrations were found on the warm day for Aesculus glabra Willd., Glechoma hederacea L., Plantago major L., and Viola soraria Willd., while there were no differences in Quercus macrocarpa Michx. Finally, the effects of elevated CO2 and ozone were examined in soybean, Glycine max L. Pioneer 93B15 under Free Air gas Concentration Enrichment (FACE) conditions. Both supplements led to elevated H2O2. Overall, mean leaf, midday, and mid-summer H2O2 concentrations ranged from 0.67 micromol (gFW)(-1) in mangrove to 3.6 micromol (gFW)(-1) in A. glabra Willd. Greatest within-species differences were only 2.5-fold in any of the studies.