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ProCg12 is active in saline condition during infection by Frankia. Salt stress (50 mM NaCl) was first applied then C. glauca plants were inoculated separately with Frankia strains Ccl3 (A–D) and CeD (E,F). ProCg12 is activated in prenodules (A,B) and nodules (C–F) of control and NaCl treated C. glauca plants, 14 days after inoculation. (C–F) Sections of matures nodules expressing green fluorescent protein (GFP). White arrows indicate reporter gene expression. (C,E) Bright field microscopy. (A,B,D,F) Epifluorescence microscopy. Bars 100 μm.
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Symbiotic nitrogen-fixing associations between Casuarina trees and the actinobacteria Frankia are widely used in agroforestry in particular for salinized land reclamation. The aim of this study was to analyze the effects of salinity on the establishment of the actinorhizal symbiosis between C. glauca and two contrasting Frankia strains (salt sensit...
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Climate change and the accelerated rate of population growth are imposing a progressive degradation of natural ecosystems worldwide. In this context, the use of pioneer trees represents a powerful approach to reverse the situation. Among others, N2-fixing actinorhizal trees constitute important elements of plant communities and have been successful...
Actinorhizal plants form a symbiotic association with the nitrogen-fixing actinobacteria Frankia. These plants have important economic and ecological benefits including land reclamation, soil stabilization, and reforestation. Recently, many non-Frankia actinobacteria have been isolated from actinorhizal root nodules suggesting that they might contr...
Citations
... Actinorhizal plants are pioneers in poor soils such as saline-alkali lands and their exceptional adaptation to these environments is closely related to their symbiosis with Frankia 9 . High salinity affected the early deformation of root hairs and reduced nodule number and size in C. glauca and Casuarina equisetifolia 199 . However, how salt stress affects the formation of actinorhizal symbiosis and the strong salt tolerance of actinorhizal plants requires further study. ...
Plants associate with nitrogen-fixing bacteria to secure nitrogen, which is generally the most limiting nutrient for plant growth. Endosymbiotic nitrogen-fixing associations are widespread among diverse plant lineages, ranging from microalgae to angiosperms, and are primarily one of three types: cyanobacterial, actinorhizal or rhizobial. The large overlap in the signaling pathways and infection components of arbuscular mycorrhizal, actinorhizal and rhizobial symbioses reflects their evolutionary relatedness. These beneficial associations are influenced by environmental factors and other microorganisms in the rhizosphere. In this review, we summarize the diversity of nitrogen-fixing symbioses, key signal transduction pathways and colonization mechanisms relevant to such interactions, and compare and contrast these interactions with arbuscular mycorrhizal associations from an evolutionary standpoint. Additionally, we highlight recent studies on environmental factors regulating nitrogen-fixing symbioses to provide insights into the adaptation of symbiotic plants to complex environments.
... This association is popular for reclamation of degraded land, extenuate the adverse effects of various biotic and abiotic stresses, and for enhancing the survival and growth parameters of the plants. Frankia-Casuarina association is also popularly used for reclamation of salinized land (Ngom et al. 2016). Ghedira et al. (2018) presented the first high-throughput proteomic study of Frankia alni in water-related stress, by characterizing the polyethylene glycol (PEG)-responding desiccome. ...
... Nodulation activities and hence nitrogen fixation was enhanced on inoculation of Frankia in host plant. Ngom et al. (2016) recoded the effects of salinity on Casuarina glauca and two strains of Frankia, viz. saltsensitive Frankia Ccl3 and salt tolerant Frankia CeD. ...
Human activities, industrialization and civilization have deteriorated the environment which eventually has led to alarming effects on plants and animals by heightened amounts of chemical pollutants and heavy metals in the environment, which create abiotic stress. Environmental conditions like drought, salinity, diminished macro-and micro-nutrients also contribute in abiotic stress, resulting in decrement of survival and growth of plants. Presence of pathogenic and competitive microorganisms , as well as pests lead to biotic stress and a plant alone can not defend itself. Thankfully, nature has rendered plant's rhizosphere with plant growth promoting rhizobacteria which maintain an allelopathic relationship with host plant to defend the plant and let it flourish in abiotic as well as biotic stress situations. This review discusses the mechanisms behind increase in plant growth via various direct and indirect traits expressed by associated microorganisms in the rhizosphere, along with their current scenario and promising future for sustainable agriculture. It also gives details of ten such bacterial species, viz. Acetobacter, Agrobacterium, Alcaligenes, Arthrobacter, Azospirillum, Azotobacter, Bacillus, Burkholderia, Enterobacter and Frankia, whose association with the host plants is famed for enhancing plant's growth and survival.
... Extensive studies have been performed on the nitrogen-fixing root nodules of C. glauca (Abdel-Lateif et al., 2013) and C. cunninghamiana (He 4 et al., 2010), which are derived from a symbiotic relationship with the nitrogen-fixing actinomycete Frankia. Other research topics include the dissection of salt stress tolerance in C. equisetifolia (Ngom et al., 2016;Tani & Sasakawa, 2003). However, it is difficult to explore the molecular basis of these physiological responses without a reference genome. ...
Australian pine (Casuarina spp.) is extensively planted in tropical and subtropical regions for wood production, shelterbelts, environmental protection, and ecological restoration. To characterize Casuarina genomic diversity, we sequenced and constructed de novo genome assemblies of the three most widely planted species: C. equisetifolia, C. glauca, and C. cunninghamiana. We generated chromosome-scale genome sequences using both Pacific Biosciences (PacBio) Sequel sequencing and chromosome conformation capture technology (Hi-C). The total genome sizes for C. equisetifolia, C. glauca, and C. cunninghamiana are 268,942,579 bp, 296,631,783 bp, and 293,483,606 bp, respectively, of which 25.91%, 27.15%, and 27.74% were annotated as repetitive sequences. We annotated 23,162, 24,673, and 24,674 protein-coding genes in C. equisetifolia, C. glauca, and C. cunninghamiana, respectively. We then collected branchlets from male and female individuals for whole-genome bisulfite sequencing (BS-seq) to explore the epigenetic regulation of sex determination in these three species. Transcriptome sequencing (RNA-seq) revealed differential expression of phytohormone-related genes between male and female plants. In summary, this study generated three chromosome-level genome assemblies and comprehensive DNA methylation and transcriptome datasets from both male and female material for three Casuarina species, providing a basis for the comprehensive investigation of genomic diversity and functional gene discovery of Casuarina in the future.
... -salt stress alleviation, higher dry biomass, chlorophyll, and proline content [30] Methylobacterium sp. 2A ...
In the face of climate change, progressive degradation of the environment, including agricultural land negatively affecting plant growth and development, endangers plant productivity. Seeking efficient and sustainable agricultural techniques to replace agricultural chemicals is one of the most important challenges nowadays. The use of plant growth-promoting microorganisms is among the most promising approaches; however, molecular mechanisms underneath plant–microbe interactions are still poorly understood. In this review, we summarized the knowledge on plant–microbe interactions, highlighting the role of microbial and plant proteins and metabolites in the formation of symbiotic relationships. This review covers rhizosphere and phyllosphere microbiomes, the role of root exudates in plant–microorganism interactions, the functioning of the plant’s immune system during the plant–microorganism interactions. We also emphasized the possible role of the stringent response and the evolutionarily conserved mechanism during the established interaction between plants and microorganisms. As a case study, we discussed fungi belonging to the genus Trichoderma. Our review aims to summarize the existing knowledge about plant–microorganism interactions and to highlight molecular pathways that need further investigation.
... Plants that associate with mycorrhizal fungi can gain substantial amounts of phosphorus, promoting plant growth and expanding the ecological niche of the host species (Corrales et al. 2016;Gerz et al. 2018;Simard et al. 2012). In parallel, plants form root nodulating symbioses with bacteria that can provide host plants with a substantial portion of their nitrogen budget (Ngom et al. 2016;Regus et al. 2017a) also expanding the host species range (Simonsen et al. 2017). But the net fitness effect of these associations can vary from highly beneficial to harmful (Hoeksema et al. 2010;Sachs and Simms 2008;Sachs et al. 2018). ...
Purpose
Legumes form root nodules to gain fixed nitrogen from rhizobia and can also access nitrogen in soil. Data suggest that plants might discriminate among these sources to optimize growth, but recognition of symbiotically fixed nitrogen and its regulation remain poorly understood.
Methods
A greenhouse inoculation study manipulated the molecular form and concentration of nitrogen available using two Lotus japonicus genotypes and the nitrogen-fixing symbiont, Mesorhizobium loti. Plants were supplied with sole organic and inorganic nitrogen sources to simulate forms that plants might receive from symbiotic nitrogen fixation or from the soil. Host benefit from and regulation of symbiosis was investigated by quantifying symbiotic trait variation and isotopic analysis of nitrogen fixation.
Results
Host growth varied in response to fertilization with alanine, aspartic acid, ammonium, and nitrate, suggesting differences in catabolism efficiency. Net benefits of nodulation were reduced or eliminated under all forms of extrinsic fertilization. However, even when symbiosis imposed significant costs, hosts did not reduce investment into nodulation or nitrogen fixation when exposed to aspartic acid, unlike with other nitrogen sources.
Conclusions
L. japonicus can adaptively downregulate investment into symbiosis in the presence of some but not all nitrogen sources. Failure to downregulate any aspect of symbiosis in the presence of aspartic acid suggests that it might be jamming the main signal used by L. japonicus to detect nitrogen fixation.
... strain QA3 showed grow on naphthalene as a sole carbon source and an operon for aromatic compound degradation in addition to ring-hydroxylating dioxygenases upregulated under naphthalene stress [26]. Some Frankia strains show salt tolerance under salt-stressed conditions and can be used as bio-fertilizers in hypersaline biotopes [27,28]. Our research goal was to confirm Frankia ability to resist cadmium stress and identify the cadmium resistance mechanism in F. alni ACN14a. ...
Background
Cadmium (Cd²⁺) is one of the highly toxic heavy metals and is considered as a carcinogenic agent. Our aim was to confirm Frankia alni ACN14a ability to resist Cd²⁺ and determine the genes involved in the resistance.
Results
Up to 10 and 22 times in Cd²⁺ accumulation were detected in F. alni ACN14a and Frankia casuarinae CcI3 hyphae when exposure to 1 mM, respectively. Scanning Electron Microscopy (SEM) exhibited a stable Cd²⁺ precipitate to the cell surface and increase in Cd²⁺ weight level reached attached 16.45 % when evaluated with SEM-EDAX analysis. Potential two Cd²⁺ operons were identified: 1- cadCA operon encoding a copper-transporting P-type ATPase A (cadA, FRAAL0989), ArsR family regulator (cadC, FRAAL0988) with 37- and 70-fold increases in their expression by qRT-PCR, respectively; 2- cadB/DX which encodes a putative cobalt-zinc-cadmium resistance protein (cadD, FRAAL3628) and heavy metal-associated domain protein (cadX, FRAAL3626) with 22- and 16-fold up-regulation when exposure to Cd²⁺-stress.
Conclusions
Cd²⁺ tolerance by F. alni ACN14a involved effluxing Cd²⁺ outside the cells and binding it to the membrane surface. Our results indicate the existence of two cadmium-resistance mechanisms in Frankia strains which support the idea of using them as bioremediation agent.
... Nevertheless, the actinorhizal symbiosis was not profoundly affected as the shoot to root biomass ratios had augmentation in the presence of the symbiont. The strains of Frankia exhibited different sensibility, tolerance, growth, and nodulation in presence of various environmental stresses including extremes of pH and temperature, heavy metal toxicity, salinity, and chemical and organic stressors such as antibiotics, phenolics, peroxides, and hydrocarbons [121,167]. This might necessitate screening for the most tolerant and compatible combinations of Frankia and actinorhizal plants. ...
... Surprisingly, in vitro salt resistance of Frankia strains had little effect on the onsite bacteria-plant root symbiotic connection under salt stress conditions. However, the successful establishment of actinorhizal plants in a saline environment was made possible, when the prior plant root-Frankia association is rooted at the sites [167]. The osmotic stress induced by PEG upregulated the proteins associated with ABCtransporters, mechano-sensitive ion channels, and CRISPR-associated (Cas) components, and downregulated the processes like aerobic respiration, nitrogen fixation, and homologous recombination in Frankia alni cells [189]. ...
Nitrogen occurs as inert and inaccessible dinitrogen gaseous form (N2) in the atmosphere. Biological nitrogen fixation is a chief process that makes this dinitrogen (N2) accessible and bioavailable in the form of ammonium (NH4+) ions. The key organisms to fix nitrogen are certain prokaryotes, called diazotrophs either in the free‐living form or establishing significant mutual relationships with a variety of plants. On such examples is ~95–100 MY old incomparable symbiosis between dicotyledonous trees and a unique actinobacterial diazotroph in diverse ecosystems. In this association, the root of the certain dicotyledonous tree (~25 genera and 225 species) belonging to three different taxonomic orders, Fagales, Cucurbitales, and Rosales (FaCuRo) known as actinorhizal trees can host a diazotroph, Frankia of order Frankiales. Frankia is gram‐positive, branched, filamentous, sporulating, and free‐living soil actinobacterium. It resides in the specialized, multilobed, and coralloid organs (lateral roots but without caps), the root nodules of actinorhizal tress. This review aims to provide systematic information on the distribution and the phylogenetic diversity of hosts from FaCuRo and their micro‐endosymbionts (Frankia spp.), colonization mechanisms, and signaling pathways. We also aim to provide details on developmental and physiological imperatives for gene regulation and functional genomics of symbiosis, phenomenal restoration ecology, influences of contemporary global climatic changes, and anthropogenic impacts on plant–Frankia interactions for the functioning of ecosystems and the biosphere.
... It was documented that Frankia-associated symbiosis enables host actinorhizal plants to grow in highly constrained soils (contaminated, waterdeficient/logged, nutrient-deficient), including intensely saline/alkaline ones [77,78]. For example, in Casuarina glauca and Casuarina equisetifolia exposed to NaCl salinity (up to 500 mM), inoculation with Frankia strains CcI3 and CeD improved plant height by up to 66% and 45%, respectively, with significantly increased biomass (shoot, root, and total), dry weight, and proline and chlorophyll contents compared to uninoculated control plants [79]. The authors explained this result by improved N nutrition and photosynthesis potential in inoculated (vs. ...
... Currently, most actinorhizal woody species (e.g., from the Casuarinas family) are largely exploited in land reclamation and restoration of mining, metal-contaminated, and salt-affected environments [81], followed by agroforestry, crop, and soil protection from wind and wildfire influence and erosion [79]. However, genotypic predispositions of actinorhizal plants and the associated actinobacteria Frankia represents valuable potential for further exploitation and improvement of cultivated crops and their symbiotic associations for food/feed production in salt-affected (agro)environments, although extremely complex processes must be elucidated by comparative genomics and proteomics prior to this. ...
Salinization of soils and freshwater resources by natural processes and/or human activities has become an increasing issue that affects environmental services and socioeconomic relations. In addition, salinization jeopardizes agroecosystems, inducing salt stress in most cultivated plants (nutrient deficiency, pH and oxidative stress, biomass reduction), and directly affects the quality and quantity of food production. Depending on the type of salt/stress (alkaline or pH-neutral), specific approaches and solutions should be applied to ameliorate the situation on-site. Various agro-hydrotechnical (soil and water conservation, reduced tillage, mulching, rainwater harvesting, irrigation and drainage, control of seawater intrusion), biological (agroforestry, multi-cropping, cultivation of salt-resistant species, bacterial inoculation, promotion of mycorrhiza, grafting with salt-resistant rootstocks), chemical (application of organic and mineral amendments, phytohormones), bio-ecological (breeding, desalination, application of nano-based products, seed biopriming), and/or institutional solutions (salinity monitoring, integrated national and regional strategies) are very effective against salinity/salt stress and numerous other constraints. Advances in computer science (artificial intelligence, machine learning) provide rapid predictions of salinization processes from the field to the global scale, under numerous scenarios, including climate change. Thus, these results represent a comprehensive outcome and tool for a multidisciplinary approach to protect and control salinization, minimizing damages caused by salt stress.
... Inoculation of young C. glauca plants (Myall Lakes National Park, Australia), grown in hydroponic nutrient solution, with Frankia CcI3 or CeD enhanced salt stress tolerance up to 200 mM NaCl, with a more pronounced positive effect of CcI3. In the case of young plants of C. equisetifolia (Louga, Senegal) grown on soil, only Frankia CeD produced a visible effect (Ngom et al. 2016). ...
Salinization is a global concern whose extent is predicted to progressively increase over this century. In this context, biosaline agriculture has been included in the set of climate-smart solutions to support sustainable and resilient ecosystems. The Casuarinaceae family is widely known for its intrinsic ability to thrive under saline environments. Therefore, understanding the mechanisms underlying salt-tolerance in this family is of utmost importance for landscape integration and soil rehabilitation. In this mini-review, we present the state of the art of Casuarina research – from gene to ecosystem – in response to salinity, towards green growth and sustainable development. Based on literature retrieval from 2000 to 2021, a general overview of salt-stress tolerance in the Casuarinaceae is presented, and the extent of the contribution of root-nodule and arbuscular mycorrhizal symbioses, as well as the related eco-physiological and molecular changes are discussed.
... Several studies have described the ability of Casuarinaceae to use adaptive mechanisms such as NaCl compartmentalization in roots (Isla et al. 2014;Selvakesavan et al. 2016), regulation of oxidative conditions (Jorge et al. 2021), synthesis of osmoprotective compounds (Carter et al. 2006;Ngom et al. 2016), maintenance of membrane integrity and potential of components involved in the C assimilation pathway . Moreover, a wide variability in salt stress resistance has been reported among Casuarina species (Van der Moezel et al. 1988). ...
... This could be due to the negative effects of NaCl on plant growth, AMF and Frankia (Evelin et al. 2009;Hanin et al. 2016) and/or on the establishment of symbiotic association (Sheng et al. 2008). Thus, a decrease in the number of nodules under saline conditions has also been reported in C. glauca, as well as a suppression of root hair deformation that may negatively affect the initiation of the symbiotic association with Frankia (Mansour et al. 2016;Ngom et al. 2016). In addition the deformation of the hyphal structure of AMF under the effect of NaCl, can reduce their efficiency in nutrient uptake therefore biomass (Huang et al. 2010). ...
... Several previous studies have shown that the improvement of salt tolerance in Casuarina by Frankia and/or mycorrhizal fungi is highly dependent on the age, ecotype and intrinsic capacity of the plant Ribeiro-Barros et al. 2016;Jorge et al. 2021), as well as on microbial strain (Mansour et al. 2016;Ngom et al. 2016;Djighaly et al. 2018). Mansour et al. (2016) showed that C. glauca inoculated with a salt-tolerant Frankia strain was able to promote nodule formation, high rate of N 2 -fixation and seedling growth. ...
Plants of the Casuarinaceae family are widely known for their ability to tolerate salt stress. Casuarinaceae are able to develop symbiotic association with arbuscular mycorrhizal fungi and with the soil bacteria Frankia. The aim of this study was to evaluate adaptation mechanisms of Casuarina to tolerate salt stress when interacting Rhizophagus fasciculatus and Frankia. Two species showing different salt tolerance levels, i.e. C. equisetifolia and C. obesa, were grown in sandy sterile soil, inoculated with R. fasciculatus and/or Frankia and then watered gradually with increased concentrations of saline solutions. Total antioxidant activity, antioxidant enzyme concentration, and salt effects on cellular ultrastructure of shoots were evaluated. C. obesa has a better salt stress tolerance compared to C. equisetifolia. Co-inoculation (R. fasciculatus and Frankia) improved the performance of both plant species in saline. Higher antioxidant activity was observed in C. obesa. At 400 mM of NaCl C. obesa revealed a maintenance of cellular integrity whereas cell membrane rupture and disintegration of cellular contents were observed in C. equisetifolia tissues. Our results suggest that a selection of appropriate plant species is important to improve plant performance in saline soils.
