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- Restoration of Triticum aestivum Growth under Salt Stress by Phosphate-Solubilizing Bacterium Isolated from Southern AlgeriaPublication . Belkebla, Nadia; Bessai, Sylia Ait; Melo, Juliana; Caeiro, Maria Filomena; Cruz, Cristina; Nabti, El-hafidSalinity causes significant agricultural losses in many areas in the world. Plant growth promoting bacteria (PGPB) are a promising solution to enhance plant growth and productivity under such stress conditions by different mechanisms, mainly phosphorous solubilization. This study aims to improve wheat seedling growth under salt stress by a halotolerant phosphorous-solubilizing bacterial strain. Soil sample was collected in the south of Algeria (Ghardaia), and bacterial isolation was carried out on nutrient agar (NA) at different NaCl concentrations (300; 600 and 900 mM). The ability of the halotolerant isolates to solubilize inorganic phosphorous at 0; 300; 600 and 900 mM NaCl was determined. The isolate that showed the highest solubilization indexes was selected and identified as Pseudomonas azotoformans. Sterile wheat (Triticum aestivum) seeds were inoculated by this strain and then sown in soil at different NaCl concentrations (0; 100; 200; 300 mM). Different growth parameters were measured after 15 days. The strain showed its highest capacity for phosphorous solubilization (255.152 ± 0.01 µg/mL) at 300 mM NaCl, and for phytate mineralization (0.168 ± 0.002 U/mL) at 100 mM NaCl. The highest amount of soluble phosphorous in the soil was 49.42 ± 0.36 ppm obtained at 100 mM NaCl. Seed germination percentage, shoot and root length and fresh and dry weights were found to be higher in bacterial inoculated seedlings compared to uninoculated ones. According to this study, the use of plant growth promoting bacteria represents an important biotechnological approach to restore phosphorous levels in saline soils and to promote plant growth in salt-affected agricultural land.
- Inoculation With Piriformospora indica Is More Efficient in Wild-Type Rice Than in Transgenic Rice Over-Expressing the Vacuolar H+-PPasePublication . Bertolazi, Amanda Azevedo; de Souza, Sávio Bastos; Ruas, Katherine Fraga; Campostrini, Eliemar; de Rezende, Carlos Eduardo; Cruz, Cristina; Melo, Juliana; Colodete, Carlos Moacir; Varma, Ajit; Ramos, Alessandro CoutinhoAchieving food security in a context of environmental sustainability is one of the main challenges of the XXI century. Two competing strategies to achieve this goal are the use of genetically modified plants and the use of plant growth promoting microorganisms (PGPMs). However, few studies assess the response of genetically modified plants to PGPMs. The aim of this study was to compare the response of over expressing the vacuolar H+-PPase (AVP) and wild-type rice types to the endophytic fungus; Piriformospora indica. Oryza sativa plants (WT and AVP) were inoculated with P. indica and 30 days later, morphological, ecophysiological and bioenergetic parameters, and nutrient content were assessed. AVP and WT plant heights were strongly influenced by inoculation with P. indica, which also promoted increases in fresh and dry matter of shoot in both genotypes. This may be related with the stimulatory effect of P. indica on ecophysiological parameters, especially photosynthetic rate, stomatal conductance, intrinsic water use efficiency and carboxylation efficiency. However, there were differences between the genotypes concerning the physiological mechanisms leading to biomass increment. In WT plants, inoculation with P. indica stimulated all H+ pumps. However, in inoculated AVP plants, H+-PPase was stimulated, but P- and V-ATPases were inhibited. Fungal inoculation enhanced nutrient uptake in both shoots and roots of WT and AVP plants, compared to uninoculated plants; but among inoculated genotypes, the nutrient uptake was lower in AVP than in WT plants. These results clearly demonstrate that the symbiosis between P. indica and AVP plants did not benefit those plants, which may be related to the inefficient colonization of this fungus on the transgenic plants, demonstrating an incompatibility of this symbiosis, which needs to be further studied.
- Dá-lhe PPublication . Dias, Teresa; Munzi, Silvana; Melo, Juliana; Santana, Margarida; Barão, Lúcia; Cruz, Cristina
- The diazotrophic bacteria Azospirillum baldaniorum and A. brasilense improve wheat seedlings' nitrogen budget through ammonia scavengingPublication . Dias, Teresa; Azmaliyev, Kamran; Melo, Juliana; Santos, Ana Margarida; Correia, Patrícia; Cruz, CristinaBesides N2 fixation, we consider that other diazotrophic traits can be explored to increase plants' nitrogen (N) budget. Here, we report initial results of the capacity of the diazotrophic plant growth promoting rhizobacteria Azospirillum baldaniorum and A. brasilense to improve wheat seedlings' N budget through ammonia (NH3) scavenging. We inoculated wheat seedlings with two Azospirillum strains (A. baldaniorum Sp245 and A. brasilense ARG2) and determined its effect on plant biomass, N content and N isotopic signatures (i.e., δ15N). Furthermore, using bipartite Petri dishes, we grew the Azospirillum strains under increasingly alkaline conditions (from pH 7.5 to 10.0), which created a gradient of atmospheric NH3 concentrations ([NH3]), and we used Saccharomyces cerevisiae mutants to explore the involvement of the AMT/MEP/Rh proteins in atmospheric NH3 scavenging. Wheat seedlings inoculated with A. baldaniorum Sp245 and A. brasilense ARG2 increased their N content by 65 and 94 % (respectively), and their negative N isotopic signatures (around −10 ‰, which contrasted with positive signatures in control plants) were compatible with NH3 transport through AMT/MEP/Rh transporters, but not with N2 fixation. Furthermore, increasing the atmospheric [NH3] stimulated the growth rate of the Azospirillum strains up to 5-fold in relation to ambient atmospheric [NH3], showing that both Azospirillum strains scavenged the atmospheric NH3 and used it to grow. Our data clearly show that: i) NH3 scavenging by A. baldaniorum Sp245 and A. brasilense ARG2 is involved in increasing plant's N budget; and ii) NH3 transport through AMT/MEP/Rh protein family transporters is involved in microbial NH3 scavenging. This overlooked microbial trait can be an interesting tool to mitigate atmospheric [NH3], especially in farming environments.
- Impact of mineral and organic fertilisation practices on elemental authenticity signature on apple Royal Gala from protected geographical indication (PGI) “Maçã de Alcobaça”Publication . Duarte, Bernardo; Carreiras, João Albuquerque; Melo, Juliana; Gonçalves, Marta; Silva, Anabela B.; de Sousa, Miguel LeãoMarket demand, climate change and soil degradation force producers to maintain the productivity and quality of high-market-value products, such as Protected Geographical Indication (PGI) fruits. “Maçã de Alcobaça” apples produced in the central-western part of Portugal, namely the variety Royal Gala, one of the PGI varieties with higher demand, are among those with higher requirements in terms of fertilization to maintain the high productivity demanded by the market. In the present work, three different soil NPK fertilization schemes were applied to experimental orchards within the PGI area (1 x mineral NPK proposed for integrated production, an intermediate strategy that included organic granular amendment and 2 x mineral NPK), and the elemental profiles of the apple pulps were analysed and compared. Some mineral elements improved their concentration in the apple pulps with fertilization due to interactions of these elements with the fertilizer components (namely, nitrogen, potassium and phosphorus) or to potential changes in the bioavailability of the elements in the soil due to fertilization application. From a nutritional perspective, enhancing the mineral profile of apple pulps can be achieved by applying 1 x NPK fertilization. Consuming an average of 2 fruits daily (160 g each) would then help meet a higher percentage of the daily requirements for most essential elements crucial for human nutrition. Also, noteworthy to mention, that none of the tested fertilization practices led to a reduction in the nutritional quality of the fruits analysed when compared to the 1 x NPK condition. The present work also had the objective of evaluating if these fertilization practices and the mineral changes induced would have implications for the PGI authenticity elemental signatures previously developed. Using Partial Least Squares-Discriminant Analysis (PLS-DA) models calibrated with PGI and non-PGI (from North Portugal and Italy) samples and feeding these models with elemental profile data of fruits collected from fertilized orchards as blind samples, it was possible to observe that all samples from the fertilization trials were correctly classified as PGI samples. This reinforces the edaphic characteristics of the cultivation area's prevalent role over the effect of fertilization practices or physiological trait changes, in shaping the elemental signature of the fruits. This was found to be mostly due to the high influence of geologically linked elements (such as Rb, Pb and Y) in the discrimination of the sample provenance. This allows us to confirm the suitability of the elemental traceability models for “Maçã de Alcobaça” PGI authenticity validation, ensuring its provenance and nutritional characteristics to the consumers and maintaining its market value even if fertilization practices are applied to fight less favourable cultivation conditions.
- In the trail of “Maçã de Alcobaça” protected geographical indication (PGI): Multielement chemometrics as a security and anti-fraud tool to depict clones, cultivars and geographical origins and nutritional valuePublication . Duarte, Bernardo; Melo, Juliana; Mamede, Renato; Carreiras, João; Figueiredo, Andreia; Fonseca, Vanessa F.; de Sousa, Miguel Leão; Silva, Anabela B.Food fraud associated with the intentional mislabelling of non-Protected Geographical Indication (PGI) is a concern for consumers. “Maçã de Alcobaça” (Alcobaça apple) is one of the oldest Portuguese PGI products, characteristic of the main apple-growing regions in the country, being of utmost importance to develop traceability and authenticity tools to depict the PGI certification status of these products. Pulp multielement signatures were able to discriminate with moderate accuracy (65.7 %) different Royal Gala clones, grown within the same cultivation area. Moreover, Variable Importance in Projection Partial Least-Squares Discriminant Analysis (VIP-PLS-DA) allowed the discrimination of the Royal Gala samples from different PGI producers with 70.0 % accuracy. Apple PGI cultivars were also discriminated accurately (82.0 %). Expanding the approach to non-PGI production areas, several cultivars could be distinguished, according to their provenance with high accuracy, namely Starking (100.0 % accuracy), Granny Smith (100.0 % accuracy), Fuji (100.0 % accuracy), Royal Gala (86.7 % accuracy) and Reineta (90.3 % accuracy). The PGI fruit's microelement nutritional traits highlighted their higher nutritional value, an important trait for food fraud reduction, informing the consumer of the product authenticity, and providing insights on the nutritional value of these high-value market products.
- Halophilic Plant Growth-Promoting Rhizobacteria as Producers of Antifungal Metabolites under Salt StressPublication . Ould Ouali, Karima; Houali, Karim; Cruz, Cristina; Melo, Juliana; Benakli, Yasmina; Ousmer, Lila; Madani, Zahia; Nabti, El-HafidSalinity is one of the main factors causing soil deterioration, making it unsuitable for agriculture. It is well documented that the application of halotolerant and halophilic plant growth-promoting bacteria (PGPR: plant growth-promoting rhizobacteria) with biological control activities as an inoculant of cultivated plants offers a biological alternative to the use of agrochemicals, particularly when subjected to salt stress. From this perspective, 70 bacterial strains were isolated from saline soils (sebkha) in arid and semi-arid areas of Eastern Algeria. Three isolates were selected based on their ability to produce bioactive molecules allowing them to promote plant growth, such as hydrolytic enzymes, indole acetic acid (auxin-phytohormone), HCN, NH3, etc. Two of these isolates belonged to the genus Serratia and the third was a halophilic Halomonas bacteria. These bacteria were identified based on their 16S rDNA sequences. Antagonism tests against phytopathogenic fungi were carried out. The identification of the antifungal molecules produced by these bacteria was determined using high-performance liquid chromatography. These bacteria can inhibit mycelial development against phytopathogenic fungi with rates reaching 80.67% against Botrytis cinerea, 76.22% against Aspergillus niger, and 66.67% against Fusarium culmorum for Serratia sp. The strain Halomonas sp. inhibited mycelial growth through the production of volatile substances of Aspergillus niger at 71.29%, Aspergillus flavus at 75.49%, and Penicillium glabrum at a rate of 72.22%. The identification of the antifungal molecules produced by these three bacteria using HPLC revealed that they were polyphenols, which makes these strains the first rhizobacteria capable of producing phenolic compounds. Finally, pot tests to determine the effectiveness of these strains in promoting wheat growth under salinity stress (125 mM, 150 mM, and 200 mM) was carried out. The results revealed that a consortium of two isolates (Serratia sp. and Halomonas sp.) performed best at 125 mM. However, at higher concentrations, it was the halophilic bacteria Halomonas sp. that gave the best result. In all cases, there was a significant improvement in the growth of wheat seedlings inoculated with the bacteria compared to non-inoculated controls.
- Inoculation with the endophytic bacterium Herbaspirillum seropedicae promotes growth, nutrient uptake and photosynthetic efficiency in ricePublication . Ramos, Alessandro C.; Melo, Juliana; de Souza, Sávio B.; Bertolazi, Amanda A.; Silva, Renderson A.; Rodrigues, Weverton P.; Campostrini, Eliemar; Olivares, Fábio L.; Eutrópio, Frederico J.; Cruz, Cristina; Dias, TeresaMain conclusion: Higher vacuolar proton pump activity may increase plant energy and nutrient use efficiency and provide the nexus between plant inoculation with Herbaspirillum seropedicae and growth promotion. Abstract: Global change and growing human population are exhausting arable land and resources, including water and fertilizers. We present inoculation with the endophytic plant-growth promoting bacterium (PGPB) Herbaspirillum seropedicae as a strategy for promoting growth, nutrient uptake and photosynthetic efficiency in rice (Oryza sativa L.). Because plant nutrient acquisition is coordinated with photosynthesis and the plant carbon status, we hypothesize that inoculation with H. seropedicae will stimulate proton (H+) pumps, increasing plant growth nutrient uptake and photosynthetic efficiency at low nutrient levels. Plants were inoculated and grown in pots with sterile soil for 90 days. Herbaspirillum seropedicae endophytic colonization was successful and, as hypothesized, inoculation (1) stimulated root vacuolar H+ pumps (vacuolar H+-ATPase and vacuolar H+-PPase), and (2) increased plant growth, nutrient contents and photosynthetic efficiency. The results showed that inoculation with the endophytic bacterium H. seropedicae can promote plant growth, nutrient uptake and photosynthetic efficiency, which will likely result in a more efficient use of resources (nutrients and water) and higher production of nutrient-rich food at reduced economic and environmental costs.
- Multiple modes of action are needed to unlock soil phosphorus fractions unavailable for plants: The example of bacteria- and fungi-based biofertilizersPublication . Basílio, Francisco; Dias, Teresa; Santana, Margarida; Melo, Juliana; Carvalho, Luís; Correia, Patrícia; Cruz, CristinaPhosphorus (P) is an essential macronutrient for all life forms. Therefore, meeting the needs of a growing human population and their changing consumption patterns drastically intensified the use of mineral P fertilizers in agriculture. As a result, the current use of mineral P fertilizers causes severe negative economic, environmental and health impacts, which creates an urgent need for more sustainable agronomic practices capable of maintaining crop yields while improving P use efficiency. We consider that agronomic options that recycle/reuse the accumulated unavailable P (turn the unavailable P accumulated in the soil into P forms available for crop uptake) are an efficient strategy for food security, food production autonomy and sovereignty, and environmental sustainability. Here, we review P cycling in the soil and plant strategies to improve P acquisition, with special emphasis on the role of soil microbes as plant allies, namely their contribution to plant P acquisition directly through the production of organic acids and phosphatases, and indirectly through the production of phytohormones. Finally, we discuss why and how the use of soil microbes (mostly bacteria and fungi) with multiple modes of action may be the key to unlock soil P fractions unavailable for crop uptake, and highlight the benefits of combining: i) high-throughput sequencing; ii) new culturing methods to isolate and cultivate novel isolates; and iii) soil ecology experiments to develop multi-strain biofertilizers with diverse, complementary, and redundant modes of action in improving plant P acquisition and other benefits.
- The Free-Living Stage Growth Conditions of the Endophytic Fungus Serendipita indica May Regulate Its Potential as Plant Growth Promoting MicrobePublication . Dias, Teresa; Pimentel, Vívian; Cogo, Antônio Jesus Dorighetto; Costa, Raquel; Bertolazi, Amanda Azevedo; Miranda, Camila; de Souza, Sávio Bastos; Melo, Juliana; Carolino, Manuela; Varma, Ajit; Eutrópio, Frederico; Olivares, Fábio Lopes; Ramos, Alessandro Coutinho; Cruz, CristinaSerendipita indica (former Piriformospora indica) is a non-obligate endophytic fungus and generally a plant growth and defence promoter with high potential to be used in agriculture. However, S. indica may switch from biotrophy to saprotrophy losing its plant growth promoting traits. Our aim was to understand if the free-living stage growth conditions (namely C availability) regulate S. indica’s phenotype, and its potential as plant-growth-promoting-microbe (PGPM). We grew S. indica in its free-living stage under increasing C availabilities (2–20 g L–1 of glucose or sucrose). We first characterised the effect of C availability during free-living stage growth on fungal phenotype: colonies growth and physiology (plasma membrane proton pumps, stable isotopic signatures, and potential extracellular decomposing enzymes). The effect of the C availability during the free-living stage of the PGPM was evaluated on wheat. We observed that C availability during the free-living stage regulated S. indica’s growth, ultrastructure and physiology, resulting in two distinct colony phenotypes: compact and explorer. The compact phenotype developed at low C, used peptone as the major C and N source, and displayed higher decomposing potential for C providing substrates; while the explorer phenotype developed at high C, used glucose and sucrose as major C sources and casein and yeast extract as major N sources, and displayed higher decomposing potential for N and P providing substrates. The C availability, or the C/N ratio, during the free-living stage left a legacy to the symbiosis stage, regulating S. indica’s potential to promote plant growth: wheat growth promotion by the explorer phenotype was ± 40% higher than that by the compact phenotype. Our study highlights the importance of considering microbial ecology in designing PGPM/biofertilizers. Further studies are needed to test the phenotypes under more extreme conditions, and to understand if the in vitro acquired characteristics persist under field conditions.