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- Early Identification of Plant Drought Stress Responses: Changes in Leaf Reflectance and Plant Growth Promoting Rhizobacteria Selection-The Case Study of Tomato PlantsPublication . Rosa, Ana Paula; Barão, Lúcia; Chambel, Lélia; Cruz, Cristina; Santana, MargaridaDrought is a worldwide problem, especially in arid and semi-arid regions. Detection of drought stress at the initial stages, before visible signs, to adequately manage irrigation and crop fertilization to avoid crop yield loss, is a desire of most farmers. Here, we evaluated the response of tomato plants to water scarcity, through changes in leaf reflectance due to modification in leaf pigments’ content, which translates into differences in spectral reflectance indices (SRI) values. Our methodology is innovative, as we were able to easily calculate and identify several SRIs for the early detection of drought stress “invisible” responses. We used a handheld spectro-radiometer to obtain SRI values from leaves of tomato plants growing under two different water regimes for 37 days. In an ensemble of 25 SRIs, we identified 12 that showed a consistent trend of significant differences between treatments along the experiment and within these, NDVI, SR, ZMI, Ctr2, GM1, and GM2 were already significantly different between treatments at day 7 after the start of the experiment and Ctr1 at day 9; although, no signs of damage were visible. Therefore, our results pinpoint these SRIs as promising proxies for the early detection of “invisible” responses to drought onset. We also analyzed the relationship between the monitored SRIs and plant morphological parameters measured during the experiment, highlighting a relationship between GM1 and plant height and leaf number. Finally, we observed a high abundance of putative beneficial bacteria among isolates collected from the tomato water-limited rhizo-environment at the terminus of the experiment, suggesting the active recruitment or selection of Plant Growth Promoting Rhizobacteria by tomato roots as a response to drought. Our work may be adapted into an easy protocol, of rapid execution, to be used in small-scale fields for early drought stress detection.
- Dá-lhe PPublication . Dias, Teresa; Munzi, Silvana; Melo, Juliana; Santana, Margarida; Barão, Lúcia; Cruz, Cristina
- Finding optimal microorganisms to increase crop productivity and sustainability under drought – a structured reflectionPublication . Rosa, Ana Paula; Dias, Teresa; Mouazen, Abdul M.; Cruz, Cristina; Santana, Margarida M.Considering the more frequent and longer drought events due to climate change, improving plant drought tolerance became a priority. The search for plant growth promoting rhizobacteria (PGPR) able to improve plant drought tolerance has been long addressed, but with inconsistent results. Here, we summarize the PGPR mechanisms that improve plant drought tolerance, identify the pitfalls in current PGPR isolation and selection routines, and discuss the key points to define new strategies to get optimal PGPR for plant drought tolerance. Drought and host genotype impact rhizo-communities, and host-mediated selection strategies may be used to obtain a drought-adapted rhizomicrobiome that can be a source for PGPR isolation. Alternatively, an integrated omics-level analysis can improve our knowledge on the mechanisms of rhizomicrobiome construction, and a targeted approach can be designed, which will be focused on key PGP traits. New strategies to build PGPR consortia for improvement of plant drought tolerance are also suggested.
- Nitric Oxide Accumulation: The Evolutionary Trigger for PhytopathogenesisPublication . Santana, Margarida; Gonzalez, Juan M.; Cruz, CristinaMany publications highlight the importance of nitric oxide (NO) in plant–bacteria interactions, either in the promotion of health and plant growth or in pathogenesis. However, the role of NO in the signaling between bacteria and plants and in the fate of their interaction, as well as the reconstruction of their interactive evolution, remains largely unknown. Despite the complexity of the evolution of life on Earth, we explore the hypothesis that denitrification and aerobic respiration were responsible for local NO accumulation, which triggered primordial antagonistic biotic interactions, namely the first phytopathogenic interactions. N-oxides, including NO, could globally accumulate via lightning synthesis in the early anoxic ocean and constitute pools for the evolution of denitrification, considered an early step of the biological nitrogen cycle. Interestingly, a common evolution may be proposed for components of denitrification and aerobic respiration pathways, namely for NO and oxygen reductases, a theory compatible with the presence of low amounts of oxygen before the great oxygenation event (GOE), which was generated by Cyanobacteria. During GOE, the increase in oxygen caused the decrease of Earth’s temperature and the consequent increase of oxygen dissolution and availability, making aerobic respiration an increasingly dominant trait of the expanding mesophilic lifestyle. Horizontal gene transfer was certainly important in the joint expansion of mesophily and aerobic respiration. First denitrification steps lead to NO formation through nitrite reductase activity, and NO may further accumulate when oxygen binds NO reductase, resulting in denitrification blockage. The consequent transient NO surplus in an oxic niche could have been a key factor for a successful outcome of an early denitrifying prokaryote able to scavenge oxygen by NO/oxygen reductase or by an independent heterotrophic aerobic respiration pathway. In fact, NO surplus could result in toxicity causing “the first disease” in oxygen- producing Cyanobacteria. We inspected in bacteria the presence of sequences similar to the NO-producing nitrite reductase nirS gene of Thermus thermophilus, an extreme thermophilic aerobe of the Thermus/Deinococcus group, which constitutes an ancient lineage related to Cyanobacteria. In silico analysis revealed the relationship between the presence of nirS genes and phytopathogenicity in Gram-negative bacteria.
- Soil Thermophiles and Their Extracellular Enzymes: A Set of Capabilities Able to Provide Significant Services and RisksPublication . Gonzalez, Juan M.; Santana, Margarida; Gomez, Enrique J.; Delgado, José A.During this century, a number of reports have described the potential roles of thermophiles in the upper soil layers during high-temperature periods. This study evaluates the capabilities of these microorganisms and proposes some potential consequences and risks associated with the activity of soil thermophiles. They are active in organic matter mineralization, releasing inorganic nutrients (C, S, N, P) that otherwise remain trapped in the organic complexity of soil. To process complex organic compounds in soils, these thermophiles require extracellular enzymes to break down large polymers into simple compounds, which can be incorporated into the cells and processed. Soil thermophiles are able to adapt their extracellular enzyme activities to environmental conditions. These enzymes can present optimum activity under high temperatures and reduced water content. Consequently, these microorganisms have been shown to actively process and decompose substances (including pollutants) under extreme conditions (i.e., desiccation and heat) in soils. While nutrient cycling is a highly beneficial process to maintain soil service quality, progressive warming can lead to excessive activity of soil thermophiles and their extracellular enzymes. If this activity is too high, it may lead to reduction in soil organic matter, nutrient impoverishment and to an increased risk of aridity. This is a clear example of a potential effect of future predicted climate warming directly caused by soil microorganisms with major consequences for our understanding of ecosystem functioning, soil health and the risk of soil aridity.
- The Plant Growth-Promoting Potential of Halotolerant Bacteria Is Not Phylogenetically Determined: Evidence from Two Bacillus megaterium Strains Isolated from Saline Soils Used to Grow WheatPublication . Ait Bessai, Sylia; Cruz, Joana; Carril, Pablo; Melo, Juliana; Santana, Margarida; Mouazen, Abdul M.; Cruz, Cristina; Yadav, Ajar Nath; Dias, Teresa; Nabti, El-hafid1) Background: Increasing salinity, further potentiated by climate change and soil degra- dation, will jeopardize food security even more. Therefore, there is an urgent need for sustainable agricultural practices capable of maintaining high crop yields despite adverse conditions. Here, we tested if wheat, a salt-sensitive crop, could be a good reservoir for halotolerant bacteria with plant growth-promoting (PGP) capabilities. (2) Methods: We used two agricultural soils from Algeria, which differ in salinity but are both used to grow wheat. Soil halotolerant bacterial strains were isolated and screened for 12 PGP traits related to phytohormone production, improved nitrogen and phosphorus availability, nutrient cycling, and plant defence. The four ‘most promising’ halotolerant PGPB strains were tested hydroponically on wheat by measuring their effect on germination, sur- vival, and biomass along a salinity gradient. (3) Results: Two halotolerant bacterial strains with PGP traits were isolated from the non-saline soil and were identified as Bacillus subtilis and Pseudomonas fluorescens, and another two halotolerant bacterial strains with PGP traits were isolated from the saline soil and identified as B. megaterium. When grown under 250 mM of NaCl, only the inoculated wheat seedlings survived. The halotolerant bacterial strain that displayed all 12 PGP traits and promoted seed germination and plant growth the most was one of the B. megaterium strains isolated from the saline soil. Although they both belonged to the B. megaterium clade and displayed a remarkable halotolerance, the two bacterial strains isolated from the saline soil differed in two PGP traits and had different effects on plant performance, which clearly shows that PGP potential is not phylogenetically determined. (4) Conclusions: Our data highlight that salt-sensitive plants and non-saline soils can be reservoirs for halotolerant microbes with the potential to become effective and sustainable strategies to improve plant tolerance to salinity. However, these strains need to be tested under field conditions and with more crops before being considered biofertilizer candidates.
- Transformation of organic and inorganic sulfur– adding perspectives to new players in soil and rhizospherePublication . Santana, Margarida; Dias, Teresa; Gonzalez, Juan M.; Cruz, CristinaSulfur (S) is a macro-element required for life. S deficiency limits plant growth. Microorganisms carry out several essential steps in the recycling of organic and inorganic S in soils. Microbes and plants interact, mainly in the rhizosphere, but the mechanisms ruling these interactions and the extent of such relationships remain poorly understood. Here, we update current perspectives on the role of specific microorganisms involved in S cycling and the spatial interaction between plants and microbes. To contextualize the pitfalls of current approaches in studying soil S transformations, we review the current main established steps, redox reactions and microbial players in the S cycle. The incorporation of novel microbial taxa, namely those important for organic S mineralization, which may be important ecosystem players in terms of soil functionality, and of the spatial-temporal context at aggregate-level for the relevance of plant-microbe interactions, introduce important implications involving the role of microorganisms in the rhizosphere and require an integrated analysis. Herein, the rhizosphere is a focus – a habitat of selected low-abundance species, where important microbial groups act in S turnover and plant growth – while keeping a perspective on important microbial feedback S fluxes that may occur in bulk soils.
- 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.
- Achromobacter xylosoxidans and Enteromorpha intestinalis Extract Improve Tomato Growth under Salt StressPublication . Santana, Margarida; Rosa, Ana Paula; Zamarreño, Angel M.; García-Mina, José María; Rai, Abdelwahab; Cruz, CristinaThe effect of seed coating salt-stressed tomato with the bacterium Achromobacter xylosoxidans BOA4 and/or irrigation with an extract of the marine algae Enteromorpha intestinalis (EI) is herein evaluated. The plant shoots and roots were harvested separately on day 50, following extensive saline stress. The addition of BOA4 and/or EI extract resulted in an average increase of 33% in plant shoot DW, but an averaged decrease of 44% in the root to shoot biomass ratio. Anthocyanin content increased by over 34% and 44% with EI and BOA4 plus EI treatments, respectively. Since enhanced protein tyrosine nitration (PTN) is a known plant response to salt stress, the PTN level was inspected through 3-nitrotyrosine content determination. This was drastically increased by salt stress; however, BOA4, EI or both caused an averaged PTN decrease of 30% in stressed roots or shoots. This PTN response could be associated with tomato phenotypic characteristics and is postulated to be inversely correlated to cytokinin contents in stressed plants, namely cis-zeatin-type-cis-zeatin (cZ) plus cis-zeatin riboside (cZR), and isopentenyladenine (iP). The latter showed a drastic average increase by 3.6-fold following BOA4 and/or EI treatments of salinized tomato. This increment could be related to cytokinin biosynthesis induced by the applied bio-stimulants; IP and derivatives are the main cytokinins in seaweeds, and Achromobacter xylosoxidans BOA4 was shown to produce up to 17.5 pmol mL−1 of isopentenyladenine. This work is the first report on the influence of bio-stimulants, used to improve salt stress tolerance, on plant PTN levels; BOA4 and/or EI treatments decreased PTN, while increasing cis-zeatin-type and iP cytokinins in tomato, the latter showed an enhanced tolerance to salt stress.
- Bacterial Inoculation and Extracts of Opuntia Rackets or Marine Algae Trigger Distinct Proline Balances in Tomato Salt Stress AlleviationPublication . Rai, Abdelwahab; Santana, Margarida; Maia, Rodrigo Nascimento; Tavares, João; Nabti, Elhafid; Cruz, CristinaHigh salt levels in soil can severely limit plant development and diminish the positive effect of plant-growth-promoting rhizobacteria (PGPR). However, extracts of organisms adapted to high salinity, such as Opuntia ficus-indica (OFI) and Enteromorpha intestinalis (EI), can restore the growth of PGPR. Therefore, we used OFI or EI extracts and their combination with the PGPR Achromobacter xylosoxidans BOA4 to evaluate salt stress relief in tomato (Solanum lycopersicum). The experimental setup consisted of a plant pot trial under greenhouse conditions with 12 treatments: control, irrigation with OFI extract; EI extract; BOA4-inoculated plus OFI extract and BOA4-inoculated plus EI extract under no salinity or salinity conditions (150 mM NaCl). The percentage of germination, and plant’s fresh and dry weight were registered 30 and 46 days after sowing. At 46 days, the ratio between proline and glutamic acid concentration (PR/GA) was determined, expecting high PR/GA ratios in plants more responsive to salt stress since proline is an osmolyte mainly synthesized from glutamate. The results showed that 52% of the control seeds under salt stress germinated, a figure that was increased to 92% in OFI-treated seeds. Tomato plants were shown to be very sensitive to salt stress since the dry weight was ca. one fourth that of the plants grown without salinity. However, EI or BOA4 plus EI stimulated plant biomass by ca. 3 times compared to the control with salt, restoring plant biomass to values comparable to those of control plants grown without salinity. The joint treatments with BOA4 and EI or OFI caused distinct PR/GA levels in plant tissues. An inverse relationship between the sum of relative shoot proline and glutamic acid contents and shoot biomass accumulation was observed, namely in treatments accumulating more biomass under no salinity and salinity conditions. This indicates that the proline/glutamate pathway represents a carbon sink that is needed to fight stress and is competing with the carbon flow used for growth.