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Abstract(s)
Wheat crops represent a primary source of energy and nutrients for humans, providing staple food for an estimated 35% of the world population. However, the excessive use of synthetic fertilizers and pesticides has posed serious threaten to wheat production, calling for the need of more sustainable strategies to increase productivity while maintaining the ecological footprint as small as possible. In such circumstances, a great deal of help could be provided by the microbial world associated to plants.
All living plants are holobionts, consisting of a host plant and its associated microbiota. Microbiota includes diverse species of fungi and bacteria that can extend the plant´s ability to adapt to the changing environment, as they can provide nutrients and protect plants against biotic and abiotic stresses. Therefore, exploiting plant-associated microorganisms has gained substantial attention as a promising approach to create “greener” solutions to both increase crop productivity while maintaining the ecological footprint as small as possible and to minimize the use of synthetic fertilizers and pesticides. Inoculation of plants with beneficial plant growth-promoting bacteria (PGPB) causes both genetic and metabolic imprints in the host, leading to a pre-conditioned state known as priming. Priming causes changes in host metabolism, acting as a stress memory to provide plants with more sustained responses to future stresses at low energetic expenses. Furthermore, effects of PGPB inoculation have been shown to be also reflected by changes in the structure and dynamics of the plant-indigenous microbiota, causing transient structural shifts in microbiota diversity and often promoting plant-beneficial members. Although microbiota-modulation events have never been included in the definition of priming, shifts in plant-indigenous communities are believed to be crucial in determining the trajectories of plant growth and health. Herbaspirillum seropedicae is a PGPB isolated from various cereal plants which has the potential for an intimate root association and growth promotion in wheat. However, the mechanisms of action lying behind the growth-promoting effects of this bacterium remain unknown. In particular, there are no evidences regarding its role as driving force for the onset of a primed state both at the holobiont´s metabolome- and microbiota-level. In such framework, the present thesis investigated the priming effect induced by H. seropedicae from a holobiont perspective. First, a multidisciplinary approach combining culturomics, genetics and targeted metabolomics approaches was used to explore putative functional changes in the wheat bacteriota in response to H. seropedicae. This analysis showed that primed plants harbored a different bacterial community, which displayed a different capacity to modulate the levels of key Trp-related metabolites, supporting the idea a mode of action of this PGPB relying on a shift in both the composition and functionality of the wheat indigenous community. Changes in the structure of the endophytic wheat microbiota were then confirmed both by 16S and ITS metabarcoding analyses, and these shifts mirrored a predicted functional diversification, which was manifested by the enrichment of microbial members with potential beneficial functions for plant growth. Furthermore, untargeted metabolomic analyses were employed to explore the alterations in the root metabolome of primed plants. The obtained preliminary results showed that alterations of different metabolites with important roles in plant growth and defense, as well as in plant-microbe and microbe-microbe crosstalk. These metabolome shifts may be related with a preventive/alert state induced by priming, where specific precursor molecules acting at different metabolic steps of the same pathway may preferentially accumulate in the host as long-term memory.
In addition, the priming effect was also studied in wheat-pathogen interactions, where primed plants that were leaf-challenged with the pathogen Pseudomonas syringae showed both reduced oxidative stress and reduced necrotic symptoms. In this scenario, H. seropedicae may increase plant sensitivity to H2O2 signaling in systemic tissues, avoiding its massive accumulation upon pathogen challenge. These systemic effects may be linked not only to the plant oxidative metabolism itself, but also to the shifts in the leaf microbiota of primed plants, where specific members may be better adapted to counteract pathogen multiplication or buffer the disease-related cellular oxidative bursts.
The results obtained throughout the realization of this thesis suggest that priming with H. seropedicae not only has the potential to help plants to respond better to stress, but also to promote an invisible microbial machinery that is potentially beneficial for the host. The highly innovative and multidisciplinary approaches used throughout this thesis contributed to the disclosure of a novel mode of action of H. seropedicae to induce a primed state in the wheat holobiont. Understanding how native microbial communities interact with PGPB could yield important insights into how the plant microbiota can be exploited to create valuable and more eco-friendly solutions for agricultural application, such as biofertilizers and biopesticides.
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Keywords
Holobiont Wheat Priming Herbaspirillum seropedicae