Integrated Metabolomics and Morpho-Biochemical Analyses Reveal a Better Performance of Azospirillum brasilense over Plant-Derived Biostimulants in Counteracting Salt Stress in Tomato

Abstract

Increased soil salinity is one of the main concerns in agriculture and food production, and it negatively affects plant growth and crop productivity. In order to mitigate the adverse effects of salinity stress, plant biostimulants (PBs) have been indicated as a promising approach. Indeed, these products have a beneficial effect on plants by acting on primary and secondary metabolism and by inducing the accumulation of protective molecules against oxidative stress. In this context, the present work is aimed at comparatively investigating the effects of microbial (i.e., Azospirillum brasilense) and plant-derived biostimulants in alleviating salt stress in tomato plants by adopting a multidisciplinary approach. To do so, the morphological and biochemical effects were assessed by analyzing the biomass accumulation and root characteristics, the activity of antioxidant enzymes and osmotic stress protection. Furthermore, modifications in the metabolomic profiles of both leaves and root exudates were also investigated by ultra-high performance liquid chromatography/quadrupole time-of-flight mass spectrometry (UHPLC/QTOF-MS). According to the results, biomass accumulation decreased under high salinity. However, the treatment with A. brasilense considerably improved root architecture and increased root biomass by 156% and 118% in non-saline and saline conditions, respectively. The antioxidant enzymes and proline production were enhanced in salinity stress at different levels according to the biostimulant applied. Moreover, the metabolomic analyses pointed out a wide set of processes being affected by salinity and biostimulant interactions. Crucial compounds belonging to secondary metabolism (phenylpropanoids, alkaloids and other N-containing metabolites, and membrane lipids) and phytohormones (brassinosteroids, cytokinins and methylsalicylate) showed the most pronounced modulation. Overall, our results suggest a better performance of A. brasilense in alleviating high salinity than the vegetal-derived protein hydrolysates herein evaluated.

Changes in Phenolic Profile and Total Phenol and Total Flavonoid Contents of Guadua angustifolia Kunth Plants under Organic and Conventional Fertilization

“…A. brasilense increases the content of phenols and flavonoids in tomato plants under salinity stress conditions, as well as in plants that were not exposed to salinity stress . In contrast, on plants of Coriandrum sativum L. inoculated with Bacillus halotolerans, the content of cinnamic acid derivatives decreased and the inoculation on Cichorium endivia L. showed significantly lower levels of cichoric and caffeoylquinic acids .…”

“…improves the content of phenols, flavonoids, and carotenoids and antioxidant activity in plants of economic and medicinal importance such as Arachis hypogea ( 45 ) and Carthamus tinctorius L. 46 A. brasilense increases the content of phenols and flavonoids in tomato plants under salinity stress conditions, as well as in plants that were not exposed to salinity stress. 47 In contrast, on plants of Coriandrum sativum L. inoculated with Bacillus halotolerans , the content of cinnamic acid derivatives decreased 48 and the inoculation on Cichorium endivia L. showed significantly lower levels of cichoric and caffeoylquinic acids. 49 Changes in phenolic compound levels in plants may be due to specific inoculant–plant interactions, such Rhizobium– rice, Azospirillum –maize, and Azospirillum – Pseudomona s– Glomus –maize.…”

Unravelling the biostimulant activity of a protein hydrolysate in lettuce plants under optimal and low N availability: a multi‐omics approach

“…According to the EU regulation 2019/1009, a plant biostimulant (PB) has been defined as a product that can promote plant growth and health by enhancing either (1) nutrient use efficiency, (2) tolerance to abiotic stress, (3) crop quality traits, (4) availability of nutrients confined in the soil and rhizosphere or a combination of the above. Overall, PBs show a diversified nature, thereby including a wide range of substances like beneficial microorganisms (e.g., mycorrhiza or plant growth promoting rhizobacteria), humic substances, seaweed extracts, and protein hydrolysates (PH) (Calvo et al 2014;Battacharyya et al 2015;Canellas et al 2015;Colla et al 2015Colla et al , 2017bHalpern et al 2015;Pii et al 2015;Rouphael et al 2015;Alzate Zuluaga et al 2022). Among these, PH is composed of a mixture of peptides and free amino acids obtained through the partial hydrolysis, either chemical or enzymatic, of a protein source, deriving from either the animal or plant kingdom (Colla et al 2015(Colla et al , 2017b.…”

“…Among these, PH is composed of a mixture of peptides and free amino acids obtained through the partial hydrolysis, either chemical or enzymatic, of a protein source, deriving from either the animal or plant kingdom (Colla et al 2015(Colla et al , 2017b. Previous studies have assessed that the application of PH-based biostimulants can increase the NUE and the tolerance to abiotic stresses (e.g., salinity, drought and high temperature) in horticultural crops (Calvo et al 2014;Halpern et al 2015;Lucini et al 2015;Colla et al 2017aColla et al , 2017bCarillo et al 2019bCarillo et al , 2019aAlzate Zuluaga et al 2022;Zuluaga et al 2023), albeit the mode of action has not been fully elucidated yet. Several authors have ascribed the positive effects brought about by the administration of PHs to direct and indirect mechanisms, as i) the upregulation of C and N metabolism by the stimulation of key enzymes, ii) the enhancement of the antioxidant defence systems, and iii) the modulation of hormone-like activities, which could, in turn, affect the growth and the biology of the root systems, thereby influencing mineral nutrient uptake/ assimilation and, ultimately, crop productivity (Colla et al 2017b).…”

Screening the maize rhizobiome for consortia that improve Azospirillum brasilense root colonization and plant growth outcomes

“…Azospirillum brasilense is one of the most widely adopted diazotrophs, and it displays versatile C-and N-metabolism. It also promotes plant growth through additional mechanisms, including phytohormone production (Alzate Zuluaga et al, 2022), development of stress tolerance (Pedrosa et al, 2020), siderophore production (Ferreira et al, 2019;Timofeeva et al, 2022), phosphate solubilization (Bargaz et al, 2021), and phytopathogen inhibition (Viejobueno et al, 2021). With this array of benefits, significant effort has been given to understanding the microbial interactions that influence the association and colonization of A. brasilense and other diazotrophic bacteria with non-leguminous maize (Zea mays) crops (Dent and Cocking, 2017;Oliveira et al, 2018;Van Deynze et al, 2018).…”