PLANT GROWTH-PROMOTING RHIZOBACTERIA AS PLANT BIOSTIMULANTS TO IMPROVE MINERAL NUTRITION AND RESOURCE USE EFFICIENCY

On the other hand, pathogenic bacteria might establish negative interactions at rhizosphere levels, thereby producing toxic metabolites that have detrimental effects on plant growth. Differently, a group of microorganisms, known as Plant Growth-Promoting Rhizobacteria (PGPR), can exert a biostimulant action on plants through different mechanisms. PGPR can protect plants from pathogens, for example by activating plants’ defence systems or by stimulating the synthesis of stress-related compounds. In addition, PGPR can synthesize bioactive compounds, like hormones, which can promote plants growth with a higher accumulation of biomass, both above and below-ground (Crecchio et al., 2018). Indeed, the enhanced growth of the root system induced by PGPR allows plants to explore a higher volume of soil and ensure a higher surface for the interception of mineral nutrients, possibly resulting in an improved mineral nutrition provision. Nonetheless, in the recent decade, several pieces of evidence have highlighted that PGPR might also act on the molecular and biochemical mechanisms underlying nutrient acquisition processes in plants, allowing plants to better exploit the natural resources already present in soil (Pii et al., 2015b, 2015a, 2016).

Iron as a case study

Iron (Fe) is an essential element to plants, and it is fairly abundant on the Earth’s crust; nevertheless, its low bioavailability in soils often represents one of the major constraints to agricultural productivity (Kobayashi and Nishizawa, 2012). To face the issue of acquiring Fe from soils, plants have evolved different strategies (Astolfi et al., 2020; Marschner and Römheld, 1994); dicots and non-graminaceous monocots, for instance, i) acidify the rhizosphere by extruding protons through the activity of plasma membrane H⁺-ATPase, ii) reduce the insoluble Fe^III to the more soluble Fe^II, via the activity of a ferric chelate reductase (FRO), and iii) transport Fe^II into root cells by the iron-regulated transporter 1 (IRT1) (Kobayashi and Nishizawa, 2012). These biochemical activities are strongly upregulated when plants are grown in soils featuring a very scarce Fe availability (Brumbarova et al., 2015), yet this is often not enough to prevent the appearance of Fe deficiency symptoms. Interestingly, several reports have highlighted that the contribution provided by PGPR dwelling in the rhizosphere might be crucial to assuring adequate Fe nutrition to plants (de Santiago et al., 2013; Pii et al., 2015a; Zhang et al., 2009; Zhao et al., 2014).

It was recently demonstrated that the inoculation of Fe deficient cucumber plants, grown in calcareous soils, with the PGPR Azospirillum brasilense led to a significant modification in the qualitative and quantitative pattern of root exudates release that eventually resulted in a quicker recovery from the nutritional disorder (Pii et al., 2015b). These observations further strengthened the idea that PGPR might improve plant mineral nutrition by affecting biochemical and molecular pathways. A deeper investigation of the mechanisms triggered by A. brasilense in Fe starved cucumber plants demonstrated that microorganisms could affect both the growth and architecture of the root system and plants’ ability to absorb Fe (Pii et al., 2016). The assessment of root morphology demonstrated that PGPR were able to enhance root growth, yet differently, according to the plant’s nutritional status: in Fe deficient plants, A. brasilense promoted the elongation of pre-existing lateral roots, while, in the case of Fe sufficient plants, the initiation of new lateral roots was triggered (Figure 1). At the molecular level, inoculated Fe deficient plants upregulated the genes encoding for the plasma membrane H⁺-ATPase and the ferric chelate reductase (FRO) as compared to control plants that allowed a more efficient (4-fold higher rate) Fe uptake (Pii et al., 2016). Interestingly, the inoculation with the PGPR also enhanced the Fe reduction activity in Fe sufficient plants, even though the gene expression analyses suggested that different molecular entities might be activated in this case (Marastoni et al., 2019; Pii et al., 2016). Consistently, genome-wide transcriptomic analyses showed that highly different sets of genes were modulated by the inoculation with the PGPR, depending on plants’ Fe provision, further corroborating that plant response to microbe interaction can be strongly dependent on the whole nutritional status.