Priming of Plant Growth Promotion by Volatiles of Root-Associated Microbacterium spp

Abstract

Volatile compounds produced by plant-associated microorganisms represent a diverse resource to promote plant growth and health. Here, we investigated the effect of volatiles from root-associated species on plant growth and development. Volatiles of eight strains induced significant increases in shoot and root biomass of but differed in their effects on root architecture. strain EC8 also enhanced root and shoot biomass of lettuce and tomato. Biomass increases were also observed for plants exposed only briefly to volatiles from EC8 prior to transplantation of the seedlings to soil. These results indicate that volatiles from EC8 can prime plants for growth promotion without direct and prolonged contact. We further showed that the induction of plant growth promotion is tissue specific; that is, exposure of roots to volatiles from EC8 led to an increase in plant biomass, whereas shoot exposure resulted in no or less growth promotion. Gas chromatography-quadrupole time of flight mass spectometry (GC-QTOF-MS) analysis revealed that EC8 produces a wide array of sulfur-containing compounds, as well as ketones. Bioassays with synthetic sulfur volatile compounds revealed that the plant growth response to dimethyl trisulfide was concentration-dependent, with a significant increase in shoot weight at 1 μM and negative effects on plant biomass at concentrations higher than 1 mM. Genome-wide transcriptome analysis of volatile-exposed seedlings showed upregulation of genes involved in assimilation and transport of sulfate and nitrate. Collectively, these results show that root-associated primes plants, via the roots, for growth promotion, most likely via modulation of sulfur and nitrogen metabolism. In the past decade, various studies have described the effects of microbial volatiles on other (micro)organisms , but their broad-spectrum activity and the mechanisms underlying volatile-mediated plant growth promotion have not been addressed in detail. Here, we revealed that volatiles from root-associated bacteria of the genus can enhance the growth of different plant species and can prime plants for growth promotion without direct and prolonged contact between the bacterium and the plant. Collectively, these results provide new opportunities for sustainable agriculture and horticulture by exposing roots of plants only briefly to a specific blend of microbial volatile compounds prior to transplantation of the seedlings to the greenhouse or field. This strategy has no need for large-scale introduction or root colonization and survival of the microbial inoculant.

Secondary Metabolites From Halotolerant Plant Growth Promoting Rhizobacteria for Ameliorating Salinity Stress in Plants

“…The study revealed that even a brief exposure of bacterial VOCs also stimulated plant growth suggesting that these can be used to prime crops without direct and prolonged exposure of plants to bacteria. Moreover, it was also demonstrated that the VOC mediated plant growth promotion was tissue specific and showed biomass increment only in plants exposed to volatiles via roots (Cordovez et al, 2018). Two bacterial volatiles, 4-nitroguaiacol, and quinoline produced by salt-tolerant Pseudomonas simiae were reported to induce soybean growth under 150 mM salt stress (Vaishnav et al, 2016).…”

Fungal volatiles influence plant defence against above‐ground and below‐ground herbivory

“…Remarkably, without direct physical contact with plants, micro‐organisms, such as fungi and bacteria, can also affect plant growth and defence through the emission of volatile organic and inorganic compounds (Kanchiswamy, Malnoy, & Maffei, 2015; Piechulla, Lemfack, & Kai, 2017; Tyagi, Mulla, Lee, Chae, & Shukla, 2018). Volatiles emitted by pathogenic and beneficial micro‐organisms can promote plant growth (Casarrubia et al., 2016; Cordovez et al., 2018; Fincheira & Quiroz, 2018; Moisan et al., 2019), and accelerate plant development (Moisan et al., 2019; Sánchez‐López et al., 2016), for instance by increasing nutrient uptake (Liu & Zhang, 2015) or by altering phytohormone homoeostasis (Bailly & Weisskopf, 2012; Zhang et al., 2007). Microbial volatiles can also enhance plant resistance to fungal, bacterial or oomycete pathogens (Farag, Zhang, & Ryu, 2013; Jain, Varma, Tuteja, & Choudhary, 2017; Kottb, Gigolashvili, Großkinsky, & Piechulla, 2015) and to insect herbivores (Aziz et al., 2016; Cordovez et al., 2017; Moisan et al., 2019).…”

Volatiles from the fungal phytopathogen Penicillium aurantiogriseum modulate root metabolism and architecture through proteome resetting

“…In the precolonization phase, before direct contact with plants occurs, beneficial bacteria and fungi emit diffusible substances (e.g., carbohydrates, proteins, fatty acids, flavonols, organic acids, amino acids and hormones) that cause massive lateral root (LR) formation and enhanced root hair (RH) growth, thus improving the root's capacity to explore for water and minerals and predisposing plants to microbial colonisation and infection (Contreras‐Cornejo, Macías‐Rodríguez, Cortés‐Penagos, & López‐Bucio, 2009; López‐Bucio et al, 2007). These microorganisms also emit a large number of volatile compounds (VCs) with molecular masses of less than 300 Da that promote growth and photosynthesis, induce systemic drought tolerance, improve nutrient acquisition, and modulate RSA in both host and non‐host plants (Cho et al, 2008; Cordovez et al, 2018; Ditengou et al, 2015; Gutiérrez‐Luna et al, 2010; Ryu et al, 2003; Zhang et al, 2009, 2010). Recent studies have shown that this capacity is not restricted to beneficial microbes; it also extends to phytopathogens and microbes that do not normally interact mutualistically with plants (Cordovez et al, 2017; García‐Gómez et al, 2019; Li et al, 2018; Moisan et al, 2019; Sánchez‐López, Baslam, et al, 2016).…”

“…RSA modulation by microbial VCs has frequently been associated with lipophilic carbon‐based compounds, which are known as volatile organic compounds (VOCs) (Bitas et al, 2015; Cordovez et al, 2018; Ditengou et al, 2015; Garnica‐Vergara et al, 2016; Gutiérrez‐Luna et al, 2010; Splivallo, Fischer, Göbel, Feussner, & Karlovsky, 2009; Zhang et al, 2007, 2008). In addition to VOCs, microorganisms also release a limited number of volatile inorganic compounds (VICs) with molecular masses of less than 45 Da such as hydrogen sulfide (H 2 S), molecular hydrogen, nitric oxide (NO), nitrogen dioxide, nitrous oxide and carbon monoxide (CO) (García‐Gómez et al, 2019; Nandi & Sengupta, 1998; Shatalin, Shatalina, Mironov, & Nudler, 2011).…”

“…To date, the majority of studies on the root response to complex mixtures of microbial VCs have been conducted using beneficial microorganisms and focused mainly on analyses of reporters for auxin‐inducible gene expression, RSA adjustments in ethylene and auxin transport/signalling mutants, transcriptome changes in roots of VC‐exposed plants and identification of bioactive microbial VOCs (Bailly et al, 2014; Camarena‐Pozos, Flores‐Núñez, López, López‐Bucio, & Partida‐Martínez, 2019; Cordovez et al, 2018; Ditengou et al, 2015; Garnica‐Vergara et al, 2016; Splivallo et al, 2009; Zhang et al, 2007). These studies have shown that RSA modulation promoted by VCs emitted by beneficial microorganisms is associated with changes in the root transcriptome, and involves processes wherein auxin, ethylene and ROS play important roles.…”