Rhizosphere ecology of lumichrome and riboflavin, two bacterial signal molecules eliciting developmental changes in plants

Abstract

Lumichrome and riboflavin are novel molecules from rhizobial exudates that stimulate plant growth. Reported studies have revealed major developmental changes elicited by lumichrome at very low nanomolar concentrations (5 nM) in plants, which include early initiation of trifoliate leaves, expansion of unifoliate and trifoliate leaves, increased stem elongation and leaf area, and consequently greater biomass accumulation in monocots and dicots. But higher lumichrome concentration (50 nM) depressed root development and reduced growth of unifoliate and second trifoliate leaves. While the mechanisms remain unknown, it is possible that lumichrome released by rhizobia induced the biosynthesis of classical phytohormones that caused the observed developmental changes in plants. We also showed in earlier studies that applying either 10 nM lumichrome, 10 nM ABA, or 10 ml of infective rhizobial cells (0.2 OD600) to roots of monocots and dicots for 44 h produced identical effects, which included decreased stomatal conductance and leaf transpiration in Bambara groundnut, soybean, and maize, increased stomatal conductance and transpiration in cowpea and lupin, and elevated root respiration in maize (19% by rhizobia and 20% by lumichrome). Greater extracellular exudation of lumichrome, riboflavin and indole acetic acid by N2-fixing rhizobia over non-fixing bacteria is perceived to be an indication of their role as symbiotic signals. This is evidenced by the increased concentration of lumichrome and riboflavin in the xylem sap of cowpea and soybean plants inoculated with infective rhizobia. In fact, greater xylem concentration of lumichrome in soybean and its correspondingly increased accumulation in leaves was found to result in dramatic developmental changes than in cowpea. Furthermore, lumichrome and riboflavin secreted by soil rhizobia are also known to function as (i) ecological cues for sensing environmental stress, (ii) growth factors for microbes, plants, and humans, (iii) signals for stomatal functioning in land plants, and (iv) protectants/elicitors of plant defense. The fact that exogenous application of ABA to plant roots caused the same effect as lumichrome on leaf stomatal functioning suggests molecular cross-talk in plant response to environmental stimuli.

The Functional Potential of the Rhizospheric Microbiome of an Invasive Tree Species, Acacia dealbata

“…The potential for production of soluble vitamins and antibiotics detected in the rhizosphere metagenomes and genomes of Bradyrhizobium, Sphaerobacter, Geodermatophilus and Kribbela may also be important in the context of plant invasions [62,70]. Soluble vitamins show the potential to protect plants against phytopathogens [71,72], to antagonize the effects of antioxidants (e.g., singlet oxygen species) [73,74] and to act as cofactors in metabolic reactions [75,76]. Recently, pyridoxine (vitamin B6) was shown to influence nitrogen balance in plants [77], an effect which can directly impact on the rate of plant development and overall plant fitness.…”

Characterizing the ecology of coral reef microorganisms across different scales within the Caribbean

“…Metabolites are organic molecules produced by all living organisms. They constitute essential building blocks of proteins (amino acids) and DNA and RNA biomolecules (nucleosides and amino sugars), are involved in essential metabolic processes (metabolic intermediates and vitamins), and can even be used by microorganisms to communicate via quorum sensing (Rajamani et al 2008;Johnson et al 2016) as well as establish microbial symbioses (Dakora et al 2015). Metabolomics is the study of metabolites using nuclear magnetic resonance spectroscopy (NMR) or mass spectrometry (MS) coupled with chromatography (Riekeberg and Powers 2017).…”

“…Within the cell, riboflavin (vitamin B2) is a required precursor for cofactors used in oxidative metabolism (Abbas and Sibirny 2011;Gutierrez-Preciado et al 2015). Extracellularly, riboflavin can also be used by bacteria as a quorum-sensing (Rajamani et al 2008), electron-transfer (Marsili et al 2008), and signal molecule in plant-microbe systems (Dakora et al 2015).…”

Increased algicidal activity of Aeromonas veronii in response to Microcystis aeruginosa: interspecies crosstalk and secondary metabolites synergism

“…Although, it has a different structure then N-acyl homoserine lactones implicated in bacterial quorum sensing, it was found that it can activate, with up to 40% effectiveness, the bacterial receptor LasR, by entering the same active site in the protein as the signal molecule 3-oxo-C12-HSL (Rajamani et al, 2008). Lumichrome also affects the development of plants (Pholo et al, 2018) by an unknown mechanism that resembles the plant hormone abscisic acid (Dakora et al, 2015).…”