Novel Plant-Microbe Rhizosphere Interaction Involving Streptomyces lydicus WYEC108 and the Pea Plant ( Pisum sativum )

Abstract

A previously undescribed plant-microbe interaction between a root-colonizing Streptomyces species, S. lydicus WYEC108, and the legume Pisum sativum is described. The interaction is potentially of great importance to the health and growth in nature of this nodulating legume. The root-colonizing soil actinomycete S. lydicus WYEC108 influences pea root nodulation by increasing root nodulation frequency, possibly at the level of infection by Rhizobium spp. S. lydicus also colonizes and then sporulates within the surface cell layers of the nodules. Colonization leads to an increase in the average size of the nodules that form and improves the vigor of bacteroids within the nodules by enhancing nodular assimilation of iron and possibly other soil nutrients. Bacteroid accumulation of the carbon storage polymer, poly-␤-hydroxybutyrate, is reduced in colonized nodules. Root nodules of peas taken from agricultural fields in the Palouse hills of northern Idaho were also found to be colonized by actinomycete hyphae. We hypothesize that root and nodule colonization is one of several mechanisms by which Streptomyces acts as a naturally occurring plant growth-promoting bacterium in pea and possibly other leguminous plants.Streptomyces lydicus WYEC108 is a root-colonizing actinomycete originally isolated and studied for its properties as an antifungal biocontrol agent. This strain is capable of mycoparasitic colonization of fungal root pathogens and excretion of antifungal metabolites within plant rhizospheres (16,62). Recently, we demonstrated that strain WYEC108 is also a plant growth-promoting bacterium in the absence of fungal pathogen challenge. This may be due to the ability of strain WYEC108 to produce hydroxamate-type siderophores and/or other plant growth-promoting metabolites in the rhizosphere (25). Streptomyces spp. have been previously described as rhizosphere-colonizing bacteria (37, 38), antifungal biocontrol agents useful in controlling fungal root diseases (51), in vitro siderophore producers, and in vitro producers of plant growthpromoting hormones (25). Plant root exudates stimulate rhizosphere growth of actinomycetes that are strongly antagonistic to fungal pathogens, while the actinomycetes utilize root exudates for growth and synthesis of antimicrobial substances (16,62). In addition, actinomycetes synthesize an array of biodegradative enzymes, including chitinases (9, 23, 35), glucanases (18,26,29,32,59,60), peroxidases (48), and other enzymes possibly involved in mycoparasitic activity. Yet, the overall importance, physiological activities, and symbiotic roles of actinomycetes in situ within plant rhizospheres remain little studied at the biochemical or mechanistic levels. We believe that Streptomyces are far more important rhizosphere bacteria than has been generally recognized.Important to the symbiotic relationship between plants and microbes is the acquisition of iron. Although abundant in nature, under aerobic conditions at a neutral or alkaline pH, iron is found in highly insoluble forms not readil...

The genus Micromonospora is widespread in legume root nodules: the example of Lupinus angustifolius

“…Long filamentous and branched structures were also observed in infected cells; however, it was not possible by visual inspection to determine whether these structures were hyphae or pleomorphic bacteriods which, in many cases, enlarge up to seven times from their original bacterial rod-shape size (Oke and Long, 1999;de Maria et al, 2005). Future studies are needed to determine how Micromonospora relates to Bradyrhizobium in a tripartite interaction; a synergistic effect of both bacteria on the plant is possible (Tokala et al, 2002).…”

“…Furthermore, Tokala et al (2002) showed that a Streptomyces strain, WYEC108, was able to colonize the roots of Pisum sativum increasing root nodulation frequency. These authors are of the opinion that these plant-microbe interactions may be common in nature.…”

Rhizosphere microbiome assemblage is affected by plant development

“…Actinobacteria, on the other hand, has recently been associated with disease suppressive soils (Mendes et al, 2011). Streptomyces species, which were significantly more abundant in the vegetative stage of Arabidopsis (Supplementary Figure S4E), are able to increase root nodulation efficiency and promote plant growth of the legume Pisum sativum (Tokala et al, 2002) while simultaneously triggering plant defense in Arabidopsis or apple trees (Cohen et al, 2005;Conn et al, 2008;Lin et al, 2012). On the other hand, Bacteroidetes' role in the rhizosphere has not yet been elucidated but it has been reported that they are important contributors to nutrient turnover in the soil (Yousuf et al, 2012).…”

Evaluation ofStreptomycesspp. for their plant-growth-promotion traits in rice

“…Streptomyces are a group of Gram-positive bacteria, with high G + C content belonging to the order Actinomycetales, which form branched mycelia and hence sometimes been classified as fungi imperfecti. Plant growth promotion potential of Streptomyces was reported on bean (Nassar et al 2003), tomato (El-Tarabily 2008), pea (Tokala et al 2002), wheat (Sadeghi et al 2012) and rice (Gopalakrishnan et al 2012a, b). Streptomyces promote plant growth either by producing indole-3-acetic acid (Aldesuquy et al 1998) or siderophores (Tokala et al 2002).…”

“…Plant growth promotion potential of Streptomyces was reported on bean (Nassar et al 2003), tomato (El-Tarabily 2008), pea (Tokala et al 2002), wheat (Sadeghi et al 2012) and rice (Gopalakrishnan et al 2012a, b). Streptomyces promote plant growth either by producing indole-3-acetic acid (Aldesuquy et al 1998) or siderophores (Tokala et al 2002). Streptomyces has also been extensively studied and used for biocontrol of soil-borne fungal pathogens (Mahadevan and Crawford 1997;Trejo-Estrada et al 1998;Macagnan et al 2008.…”