Thaxtomin A-deficient endophytic Streptomyces sp. enhances plant disease resistance to pathogenic Streptomyces scabies

Abstract

Each plant species in nature harbors endophytes, a community of microbes living within host plants without causing any disease symptom. However, the exploitation of endophyte-based phytoprotectants is hampered by the paucity of mechanistic understandings of endophyte-plant interaction. We here reported two endophytic Streptomyces isolates IFB-A02 and IFB-A03 recovered from a stress-tolerant dicotyledonous plant Artemisia annua L. After the determination of their non-pathogenicity at the genomic level and from the toxin (thaxtomin A, TXT) level, the endophytism of both isolates was supported by their successful colonization in planta. Of the two endophytes, IFB-A03 was further studied for the mechanism of endophyte-conferred phytoprotection owing to its plant growth promotion in model eudicot Arabidopsis thaliana. Using the endophyte-Arabidopsis co-cultivation system into which pathogenic Streptomyces scabies was introduced, we demonstrated that IFB-A03 pre-inoculation could activate the salicylic acid (SA)-mediated plant defense responses upon pathogen challenge. Moreover, IFB-A03 was shown to partially rescue the defense deficiency in eds5 (enhanced disease susceptibility 5) Arabidopsis mutants, putatively acting at the upstream of SA accumulation in the defense signaling pathway associated with the systemic acquired resistance (SAR). These data suggest that endophytic Streptomyces sp. IFB-A03 could be a promising candidate for biocontrol agents against S. scabies--a causative pathogen of common scab diseases prevailing in agronomic systems.

Rhizosphere microbiome assemblage is affected by plant development

“…For example, dTDP-glucose 4,6-dehydratase involved in streptomycin biosynthesis is more abundant during plant bolting and flowering. Streptomycin is an antibiotic mainly produced by Streptomyces and it is antagonistic against grampositive and -negative bacteria and has been shown to enhance plant defenses and trigger systemic resistance (Schatz et al, 2005;Conn et al, 2008;Lin et al, 2012). Additionally, we observe that dTDPglucose-4,6-dehydratase positively correlates with the root exudate compound myo-Inositol which increases streptomycin biosynthesis (Majumdar and Kutzner, 1962;Heding, 1964).…”

“…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).…”

Long-Term Induction of Defense Gene Expression in Potato by Pseudomonas sp. LBUM223 and Streptomyces scabies

“…Although few studies on the defense responses induced by S. scabies in potato exist, focusing mostly on responses in individual tubers and not entire plant systems (16), there have been studies performed in A. thaliana plant systems. Interestingly, the inoculation of A. thaliana seedlings with S. scabies, after preinoculation with a nonpathogenic endophytic Streptomyces isolate, also induced an SA-related SAR response (23). Some reports on the effect of thaxtomin A, the phytotoxin responsible for scab symptoms, have also been accomplished in A. thaliana.…”

“…To our knowledge, S. scabies' ability to induce SAR in potato plants has never been studied. However, some reports suggest that S. scabies, or the thaxtomin A it produces, are capable of inducing defense responses in A. thaliana (5,14,15,23).…”

Endophytic Streptomyces in the traditional medicinal plant Arnica montana L.: secondary metabolites and biological activity

“…There is evidence for symbiosis with arbuscular mycorrhizal fungi, but no report exists on a symbiosis with endophytic Streptomyces ). Up to now only a few species of the large plant family of Asteraceae were reported to interact with endophytic Streptomyces, among them Artemisia annua, which is also a plant with known medicinal properties (Sardi et al 1992;Jiménez-Esquilín and Roane 2005;Castillo et al 2007;Lin et al 2012;Tanvir et al 2014).…”