Microbe-plant interactions between Streptomyces and model agricultural plants – Hordeum vulgare and Lycopersicon esculentum (Microtom)

  • H. V. Mutenko
  • B. O. Ostash
  • M. Rothballer
  • A. Weiss
  • M. Schmid
  • A. Hartmann
  • V. O. Fedorenko

Abstract

Aim. Microbe-plant interactions (MPI) constitute an important aspect of ecology because of their significant influence on plant’s ability to withstand abiotic stress and infection. In comparison to proteobacteria and bacilli, the roles of streptomycetes in MPI remain poorly studied. Here, we elucidate some aspects of MPI between two model plant species, Hordeum vulgare and Lycopersicon esculentum, and several strains of Streptomyces lividans 1326 and S. ghanaensis ATCC14672. Methods. Microbiology, microscopy and molecular genetics were combined to reveal the MPI. Results. We demonstrate the colonization of H. vulgare and L. esculentum roots by different strains of S. ghanaensis deficient in production of either the antibiotic moenomycin or signaling molecule of the γ-butyrolactone type. The treatment of H. vulgare seeds with S. lividans spores increased the root biomass. Plants treated with 1,4-butyrolactone had no positive influence on plants, at milimolar concentrations this compound inhibited the root and shoot growth of L. esculentum. Conclusions. Roots of two mono- and dicot plants are colonized by Streptomyces; reporter gene uidA is useful to monitor the colonization. Under our experimental conditions the ability to colonize plants by streptomycetes was not affected by the deficiency in antibiotic or butenolide production.

Keywords: Streptomyces ghanaensis, moenomycinA, low-molecular weight signal compounds, root colonization.

References

McCormick J., Flardh K. Signals and regulators that govern Streptomyces development. FEMS Microbiol. Rev. 2012. Vol. 36. P. 206–231. doi: 10.1111/j.1574-6976.2011.00317.x.

Schrey S., Tarkka M. Friends and foes: streptomycetes as modulators of plant disease and symbiosis. Antonie van Leeuw. 2008. Vol. 94. P. 11–19. doi: 10.1007/s10482-008-9241-3.

Kanini G., Katsifas E., Savvides A., Karagouni A. Streptomyces rochei ACTA1551, an indigenous Greek isolate studied as a potential biocontrol agent against Fusarium oxysporum f. sp. lycopersici. BioMed Res. Int. 2013. Vol. 3. P. 1–10. doi: 10.1155/2013/387230.

Li X., Huang P., Wang Q., Xiao L. Staurosporine from the endophytic Streptomyces sp. strain CNS-42 acts as a potential biocontrol agent and growth elicitor in cucumber. Antonie van Leeuw. 2014. Vol. 106. P. 515–525. doi: 10.1007/s10482-014-0220-6.

Kim J., Han J., Lee S., Lee D., Hwang I., Kim B. Disease control effect of strevertenes produced by Streptomyces psammoticus against tomato Fusarium wilt. J Agric Food Chem. 2011. Vol. 59. P. 1893–1899. doi: 10.1021/jf1038585.

Cao P., Liu C., Sun P., Fu X., Wang S., Wu F., Wang X. An endophytic Streptomyces sp. strain DHV3-2 from diseased root as a potential biocontrol agent against Verticillium dahliae and growth elicitor in tomato (Solanum lycopersicum). Antonie van Leeuw. 2016. Vol. 109. P. 1573–1582. doi: 10.1007/s10482-016-0758-6.

Yekkour A., Sabaou N., Zitouni A., Erakhi R., Mathieu F., Lebrihi A. Characterization and antagonistic properties of Strepto-myces strains isolated from Saharan soils, and evaluation of their ability to control seedling blight of barley caused by Fusa-rium culmorum. Lett. Appl. Microbiol. 2012. Vol. 55. P. 427–435. doi: 10.1111/j.1472-765x.2012.03312.x.

Meshke H., Schrempf H. Streptomyces lividans inhibits the proliferation of the fungus Verticillium dahliae on seeds and roots of Arabidopsis thaliana. Microb. Biotechnol. 2010. Vol. 3. P. 428–443. doi: 10.1111/j.1751-7915.2010.00165.x.

Meij A., Willemse J., Schneijderberg M., Geurts R., Raaijmakers J., Wezel G. Inter-and intracellular colonization of Arabidop-sis roots by endo phytic actinobacteria and the impact of plant hormones on their antimicrobial activity. Antonie van Leeuw. 2018. Vol. 111. P. 679–690. doi: 10.1007/s10482-018-1014-z.

Schuhegger R., Ihring A., Gantner S., Bahnweg G. Induction of systemic resistance in tomato by N-acyl-L-homoserine lac-tone-producing rhizosphere bacteria. Plants Cell and Env. 2006. Vol. 29. P. 909–918. doi: 10.1111/j.1365-3040.2005.01471.x.

Willey J., Gaskell A. Morphogenetic signaling molecules of the Streptomycetes. Chem. Rev. 2011. Vol. 111. P. 174–187. doi: 10.1021/cr1000404.

Kitani S., Miyamoto K., Takamatsu S., Herawati E., Iguchi H., Nishitomi K., Uchida M., Nagamitsu T. Avenolide, a Strepto-myces hormone controlling antibiotic production in Streptomyces avermitilis. Proc. Natl. Acad. Sci. USA. 2011. Vol. 108. P. 16410–16415. doi: 10.1073/pnas.1113908108.

Ostash B., Saghatelian A., Walker S. A streamlined metabolic pathway for the biosynthesis of moenomycin. Chem. Biol. 2007. Vol. 14. P. 257–267. doi: 10.101.6/j.chembiol.2007.01.008.

Myronovskyi M., Welle E., Fedorenko V., Luzhetskyy A. Beta-glucuronidase as a sensitive and versatile reporter in actinomy-cetes. Appl. Environ. Microbiol. 2011. Vol. 77. P. 5370–5383. doi: 10.1128/AEM.00434-11.

Makitrynskyy R., Ostash B., Tsypik O., Rebets Y., Doud E., Meredith T., Luzhetskyy A., Bechtold A., Walker S., Fedorenko V. Pleiotropic regulatory genes bldA, adpA and absB are implicated in production of phosphoglycolipid antibiotic moenomy-cin. Open Biol. 2013. Vol. 3. P. 130121. doi: 10.1098/rsob.130121.

Tan G., Bai L., Zhang J. Exogenous 1,4-butyrolactone stimulates A-factor-like cascade and validamycin biosynthesis in Strep-tomyces hygroscopicus 5008. Biotechnol. Bioeng. 2013. Vol. 110. P. 2984–2993. doi: 10.1002/bit.24965.

Rey T., Dumas B. Plenty is no plague: Streptomyces symbiosis with crops. Trends Plants Sci. 2017. Vol. 22. P. 30–37. doi: 10.1016/j.tplants.2016.10.008.

Schikora A., Schenk S., Stein E., Moliton A., Zuccaro A., Kogel K. N-acyl-homoserine lactone confers resistance toward biotrophic and hemibiotrophic pathogens via altered activation of AtMPK61. Plant Physiol. 2011. Vol. 157. P. 1407–1418. doi: 10.1104/pp.111.180604.