Melatonin-Producing Endophytic Bacteria from Grapevine Roots Promote the Abiotic Stress-Induced Production of Endogenous Melatonin in Their Hosts.

Jian Jiao,Yanlin Liu,Sha Chen,Yaner Ma,Chunlong Yuan,Yuyang Song,Yi Qin,Chonghuai Liu

doi:10.3389/fpls.2016.01387

Abstract

Endophytes form symbiotic relationships with plants and constitute an important source of phytohormones and bioactive secondary metabolites for their hosts. To date, most studies of endophytes have focused on the influence of these microorganisms on plant growth and physiology and their role in plant defenses against biotic and abiotic stressors; however, to the best of our knowledge, the ability of endophytes to produce melatonin has not been reported. In the present study, we isolated and identified root-dwelling bacteria from three grapevine varieties and found that, when cultured under laboratory conditions, some of the bacteria strains secreted melatonin and tryptophan-ethyl ester. The endophytic bacterium Bacillus amyloliquefaciens SB-9 exhibited the highest level of in vitro melatonin secretion and also produced three intermediates of the melatonin biosynthesis pathway: 5-hydroxytryptophan, serotonin, and N-acetylserotonin. After B. amyloliquefaciens SB-9 colonization, the plantlets exhibited increased plant growth. Additionally, we found that, in grapevine plantlets exposed to salt or drought stress, colonization by B. amyloliquefaciens SB-9 increased the upregulation of melatonin synthesis, as well as that of its intermediates, but reduced the upregulation of grapevine tryptophan decarboxylase genes (VvTDCs) and a serotonin N-acetyltransferase gene (VvSNAT) transcription, when compared to the un-inoculated control. Colonization by B. amyloliquefaciens SB-9 was also able to counteract the adverse effects of salt- and drought-induced stress by reducing the production of malondialdehyde and reactive oxygen species (H2O2 and O2-) in roots. Therefore, our findings demonstrate the occurrence of melatonin biosynthesis in endophytic bacteria and provide evidence for a novel form of communication between beneficial endophytes and host plants via melatonin.

Highlights

Melatonin (N-acetyl-5-methoxytryptamine) was first isolated from the bovine pineal gland (Lerner et al, 1958) and is recognized as ubiquitous among living organisms, including humans, animals, plants, bacteria, fungi, and macroalgae (Tilden et al, 1997; Rodriguez-Naranjo et al, 2012; Tan et al, 2012)
This conjecture is based on observations that (i) melatonin has been identified in microorganisms, such as aerobic photosynthetic bacteria (Tilden et al, 1997), recombinant E. coli (Byeon and Back, 2016) and some fungi (Manchester et al, 1995; Hardeland and Poeggeler, 2003); (ii) melatonin biosynthesis is likely to be evolutionarily conserved (Tan et al, 2014); (iii) the cellular machinery for melatonin synthesis in eukaryotes may have been inherited from bacteria, as a result of endosymbiosis (Tan et al, 2013); and (iv) bioinformatic analyses has revealed that enzymes involving in melatonin synthesis occur in bacterial genomes (Pavlicek et al, 2010; Falcón et al, 2014)
Melatonin was previously identified in the primitive photosynthetic bacterium Erythrobacter longus (Tilden et al, 1997) and in the gram-negative bacterium Escherichia coli (Hardeland and Poeggeler, 2003); few other bacteria are known to produce melatonin

Summary

Introduction

Melatonin (N-acetyl-5-methoxytryptamine) was first isolated from the bovine pineal gland (Lerner et al, 1958) and is recognized as ubiquitous among living organisms, including humans, animals, plants, bacteria, fungi, and macroalgae (Tilden et al, 1997; Rodriguez-Naranjo et al, 2012; Tan et al, 2012). For example, have been shown to enter and proliferate within plant roots (Hardoim et al, 2008), and in grapevines, naturally occurring endophytes have been isolated from roots, stems, leaves, and various reproductive tissues (e.g., inflorescences, seeds, and fruits; Compant et al, 2011) These symbiotic organisms are important in defending their hosts against phytopathogens (Lindow and Brandl, 2003; West et al, 2010) and may promote the growth of their host plants via nitrogen fixation (Elbeltagy et al, 2001), phosphorus solubilization (Richardson et al, 2009), and the enhancement of plant hormones levels (Ali et al, 2009). To the best of our knowledge, the ability of endophytic bacteria to produce melatonin has not been reported, and the synthetic pathway of melatonin in heterotrophic bacteria remains to be elucidated

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Conclusion