Novel insights into plant-endophyte communication: maytansine as an example

Studies on microbe-host interactions in plant and animal systems aimed at understanding the role of these associations and their utility in pharmaceutical and agricultural sectors are gaining impetus [1]. Several recent studies have lent evidence to the fact that certain so-called “plant metabolites” are actually biosynthesized by associated endophytic microorganisms [2,3]. Given the central role of chemical crosstalk in plants and associated endophytes [see Figure (A)], it is essential to unravel the factors that affect the nature, distribution and amount of “communication” molecules at the plant-microbe and microbe-microbe interface to gain fundamental insights on endophytic biosynthetic pathways in distinct ecological niches.

We recently investigated biosynthesis of the important anticancer and cytotoxic compound maytansine in Celastraceae plants in order to elucidate its actual producer(s), which has been an open question since its discovery in the 1970 s. We showed that maytansine is actually a biosynthetic product of root-associated endophytic bacterial community in Putterlickia verrucosa and Putterlickia retrospinosa plants [4]. This extremely interesting outcome provided the scientific basis to investigate the actual producer(s) responsible for maytansine biosynthesis in Maytenus plants. Endophytic communities harboring different tissues of Maytenus serrata originating from Cameroon were investigated using a combination of bioanalytical tools such as HPLC-HRMSⁿ and MALDI-MSI, and targeted genome mining techniques to elucidate the source and sites of maytansine biosynthesis. We proved that the biosynthesis of maytansine in M. serrata is shared between the endophytic bacterial community colonizing the stem and the host plant containing non-culturable cryptic endophytes [see Figure (B)] [5]. Our work demonstrates that maytansine is biosynthesized in M. serrata only when the host plant joins forces with its selected and very eco-specific endophytic bacterial community.

Acknowledgements: This work was funded by the “Welcome to Africa” initiative of the German Federal Ministry of Education and Research (BMBF) and German Academic Exchange Service (DAAD). The Ministry of Innovation, Science, Research and Technology of the State of North Rhine-Westphalia, Germany, and the German Research Foundation (DFG) are thankfully acknowledged for granting a high-resolution mass spectrometer.

Keywords: Endophytes, endophytic bacterial community, cross-species biosynthesis, maytansine, plant-endophyte communication.

References:

[1] Kusari S, Hertweck C, Spiteller M. Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 2012; 19: 792 – 798

[2] Kusari S, Spiteller M. Are we ready for industrial production of bioactive plant secondary metabolites utilizing endophytes? Nat Prod Rep 2011; 28: 1203 – 1207

[3] Kusari S, Spiteller, M. Metabolomics of endophytic fungi producing associated plant secondary metabolites: progress, challenges and opportunities. In: Roessner U, editor. Metabolomics. Rijeka, Croatia: InTech, 2012; 241 – 266

[4] Kusari S, Lamshöft M, Kusari P, Gottfried S, Zühlke S, Louven K, Hentschel U, Kayser O, Spiteller M. Endophytes are hidden producers of maytansine in Putterlickia roots. J Nat Prod 2014; 77: 2577 – 2584

[5] Kusari P, Kusari S, Eckelmann D, Zühlke S, Kayser O, Spiteller M. Cross-species biosynthesis of maytansine in Maytenus serrata. RSC Adv 2016; 6: 10011 – 10016