Spatial and developmental synthesis of endogenous sesquiterpene lactones supports function in growth regulation of sunflower

Otmar Spring,Carolin Meier,Nathalie D. Lackus,Maximilian Frey,Katharina Schmauder,Jan Wellhausen,Lisa V. Smith,Jasmin Schreiner

doi:10.1007/s00425-020-03409-y

Abstract

Main conclusionTissue-specific occurrence and formation of endogenous sesquiterpene lactones has been assessed and suggests physiological function as antagonists of auxin-induced plant growth in sunflower.Sunflower, Helianthus annuus, accumulate high concentrations of bioactive sesquiterpene lactones (STL) in glandular trichomes, but in addition, structurally different STL occur in only trace amounts in the inner tissues. The spatial and temporal production of these endogenous STL during early phases of plant development is widely unknown and their physiological function as putative natural growth regulators is yet speculative. By means of HPLC and MS analysis it was shown that costunolide, dehydrocostuslactone, 8-epixanthatin and tomentosin are already present in dry seeds and can be extracted in low amounts from cotyledons, hypocotyls and roots of seedlings during the first days after germination. Semi-quantitative and RT-qPCR experiments with genes of the key enzymes of two independent routes of the endogenous STL biosynthesis confirmed the early and individual expression in these organs and revealed a gradual down regulation during the first 72–96 h after germination. Light irradiation of the plants led to a fast, but transient increase of STL in parts of the hypocotyl which correlated with growth retardation of the stem. One-sided external application of costunolide on hypocotyls conferred reduced growth of the treated side, thus resulting in the curving of the stem towards the side of the application. This indicates the inhibiting effects of STL on plant growth. The putative function of endogenous STL in sunflower as antagonists of auxin in growth processes is discussed.

Highlights

For a long time, sesquiterpene lactones (STL) of sunflower Helianthus annuus L. were thought to be only produced and stored in trichomes of leaves or flowers (Spring et al 1985, 1987, 1989a) with the function to protect the plant against predators (Spring et al 1989b; Mullin et al 1991)
Sunflower seedlings, germinated in darkness for 48 h and raised up to 192 h in hydroponic culture with a 14 h light period per day were analyzed for the presence of STL in different plant organs
While 8-epixanthatin dominated in cotyledons, tomentosin concentrations were highest in hypocotyls and dehydrocostuslactone reached highest amounts in roots

Summary

Introduction

Sesquiterpene lactones (STL) of sunflower Helianthus annuus L. were thought to be only produced and stored in trichomes of leaves or flowers (Spring et al 1985, 1987, 1989a) with the function to protect the plant against predators (Spring et al 1989b; Mullin et al 1991). In the late 1990s a first report on the presence of 8-epixanthatin (8-EPI), a STL of the xanthanolide type, in extracts of sunflower hypocotyls was published (YokotaniTomita et al 1997). The fast accumulation of 8-epixanthatin after blue light irradiation and the inhibition of elongation growth upon unilateral external application on hypocotyls suggested a functional role of the compound in growth regulation (Yokotani-Tomita et al 1999). The much lower concentrations of these endogenous STL (nM to low μM) compared to the externally deposited STL in trichomes (mM concentrations) makes them less suitable as toxic antifeedants, but rather suggests an internal physiological function of these metabolites with an independently regulated pathway (Padilla-Gonzalez et al 2016)

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Results

Conclusion