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

Abstract

Main conclusion Tissue-specific occurrence and formation of endogenous sesquiterpene lactones has been assessed and suggests physiological function as antagonists of auxin-induced plant growth in sunflower. Abstract 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.

Are sesquiterpene lactones the elusive KARRIKIN-INSENSITIVE2 ligand?

“…Our results show that particularly two sunflower STLs, 8-epixanthatin and tomentosin, can bind to the hydrophobic pockets of HaKAI2s with high affinity. Our results are in line with a recent study, showing that these two STLs accumulate in the light-exposed hypocotyls of sunflower (Spring et al 2020 ). This finding sheds light on the effect of STLs in hypocotyl elongation that has been reported for many decades but without conclusive insight in the elusive mechanism underlying this effect.…”

“…To support this hypothesis, we have generated homology models of the sunflower KAI2s (HaKAI2s) and used them for molecular docking studies with STLs. Our results show that particularly two sunflower STLs, 8-epixanthatin and tomentosin, can bind to the hydrophobic pockets of HaKAI2s with high (Spring et al 2020). This finding sheds light on the effect of STLs in hypocotyl elongation that has been reported for many decades but without conclusive insight in the elusive mechanism underlying this effect.…”

“…A recent study showed that the exposure of sunflower cotyledons to blue light results in a fast accumulation (< 2 h) of 8-epixanthatin and tomentosin in the hypocotyl, which continues until reaching a maximum at 72 h (Spring et al 2020 ). The other STLs, dehydrocostus lactone (which is abundantly present in roots) and costunolide, were only present in trace amounts and their concentrations did not change over time.…”

Costunolide Influences Germ Tube Orientation in Sunflower Broomrape – A First Step Toward Understanding Chemotropism

“…The samples tested in the chemotropism bioassays were sunflower root exudate, a methanol extract of sunflower seed oil, costunolide, and GR24. The root exudate and seed oil extract were chosen because they were known to contain four STLs with germination-inducing capacity for O. cumana (Raupp and Spring, 2013) and plant growth-influencing bioactivity (Spring et al, 2020). Costunolide was selected as a model compound of the four STLs because of its commercial availability in sufficient amounts for the experiments, whereas 8-epixanthatin and tomentosin would have required laborious cultivation of suitable source plants (e.g., Xanthium strumarium L.), compound extraction, and purification.…”

“…They are produced in the early stages of seedling development (Spring et al, 2020), are released with root exudates, effectively induce germination of O. cumana (Joel et al, 2011;Raupp and Spring, 2013), inhibit auxin-induced elongation growth (Spring and Hager, 1982), impede polar auxin transport in plants (Ueda et al, 2013), and induce the phototropic (and possibly gravitropic) curvature of sunflower hypocotyls (Yokotani-Tomita et al, 1999;Spring et al, 2020). The four sunflower STLs, dehydrocostus lactone, costunolide, 8-epixanthatin, and tomentosin, present in leaves, stems, and roots of seedlings as well as in sunflower seeds and oil (Spring et al, 2020;Spring, 2021) not only induce the germination of O. cumana but simultaneously have the potential to trigger the host-directed growth of the parasitic germ tube observable in rhizotron experiments (Figure 1). It was the aim of this study to test this assumption by establishing a bioassay suitable for observing the germination of seeds and visualizing germ tube development at different distances from the source of target compounds.…”