Decoupling of Plant Growth and Accumulation of Biologically Active Compounds in Leaves, Roots, and Root Exudates of Hypericum perforatum L. by the Combination of Jasmonate and Far-Red Lighting

Abstract

The plant hormone jasmonic acid (JA) fine tunes the growth–defense dilemma by inhibiting plant growth and stimulating the accumulation of secondary compounds. We investigated the interactions between JA and phytochrome B signaling on growth and the accumulation of selected secondary metabolites in Hypericum perforatum L., a medically important plant, by spraying plants with methyl jasmonate (MeJA) and by adding far-red (FR) lighting. MeJA inhibited plant growth, decreased fructose concentration, and enhanced the accumulation of most secondary metabolites. FR enhanced plant growth and starch accumulation and did not decrease the accumulation of most secondary metabolites. MeJA and FR acted mostly independently with no observable interactions on plant growth or secondary metabolite levels. The accumulation of different compounds (e.g., hypericin, flavonols, flavan-3-ols, and phenolic acid) in shoots, roots, and root exudates showed different responses to the two treatments. These findings indicate that the relationship between growth and secondary compound accumulation is specific and depends on the classes of compounds and/or their organ location. The combined application of MeJA and FR enhanced the accumulation of most secondary compounds without compromising plant growth. Thus, the negative correlations between biomass and the content of secondary compounds predicted by the growth-defense dilemma were overcome.

The Influence of Exogenous Jasmonic Acid on the Biosynthesis of Steroids and Triterpenoids in Calendula officinalis Plants and Hairy Root Culture

“…However, various reports have indicated that plant defense response activation is often associated with growth inhibition [ 28 , 29 , 30 , 31 ]. Even though it remains unclear how growth rate is coupled with metabolic changes during jasmonate-induced defense mechanisms, this phenomenon has been reported for many plant species, such as sunflower ( Helianthus annuus ), tomato ( Solanum lycopersicum ), soybean ( Glycine max ), rice ( Oryza sativa ), and Hypericum perforatum [ 32 , 33 , 34 ]. In this C. officinalis study, growth inhibition upon jasmonic acid elicitation was observed in both hairy root cultures and pot plants.…”

Genome-Wide Identification of CYP72A Gene Family and Expression Patterns Related to Jasmonic Acid Treatment and Steroidal Saponin Accumulation in Dioscorea zingiberensis

“…D. zingiberensis seeds were cultivated in an environmentally controlled greenhouse with 26 ± 2 °C and 16 h light/day. According to the manufacturer's instruction and previous research, jasmonic acid (JA, Macklin, 98%) was dissolved in 80% ethanol and diluted in 1/2 Hoagland solution to obtain 25, 50, 100 and 200 µmol/L solutions [40,41]. Ethanol was diluted in 1/2 Hoagland solution and used as a control solution.…”

Light exposure of roots in aeroponics enhances the accumulation of phytochemicals in aboveground parts of the medicinal plants Artemisia annua and Hypericum perforatum

“…Indications that both enhanced accumulation of secondary compounds and efficient plant growth are possible simultaneously have come from experiments with Arabidopsis in which plant growth and the accumulation of secondary compounds were decoupled by the simultaneous activation of jasmonic acid (JA) signaling and deactivation of phytochrome B signaling pathways (Campos et al, 2016). Our previous investigation with Hypericum perforatum also supported the decoupling of growth and accumulation of secondary compounds by simultaneous activation of JA and deactivation of the phytochrome signaling pathways, respectively, as we saw a significant enhancement in the yield of pharmacologically active compounds by these treatments (Paponov et al, 2021a). Whether the application of other stress conditions or elicitors can facilitate this enhanced accumulation of secondary compounds without compromising plant growth is unknown and requires further investigation.…”