Bidirectional Secretions from Glandular Trichomes of Pyrethrum Enable Immunization of Seedlings

Abstract

Glandular trichomes are currently known only to store mono-and sesquiterpene compounds in the subcuticular cavity just above the apical cells of trichomes or emit them into the headspace. We demonstrate that basipetal secretions can also occur, by addressing the organization of the biosynthesis and storage of pyrethrins in pyrethrum (Tanacetum cinerariifolium) flowers. Pyrethrum produces a diverse array of pyrethrins and sesquiterpene lactones for plant defense. The highest concentrations accumulate in the flower achenes, which are densely covered by glandular trichomes. The trichomes of mature achenes contain sesquiterpene lactones and other secondary metabolites, but no pyrethrins. However, during achene maturation, the key pyrethrin biosynthetic pathway enzyme chrysanthemyl diphosphate synthase is expressed only in glandular trichomes. We show evidence that chrysanthemic acid is translocated from trichomes to pericarp, where it is esterified into pyrethrins that accumulate in intercellular spaces. During seed maturation, pyrethrins are then absorbed by the embryo, and during seed germination, the embryo-stored pyrethrins are recruited by seedling tissues, which, for lack of trichomes, cannot produce pyrethrins themselves. The findings demonstrate that plant glandular trichomes can selectively secrete in a basipetal direction monoterpenoids, which can reach distant tissues, participate in chemical conversions, and immunize seedlings against insects and fungi.

Coexpression Analysis Identifies Two Oxidoreductases Involved in the Biosynthesis of the Monoterpene Acid Moiety of Natural Pyrethrin Insecticides in Tanacetum cinerariifolium

“…2A) were determined by analysis of methyl tert-butyl ether (MTBE)-extracted macerated tissues by gas chromatography-mass spectrometry (GC-MS). As observed previously (Kikuta et al, 2012;Ramirez et al, 2012), pyrethrin content in flowers increased as they matured (Fig. 2B), and leaves contained negligible amounts of pyrethrins compared with the amounts observed in flowers.…”

Chrysanthemyl Diphosphate Synthase Operates in Planta as a Bifunctional Enzyme with Chrysanthemol Synthase Activity

“…CDS has been reported to catalyze the first committed step of pyrethrin biosynthesis by joining two molecules of DMAPP to produce CPP (8), but the recently evolved enzyme also has roles in other composite plant species that do not produce pyrethrins (12,13). Interestingly, our in vitro and in vivo results demonstrate that CDS also catalyzes the subsequent conversion of CPP to chry- santhemol, which furthers our understanding of the monoterpene branch of pyrethrin biosynthesis that occurs in pyrethrum glandular trichomes (9).…”

“…The gene responsible for this step has been cloned, and the recombinant enzyme has been characterized as chrysanthemyl diphosphate synthase (CDS, EC 2.5.1.67) (8). The genes and enzymes involved in the next steps, converting CPP into the monoterpene alcohol, chrysanthemol, and the further oxidation to chrysanthemic acid, have not been identified yet, but, recently, the reactions have been shown to occur in the glandular trichomes (9). The final step of the esterification of chrysanthemic acid with one of the lipid alcohols is performed by a recently cloned GDSL lipase from pyrethrum.…”

“…The final step of the esterification of chrysanthemic acid with one of the lipid alcohols is performed by a recently cloned GDSL lipase from pyrethrum. This enzyme transfers the chrysanthemoyl group from the CoA thioester to pyrethrolone to produce pyrethrin I but does so in the pericarp of the seeds and not in the glandular trichomes (9,10 CDS, the enzyme catalyzing the first pathway-specific step, evolved from farnesyl diphosphate synthase (FDS) (8,11,12). It takes two molecules of DMAPP as substrate to produce CPP as major product and lavandulyl diphosphate (LPP) as minor product (Fig.…”

Cell Wall Maturation of Arabidopsis Trichomes Is Dependent on Exocyst Subunit EXO70H4 and Involves Callose Deposition

“…Bars = 20 mm. glandular trichomes of other species, which also usually have cell wall domains specialized for phytochemical deposition (Turner and Croteau, 2004;Ramirez et al, 2012). Heavy-metal stress has been shown previously to up-regulate the secretory pathway genes in O. sativa, including EXO70FX14 and EXO70FX15, which were induced by the copper stress.…”