The development of type VI glandular trichomes in the cultivated tomato Solanum lycopersicum and a related wild species S. habrochaites

Abstract

BackgroundType VI glandular trichomes represent the most abundant trichome type on leaves and stems of tomato plants and significantly contribute to herbivore resistance, particularly in the wild species. Despite this, their development has been poorly studied so far. The goal of this study is to fill this gap. Using a variety of cell imaging techniques, a detailed record of the anatomy and developmental stages of type VI trichomes in the cultivated tomato (Solanum lycopersicum) and in a related wild species (S. habrochaites) is provided.ResultsIn both species, the development of these structures follows a highly reproducible cell division pattern. The two species differ in the shape of the trichome head which is round in S. habrochaites and like a four-leaf clover in S. lycopersicum, correlating with the presence of a large intercellular cavity in S. habrochaites where the produced metabolites accumulate. In both species, the junction between the intermediate cell and the four glandular cells constitute a breaking point facilitating the decapitation of the trichome and thereby the quick release of the metabolites. A strongly auto-fluorescent compound transiently accumulates in the early stages of development suggesting a potential role in the differentiation process. Finally, immuno-labelling with antibodies recognizing specific cell wall components indicate a key role of pectin and arabinogalactan components in the differentiation of type VI trichomes.ConclusionsOur observations explain the adaptive morphologies of type VI trichomes for metabolite storage and release and provide a framework for further studies of these important metabolic cellular factories. This is required to better exploit their potential, in particular for the breeding of pest resistance in tomato.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0678-z) contains supplementary material, which is available to authorized users.

Plant Glandular Trichomes: Natural Cell Factories of High Biotechnological Interest

“…We chose not to review the development of trichomes in Arabidopsis, as this has been thoroughly reviewed (Balkunde et al, 2010;An et al, 2011;Tominaga-Wada et al, 2011;Pattanaik et al, 2014;Matías-Hernández et al, 2016). Unlike the situation of Arabidopsis, which contains a single type of unicellular, nonglandular trichome, our understanding of the molecular genetic aspects of glandular trichome development is still in its infancy but currently improving due to recent progress in omics and genomeediting technologies as well as to a growing focus from several research teams to characterize this process in different plant species (Li et al, 2004;Dai et al, 2010;Bosch et al, 2014;Bergau et al, 2015;Liu et al, 2016). The (draft) genome sequences of a number of plant species with glandular trichomes are now available.…”

“…Indeed, glandular trichome initiation and differentiation occur at different times in different locations within a single leaf. Therefore, even very young leaves contain a trichome population of mixed developmental stages (Bergau et al, 2015). Given the way most EST resources were generated up to now, the expression of genes playing a role in early developmental steps may be, in the best case, underestimated or, in the worst case, even not detected.…”

“…The development of multicellular glandular trichomes proceeds through the enlargement of single epidermal cells, followed by several cell divisions to generate a structure perpendicular to the epidermal surface (Fig. 2), and specific types of glandular trichomes seem to have a well-defined developmental plan (Tissier, 2012a;Bergau et al, 2015). This highly regulated differentiation program also includes a polarized and localized cell wall lysis and remodeling (Bergau et al, 2015).…”

“…2), and specific types of glandular trichomes seem to have a well-defined developmental plan (Tissier, 2012a;Bergau et al, 2015). This highly regulated differentiation program also includes a polarized and localized cell wall lysis and remodeling (Bergau et al, 2015).…”

Bioenergetics of Monoterpenoid Essential Oil Biosynthesis in Nonphotosynthetic Glandular Trichomes

“…In type VI GTs of Solanum habrochaites, the accumulation of terpenoids occurs over a longer period of time, while in peppermint GT, filling concludes within a matter of days (Turner et al, 2000a(Turner et al, , 2000b. Terpenoids in S. habrochaites GTs are derived from both the mevalonate and MEP pathways (Bergau et al, 2015;Balcke et al, 2017), whereas in peppermint, terpenoids of GTs are produced solely via the MEP pathway and, therefore, the reactions catalyzed by HDS and HDR (McCaskill and Croteau, 1995;Eisenreich et al, 1997;Lange et al, 2001). It is tempting to speculate that the major GT-specific Fd isoform of peppermint (and possibly other Lamiaceae) might have evolved to facilitate the particularly high flux through the reactions catalyzed by HDS and HDR en route to monoterpenoid end products.…”