Announcing a brand new cellular organelle – the tannosome

Tannins are present in most vascular plants and serve diverse roles. They provide defence against herbivores and pathogens, and protection against UV radiation. These secondary metabolites are polymers of catechins belonging to the vast family of flavonoids. Sucrose gradient sub-cellular fractionation, molecular biology and immunocytochemical approaches suggest that flavonoids are synthesized by a multienzymatic complex loosely bound to the cytosolic face of the endoplasmic reticulum. However no ultrastructural and morphological research has been conducted into the ontogenesis of intracellular tannin-forming elements in terrestrial plants.

A new paper in Annals of Botany (free access) describes detailed ultrastructural and morphological examination of the possible involvement of chloroplasts in the formation of tannin-forming structures in vascular plants. This resulted in the discovery of a new chloroplast-derived organelle, the tannosome. These structures are are formed by pearling of the thylakoids into 30 nm spheres, which are then encapsulated in a tannosome shuttle formed by budding from the chloroplast and bound by a membrane resulting from the fusion of both chloroplast envelopes. The shuttle conveys numerous tannosomes through the cytoplasm towards the vacuole in which it is then incorporated by invagination of the tonoplast. Finally, shuttles bound by a portion of tonoplast aggregate into tannin accretions which are stored in the vacuole. Polymerization of tannins occurs inside the tannosome regardless of the compartment being crossed. The complete sequence of events described occurs in all studied vascular plants.

The tannosome is an organelle forming condensed tannins in the chlorophyllous organs of Tracheophyta. (2013) Annals of Botany doi: 10.1093/aob/mct168
Condensed tannins (also called proanthocyanidins) are widespread polymers of catechins and are essential for the defence mechanisms of vascular plants (Tracheophyta). A large body of evidence argues for the synthesis of monomeric epicatechin on the cytosolic face of the endoplasmic reticulum and its transport to the vacuole, although the site of its polymerization into tannins remains to be elucidated. The aim of the study was to re-examine the cellular frame of tannin polymerization in various representatives of the Tracheophyta. Light microscopy epifluorescence, confocal microscopy, transmission electron microscopy (TEM), chemical analysis of tannins following cell fractionation, and immunocytochemistry were used as independent methods on tannin-rich samples from various organs from Cycadophyta, Ginkgophyta, Equisetophyta, Pteridophyta, Coniferophyta and Magnoliophyta. Tissues were fixed in a caffeine–glutaraldehyde mixture and examined by TEM. Other fresh samples were incubated with primary antibodies against proteins from both chloroplastic envelopes and a thylakoidal chlorophyll-carrying protein; they were also incubated with gelatin–Oregon Green, a fluorescent marker of condensed tannins. Coupled spectral analyses of chlorophyll and tannins were carried out by confocal microscopy on fresh tissues and tannin-rich accretions obtained through cell fractionation; chemical analyses of tannins and chlorophylls were also performed on the accretions. The presence of the three different chloroplast membranes inside vacuolar accretions that constitute the typical form of tannin storage in vascular plants was established in fresh tissues as well as in purified organelles, using several independent methods. Tannins are polymerized in a new chloroplast-derived organelle, the tannosome. These are formed by pearling of the thylakoids into 30 nm spheres, which are then encapsulated in a tannosome shuttle formed by budding from the chloroplast and bound by a membrane resulting from the fusion of both chloroplast envelopes. The shuttle conveys numerous tannosomes through the cytoplasm towards the vacuole in which it is then incorporated by invagination of the tonoplast. Finally, shuttles bound by a portion of tonoplast aggregate into tannin accretions which are stored in the vacuole. Polymerization of tannins occurs inside the tannosome regardless of the compartment being crossed. A complete sequence of events apparently valid in all studied Tracheophyta is described.

Editorial Comment:
It’s not unusual for Annals of Botany to publish groundbreaking research of fundamental importance such as this paper. And it’s not surprising that clued-in authors choose to publish high quality plant science research in specialist journals such as Annals rather than in trendy catch-all science journals where results of this significance get lost in the over concentration on medical research. It’s only surprising that it comes as a surprise to some people. It’s what we have been doing for the last 126 years.