The occurrence of chloroplast peripheral reticulum in grasses: a matter of phylogeny or a matter of function?

Abstract

The chloroplast peripheral reticulum (PR) is a structure of unknown function. Some authors postulated that it is a characteristic feature of C 4 plants, although it was reported from C 3 species as well. It is unknown whether the occurrence of PR follows a phylogenetic (it is found in clades containing C 4 species, regardless of the photosynthetic type) or functional (photosynthetic pathway dependent) pattern. Here, we present a phylogenetically controlled analysis of the occurrence, form and functional aspects of PR in grasses. The occurrence of the PR follows a functional and not a phylogenetic pattern. Its most elaborated form (PR type I) is a unique feature of C 4 species. Although PR was found in some of the studied C 3 grasses, it was always less developed than PR in the chloroplasts of Kranz mesophyll cells of C 4 species. The size of PR in C 4 plants was found to increase when the plants were grown under low light intensity. Additional observations, such as a negative correlation between PR size and chloroplast surface and PR occurrence in vicinity of mitochondria or plasmodesmata, suggest that PR may play some role in C 4 metabolism.

Vesicles Are Persistent Features of Different Plastids

“…Type I consists of single or double rows of tubules around the (whole) periphery of the chloroplast. Type II is characterized by large groups of vesicles and tubules in certain regions of the plastids' periphery, whereas type III is represented by individual vesicles budding from the chloroplast inner envelope membrane . Types I and II are hypothesized as adaptations to increased transport demands in/out of the chloroplast, while type III could represent either poorly developed PR or be the type of vesicles discussed within this paper and previously .…”

“…There is an ongoing discussion about the vesicle transport system in the cytoplasm of plants, if it is indeed vesicles or tubules . In plastids, the shape of the structures differs, as does the classifications: from invaginations of envelope membranes and tubules (in different planes of sectioning) to the solitary vesicles of different stages and shapes . Vesicles do not always appear to be completely round.…”

“…On the other hand, types II and III occur in both C3 and C4 plants, but in C4 they are primarily found in bundle sheath cells. When PR is found in C3 plants, it is mostly of type III , i.e. in the form of single vesicle‐like structures.…”

“…Types I and II are hypothesized as adaptations to increased transport demands in/out of the chloroplast, while type III could represent either poorly developed PR or be the type of vesicles discussed within this paper and previously . Even if PR is predominantly found in C4 plants, it has also been observed in some C3 plants, such as wheat, which has PR types II and III . However, the distribution of PR types differs between groups.…”

“…Type II is characterized by large groups of vesicles and tubules in certain regions of the plastids' periphery, whereas type III is represented by individual vesicles budding from the chloroplast inner envelope membrane (29,30). Types I and II are hypothesized as adaptations to increased transport demands in/out of the chloroplast, while type III could represent either poorly developed PR or be the type of vesicles discussed within this paper and previously (30,31). Even if PR is predominantly found in C4 plants, it has also been observed in some C3 plants, such as wheat, which has PR types II and III (30).…”