Stromule formation is dependent upon plastid size, plastid differentiation status and the density of plastids within the cell.

Mark T Waters,Rupert G Fray,Kevin A Pyke

doi:10.1111/j.1365-313x.2004.02164.x

Abstract

Stromules are motile extensions of the plastid envelope membrane, whose roles are not fully understood. They are present on all plastid types but are more common and extensive on non-green plastids that are sparsely distributed within the cell. During tomato fruit ripening, chloroplasts in the mesocarp tissue differentiate into chromoplasts and undergo major shifts in morphology. In order to understand what factors regulate stromule formation, we analysed stromule biogenesis in tobacco hypocotyls and in two distinct plastid populations in tomato mesocarp. We show that increases in stromule length and frequency are correlated with chromoplast differentiation, but only in one plastid population where the plastids are larger and less numerous. We used tobacco hypocotyls to confirm that stromule length increases as plastids become further apart, suggesting that stromules optimize the plastid-cytoplasm contact area. Furthermore, we demonstrate that ectopic chloroplast components decrease stromule formation on tomato fruit chromoplasts, whereas preventing chloroplast development leads to increased numbers of stromules. Inhibition of fruit ripening has a dramatic impact on plastid and stromule morphology, underlining that plastid differentiation status, and not cell type, is a significant factor in determining the extent of plastid stromules. By modifying the plastid surface area, we propose that stromules enhance the specific metabolic activities of plastids.

Highlights

Plastids are a family of interrelated organelles that assume various forms, such as chloroplasts, chromoplasts and amyloplasts, each with specialized roles and appearances which have formed the basis for their traditional classification (Waters and Pyke, 2004)
An overview of plastid morphology in various tobacco cell types revealed that stromules are distributed in a tissue-specific manner, with an emergent trend that stromules are most abundant on non-green plastids such as those found in roots and cultured suspension cells (Kohler and Hanson, 2000)
Chloroplasts such as those in leaf mesophyll cells exhibit few stromules, and these tend to be short and ephemeral in nature. Such observations suffer from the problem of confounding factors, as non-green plastids are often present at lower numbers within the cell and are frequently smaller; in these cells stromules might help increase the surface area for plastid–cytoplasm contact

Summary

Introduction

Plastids are a family of interrelated organelles that assume various forms, such as chloroplasts, chromoplasts and amyloplasts, each with specialized roles and appearances which have formed the basis for their traditional classification (Waters and Pyke, 2004). These protrusions, known as stromules (stroma-filled tubules), sometimes link individual plastids and allow them to exchange macromolecules (Kwok and Hanson, 2004a) Evidence of such plastid shape dynamics has been reported sporadically in the past (Gray et al, 2001), modern microscopy techniques coupled with GFP have allowed the reliable study of the motile nature of both pigmented and non-pigmented plastids in a wide variety of plant species. An overview of plastid morphology in various tobacco cell types revealed that stromules are distributed in a tissue-specific manner, with an emergent trend that stromules are most abundant on non-green plastids such as those found in roots and cultured suspension cells (Kohler and Hanson, 2000) Chloroplasts such as those in leaf mesophyll cells exhibit few stromules, and these tend to be short and ephemeral in nature. Cellular differentiation, in conjunction with plastid differentiation, may influence stromule biogenesis

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Conclusion