Abstract

Plastids in the leaf epidermal cells of plants are regarded as immature chloroplasts that, like mesophyll chloroplasts, undergo binary fission. While mesophyll chloroplasts have generally been used to study plastid division, recent studies have suggested the presence of tissue- or plastid type-dependent regulation of plastid division. Here, we report the detailed morphology of plastids and their stromules, and the intraplastidic localization of the chloroplast division-related protein AtFtsZ1-1, in the leaf epidermis of an Arabidopsis mutant that harbors a mutation in the chloroplast division site determinant gene AtMinE1. In atminE1, the size and shape of epidermal plastids varied widely, which contrasts with the plastid phenotype observed in atminE1 mesophyll cells. In particular, atminE1 epidermal plastids occasionally displayed grape-like morphology, a novel phenotype induced by a plastid division mutation. Observation of an atminE1 transgenic line harboring an AtMinE1 promoter::AtMinE1-yellow fluorescent protein fusion gene confirmed the expression and plastidic localization of AtMinE1 in the leaf epidermis. Further examination revealed that constriction of plastids and stromules mediated by the FtsZ1 ring contributed to the plastid pleomorphism in the atminE1 epidermis. These results illustrate that a single plastid division mutation can have dramatic consequences for epidermal plastid morphology, thereby implying that plastid division and morphogenesis are differentially regulated in epidermal and mesophyll plastids.

Highlights

  • Plastids are ancient prokaryote-derived organelles in plant cells that multiply via division of preexisting organelles

  • Extending our earlier observations (Fujiwara et al, 2009), we explored the detailed morphology of leaf epidermal plastids, stromules, and other types of plastid substructures, the localization of FtsZ1 within the plastids, and their possible associations with plastid constriction in the atminE1 mutant

  • Dual detection of stroma-targeted cyan fluorescent protein (CFP) and FtsZ1–green fluorescent protein (GFP) [AtFtsZ1-1–sGFP(S65T)] (Fujiwara et al, 2008) in a transgenic line revealed that the peanut-shaped plastids in the leaf epidermis were associated with the production of centrally located FtsZ1–GFP signals within the plastids (Figure 1E, right)

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Summary

Introduction

Plastids are ancient prokaryote-derived organelles in plant cells that multiply via division of preexisting organelles. The photosynthetic plastids, chloroplasts, undergo symmetric division, which produces a homogeneous population of spherical chloroplasts in each mature-leaf cell (Possingham and Lawrence, 1983; López-Juez and Pyke, 2005; Figures 1A,B). In the model plant Arabidopsis thaliana, approximately 10 nuclear-encoded proteins are located at distinct subplastidic compartments, which constitute the division apparatus (Yang et al, 2008; Okazaki et al, 2010). Among these proteins, the prokaryotic tubulinlike protein FtsZ, which stands for “Filamenting temperaturesensitive Z”, plays a central role in the initiation and progress of chloroplast division. A. thaliana has two phylogenetically distinct, functionally non-redundant FtsZ proteins, FtsZ1 and FtsZ2 (Stokes and Osteryoung, 2003; Miyagishima et al, 2004), both of which have polymerization and filament-bundling activities, enabling them to form a contractile ring structure at the mid-chloroplast site (McAndrew et al, 2001; Vitha et al, 2001; Yoder et al, 2007)

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