Developmentally regulated association of plastid division protein FtsZ1 with thylakoid membranes in <i>Arabidopsis thaliana</i>

El-Kafafi, El-Sayed; Karamoko, Mohamed; Pignot-Paintrand, Isabelle; Grünwald, Didier; Mandaron, Paul; Lerbs-Mache, Silva; Falconet, Denis

doi:10.1042/bj20070543

Cited by 23 publications

(30 citation statements)

References 48 publications

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“…Interestingly, the apparent plasticity of FtsZ coassembly in vitro is consistent with genetic studies showing that chloroplast FtsZ filaments assemble under a wide range of in vivo stoichiometries, although significant deviations from the wild type stoichiometry alters FtsZ filament morphology and perturbs plastid division (17,19,20,24,61). Nevertheless, the ability of FtsZ1 and FtsZ2 to coassemble at different stoichiometries raises the intriguing possibility that the degree of heteropolymerization and/or bundling may be regulated in vivo as a means of regulating FtsZ filament morphology and hence Z ring constriction and dynamics.…”

Section: Discussionsupporting

confidence: 63%

“…Nevertheless, the ability of FtsZ1 and FtsZ2 to coassemble at different stoichiometries raises the intriguing possibility that the degree of heteropolymerization and/or bundling may be regulated in vivo as a means of regulating FtsZ filament morphology and hence Z ring constriction and dynamics. Such regulation may be necessary because plants have multiple plastid types that vary greatly in size and division activity; perhaps the relative levels of FtsZ1 and FtsZ2 vary in different plastid types or at different stages of development (61). In this context, it is interesting to note that complete FtsZ2 rings are occasionally observed in small plastids of ftsZ1 null mutants (25), but the converse is not true (19).…”

Section: Discussionmentioning

confidence: 97%

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GTP-dependent Heteropolymer Formation and Bundling of Chloroplast FtsZ1 and FtsZ2

Olson

Wang

Osteryoung

2010

Journal of Biological Chemistry

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Bacteria and chloroplasts require the ring-forming cytoskeletal protein FtsZ for division. Although bacteria accomplish division with a single FtsZ, plant chloroplasts require two FtsZ types for division, FtsZ1 and FtsZ2. These proteins colocalize to a mid-plastid Z ring, but their biochemical relationship is poorly understood. We investigated the in vitro behavior of recombinant FtsZ1 and FtsZ2 separately and together. Both proteins bind and hydrolyze GTP, although GTPase activities are low compared with the activity of Escherichia coli FtsZ. Each protein undergoes GTP-dependent assembly into thin protofilaments in the presence of calcium as a stabilizing agent, similar to bacterial FtsZ. In contrast, when mixed without calcium, FtsZ1 and FtsZ2 exhibit slightly elevated GTPase activity and coassembly into extensively bundled protofilaments. Coassembly is enhanced by FtsZ1, suggesting that it promotes lateral interactions between protofilaments. Experiments with GTPase-deficient mutants reveal that FtsZ1 and FtsZ2 form heteropolymers. Maximum coassembly occurs in reactions containing equimolar FtsZ1 and FtsZ2, but significant coassembly occurs at other stoichiometries. The FtsZ1:FtsZ2 ratio in coassembled structures mirrors their input ratio, suggesting plasticity in protofilament and/or bundle composition. This behavior contrasts with that of ␣-and ␤-tubulin and the bacterial tubulin-like proteins BtubA and BtubB, which coassemble in a strict 1:1 stoichiometry. Our findings raise the possibility that plasticity in FtsZ filament composition and heteropolymerization-induced bundling could have been a driving force for the coevolution of FtsZ1 and FtsZ2 in the green lineage, perhaps arising from an enhanced capacity for the regulation of Z ring composition and activity in vivo.Cell division in bacteria and chloroplast division in plants both require FtsZ, a tubulin-like GTPase that functions as a contractile ring, the Z ring, inside the cell or chloroplast. Mutations in bacterial FtsZ genes disrupt cell division, resulting in long filamented cells (reviewed in Refs. 1-3). Purified bacterial FtsZ undergoes GTP-dependent, hydrolysis-independent polymerization primarily into single protofilaments (4, 5), but protofilament sheets and bundles form in the presence of stabilizing agents that promote lateral interactions (6 -8). Polymerization stimulates FtsZ GTPase activity because the catalytic site for GTP hydrolysis lies in the longitudinal interface between adjacent monomers within the polymer (9). GTP hydrolysis destabilizes protofilaments, leading to disassembly (10). The in vivo structure of the bacterial Z ring is not yet clear, but recent models suggest it may be built from short overlapping protofilaments that are stabilized at the division site by accessory factors (11, 12). The Z ring functions partly as a scaffold for other cell division proteins and recently has also been shown to provide contractile force for membrane constriction (13,14).In most bacteria, including the cyanobacterial relatives of chloropl...

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Section: Discussionsupporting

confidence: 63%

Section: Discussionmentioning

confidence: 97%

GTP-dependent Heteropolymer Formation and Bundling of Chloroplast FtsZ1 and FtsZ2

Olson

Wang

Osteryoung

2010

Journal of Biological Chemistry

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“…It has been suggested that a cytoskeleton-like FtsZ network in chloroplasts aids in maintaining the chloroplast structure. Overexpression of FtsZ has been demonstrated to lead to alterations of the chloroplasts in Arabidopsis (Arabidopsis thaliana) leaves (El-Kafafi et al, 2008) that are similar to those observed here for desiccated P. patens gametophores.…”

Section: Alterations In Cellular Structure Help To Limit Desiccation supporting

confidence: 61%

Exploring the Mechanism of Physcomitrella patens Desiccation Tolerance through a Proteomic Strategy

et al. 2009

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The moss Physcomitrella patens has been shown to tolerate abiotic stresses, including salinity, cold, and desiccation. To better understand this plant's mechanism of desiccation tolerance, we have applied cellular and proteomic analyses. Gametophores were desiccated over 1 month to 10% of their original fresh weight. We report that during the course of dehydration, several related processes are set in motion: plasmolysis, chloroplast remodeling, and microtubule depolymerization. Despite the severe desiccation, the membrane system maintains integrity. Through two-dimensional gel electrophoresis and image analysis, we identified 71 proteins as desiccation responsive. Following identification and functional categorization, we found that a majority of the desiccation-responsive proteins were involved in metabolism, cytoskeleton, defense, and signaling. Degradation of cytoskeletal proteins might result in cytoskeletal disassembly and consequent changes in the cell structure. Late embryogenesis abundant proteins and reactive oxygen species-scavenging enzymes are both prominently induced, and they might help to diminish the damage brought by desiccation.

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“…We could not confirm earlier reports of altered starch accumulation and granule number in arc3, arc5, arc6, and arc10 mutants (Austin and Webber, 2005;El-Kafafi et al, 2008); thus, there is at present no good evidence that components of the chloroplast division apparatus act as primers for granule initiation. Our observations do not allow us to distinguish between other possible priming mechanisms.…”

Section: Granule Initiation Is Infrequent In Mature Leavescontrasting

confidence: 55%

“…However, there are indications that some of the ARC proteins may influence starch accumulation. Arabidopsis arc3, arc5, arc6, and arc10 mutants were reported to have increased starch accumulation, whereas plants overexpressing FtsZ1 (ARC10) have no starch granules (Austin and Webber, 2005;El-Kafafi et al, 2008). Overexpression of FtsZ in potato (Solanum tuberosum) tubers resulted in smaller plastids apparently containing fewer, larger starch granules (de Pater et al, 2006) and rice (Oryza sativa) endosperm misexpressing FtsZ proteins contains granules of abnormal sizes and shapes (Yun and Kawagoe, 2010).…”

Section: Relationship Between Starch Granule Number and Chloroplast Vmentioning

confidence: 99%

Control of Starch Granule Numbers in Arabidopsis Chloroplasts

et al. 2011

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The aim of this work was to investigate starch granule numbers in Arabidopsis (Arabidopsis thaliana) leaves. Lack of quantitative information on the extent of genetic, temporal, developmental, and environmental variation in granule numbers is an important limitation in understanding control of starch degradation and the mechanism of granule initiation. Two methods were developed for reliable estimation of numbers of granules per chloroplast. First, direct measurements were made on large series of consecutive sections of mesophyll tissue obtained by focused ion beam-scanning electron microscopy. Second, average numbers were calculated from the starch contents of leaves and chloroplasts and estimates of granule mass based on granule dimensions. Examination of wild-type plants and accumulation and regulation of chloroplast (arc) mutants with few, large chloroplasts provided the following new insights. There is wide variation in chloroplast volumes in cells of wild-type leaves. Granule numbers per chloroplast are correlated with chloroplast volume, i.e. large chloroplasts have more granules than small chloroplasts. Mature leaves of wild-type plants and arc mutants have approximately the same number of granules per unit volume of stroma, regardless of the size and number of chloroplasts per cell. Granule numbers per unit volume of stroma are also relatively constant in immature leaves but are greater than in mature leaves. Granule initiation occurs as chloroplasts divide in immature leaves, but relatively little initiation occurs in mature leaves. Changes in leaf starch content over the diurnal cycle are largely brought about by changes in the volume of a fixed number of granules.Chloroplasts in Arabidopsis (Arabidopsis thaliana) mesophyll cells are generally stated to contain about five starch granules at the end of the light period (Zeeman et al., 2002(Zeeman et al., , 2007, but nothing is known about how this number is determined or the extent of genetic, temporal, developmental, and environmental variation in the number. This is an important limitation in understanding control of starch degradation at night, a process essential for the normal growth of the plant (Gibon et al., 2006;Smith and Stitt, 2007;Stitt et al., 2007;Usadel et al., 2008). The surface area and volume of starch granules in the chloroplast are relevant to the control of starch degradation in two ways. First, surface area can potentially limit the rate of degradation during the night. This limitation is not a major determinant of the rate of degradation in wild-type Arabidopsis leaves in controlled conditions; degradation is near linear through most of the night and consumes almost all of the starch reserves by dawn. If degradation were limited by surface area, the rate would decline with time through the night. However, reductions in starch granule numbers may result in limitation of starch degradation. The starch synthase4 (ss4) mutant of Arabidopsis has only one starch granule per chloroplast. It has a low rate of starch degradation and a low...

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Developmentally regulated association of plastid division protein FtsZ1 with thylakoid membranes in Arabidopsis thaliana

Cited by 23 publications

References 48 publications

GTP-dependent Heteropolymer Formation and Bundling of Chloroplast FtsZ1 and FtsZ2

GTP-dependent Heteropolymer Formation and Bundling of Chloroplast FtsZ1 and FtsZ2

Exploring the Mechanism of Physcomitrella patens Desiccation Tolerance through a Proteomic Strategy

Control of Starch Granule Numbers in Arabidopsis Chloroplasts

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