A Genetic Analysis of Chloroplast Division and Expansion in Arabidopsis thaliana

Pyke, Kevin; Leech, Rachel M.

doi:10.1104/pp.104.1.201

Cited by 189 publications

(178 citation statements)

References 16 publications

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“…Like other chloroplast division mutants, leaf mesophyll cells in arc5 (Ler) mutants contain fewer and larger chloroplasts than do wild type cells, which have about 120 chloroplasts at maturity (21,22) (Fig. 1 A).…”

Section: Resultsmentioning

confidence: 97%

“…Arabidopsis thaliana strains Columbia (Col-0) and Landsberg erecta (Ler) were used for all experiments as indicated. The arc5 mutant was identified in the Ler background by Pyke and Leech (21). Plants were grown as described (4).…”

Section: Methodsmentioning

confidence: 99%

“…The Arabidopsis mutant arc5 contains an ethyl methanesulfonate (EMS)-induced mutation conferring a chloroplast division defect in which chloroplasts initiate but rarely complete constriction (21,22). As a result, arc5 chloroplasts often exhibit a dumbbell shape (Fig.…”

mentioning

confidence: 99%

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ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

Gao

Kadirjan-Kalbach

Froehlich

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

253

254

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Chloroplast division in plant cells is orchestrated by a complex macromolecular machine with components positioned on both the inner and outer envelope surfaces. The only plastid division proteins identified to date are of endosymbiotic origin and are localized inside the organelle. Employing positional cloning methods in Arabidopsis in conjunction with a novel strategy for pinpointing the mutant locus, we have identified a gene encoding a new chloroplast division protein, ARC5. Mutants of ARC5 exhibit defects in chloroplast constriction, have enlarged, dumbbellshaped chloroplasts, and are rescued by a wild-type copy of ARC5. The ARC5 gene product shares similarity with the dynamin family of GTPases, which mediate endocytosis, mitochondrial division, and other organellar fission and fusion events in eukaryotes. Phylogenetic analysis showed that ARC5 is related to a group of dynamin-like proteins unique to plants. A GFP-ARC5 fusion protein localizes to a ring at the chloroplast division site. Chloroplast import and protease protection assays indicate that the ARC5 ring is positioned on the outer surface of the chloroplast. Thus, ARC5 is the first cytosolic component of the chloroplast division complex to be identified. ARC5 has no obvious counterparts in prokaryotes, suggesting that it evolved from a dynamin-related protein present in the eukaryotic ancestor of plants. These results indicate that the chloroplast division apparatus is of mixed evolutionary origin and that it shares structural and mechanistic similarities with both the cell division machinery of bacteria and the dynamin-mediated organellar fission machineries of eukaryotes.T he chloroplasts of plants and algae are widely believed to have evolved only once from a free-living cyanobacterial endosymbiont (1). Over evolutionary time, many of the genes once present in the endosymbiont have been transferred to the nuclear genome where they have acquired sequences encoding transit peptides that direct their gene products back to the chloroplast (1, 2). This scenario describes the origin of the five previously identified plastid division proteins in plants, all of which evolved from related cell division proteins in cyanobacteria, are encoded in the nucleus, and are localized inside the chloroplast. These include FtsZ1 and FtsZ2, tubulin-like proteins that localize to a ring at the site of plastid constriction (3-10), MinD and MinE, which regulate placement of the plastid division site (11-13), and ARTEMIS, which appears to mediate constriction of the envelope membranes (14).Despite localization of the previously identified plastid division proteins inside the chloroplasts in plant cells, ultrastructural studies have shown that plastid division entails the coordinated activity of components localized outside as well as inside the organelle. In plants, the chloroplast division complex comprises electron-dense structures situated both on the stromal surface of the inner envelope membrane and on the cytosolic surface of the outer membrane (15). These structur...

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Section: Resultsmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

Gao

Kadirjan-Kalbach

Froehlich

et al. 2003

Proc. Natl. Acad. Sci. U.S.A.

253

254

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“…At 3 and 9 h, agb1-2 plants showed large patches of weakly fluorescing epidermal cells. Chloroplast fluorescence in epidermal cells, which have fewer but larger chloroplasts than guard cells in Arabidopsis (Pyke and Leech, 1994), was more intense in the agb1-2 mutant than in wild-type plants. At 20 h after the onset of O 3 exposure, the cellular distribution of ROS fluorescence in agb1-2 plants resembled that in wild-type plants and often was more intense.…”

Section: The Early Component Of the Oxidative Burst Requires Both Ga mentioning

confidence: 94%

Different Signaling and Cell Death Roles of Heterotrimeric G Protein α and β Subunits in the Arabidopsis Oxidative Stress Response to Ozone

et al. 2005

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Arabidopsis thaliana plants with null mutations in the genes encoding the a and b subunits of the single heterotrimeric G protein are less and more sensitive, respectively, to O 3 damage than wild-type Columbia-0 plants. The first peak of the bimodal oxidative burst elicited by O 3 in wild-type plants is almost entirely missing in both mutants. The late peak is normal in plants lacking the Gb protein but missing in plants lacking the Ga protein. Endogenous reactive oxygen species (ROS) are first detectable in chloroplasts of leaf epidermal guard cells. ROS production in adjacent cells is triggered by extracellular ROS signals produced by guard cell membrane-associated NADPH oxidases encoded by the AtrbohD and AtrbohF genes. The late, tissue damage-associated component of the oxidative burst requires only the Ga protein and arises from multiple cellular sources. The early component of the oxidative burst, arising primarily from chloroplasts, requires signaling through the heterotrimer (or the Gbg complex) and is separable from Ga-mediated activation of membrane-bound NADPH oxidases necessary for both intercellular signaling and cell death.

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“…A number of genes have been identified that promote or restrain chloroplast division (for review, see Osteryoung and Pyke, 2014). One early discovery for the arc (accumulation and replication of chloroplast) mutants was that their chloroplast coverage did not diverge from the wild type, indicating that the mechanisms that regulate chloroplast size and division are independent (Pyke and Leech, 1994). One protein recently identified as a regulator of chloroplast coverage is REDUCED CHLOROPLAST COVERAGE1, which is extraplastidic in localization (Larkin et al, 2016).…”

Section: Regulation Of Chloroplast Number and Sizementioning

confidence: 99%

The Rubisco Chaperone BSD2 May Regulate Chloroplast Coverage in Maize Bundle Sheath Cells

et al. 2017

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In maize (Zea mays), Bundle Sheath Defective2 (BSD2) plays an essential role in Rubisco biogenesis and is required for correct bundle sheath (BS) cell differentiation. Yet, BSD2 RNA and protein levels are similar in mesophyll (M) and BS chloroplasts, although Rubisco accumulates only in BS chloroplasts. This raises the possibility of additional BSD2 roles in cell development. To test this hypothesis, transgenic lines were created that overexpress and underexpress BSD2 in both BS and M cells, driven by the cell type-specific Rubisco Small Subunit (RBCS) or Phosphoenolpyruvate Carboxylase (PEPC) promoters or the ubiquitin promoter. Genetic crosses showed that each of the transgenes could complement Rubisco deficiency and seedling lethality conferred by the bsd2 mutation. This was unexpected, as RBCS-BSD2 lines lacked BSD2 in M chloroplasts and PEPC-BSD2 lines expressed half the wild-type BSD2 level in BS chloroplasts. We conclude that BSD2 does not play a vital role in M cells and that BS BSD2 is in excess of requirements for Rubisco accumulation. BSD2 levels did affect chloroplast coverage in BS cells. In PEPC-BSD2 lines, chloroplast coverage decreased 30% to 50%, whereas lines with increased BSD2 content exhibited a 25% increase. This suggests that BSD2 has an ancillary role in BS cells related to chloroplast size. Gas exchange showed decreased photosynthetic rates in PEPC-BSD2 lines despite restored Rubisco function, correlating with reduced chloroplast coverage and pointing to CO 2 diffusion changes. Conversely, increased chloroplast coverage did not result in increased Rubisco abundance or photosynthetic rates. This suggests another limitation beyond chloroplast volume, most likely Rubisco biogenesis and/or turnover rates.

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A Genetic Analysis of Chloroplast Division and Expansion in Arabidopsis thaliana

Cited by 189 publications

References 16 publications

ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery

Different Signaling and Cell Death Roles of Heterotrimeric G Protein α and β Subunits in the Arabidopsis Oxidative Stress Response to Ozone

The Rubisco Chaperone BSD2 May Regulate Chloroplast Coverage in Maize Bundle Sheath Cells

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