How do bacteria localize proteins to the cell pole?

Laloux, Géraldine; Jacobs‐Wagner, Christine

doi:10.1242/jcs.138628

Cited by 163 publications

(166 citation statements)

References 119 publications

(147 reference statements)

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“…Furthermore, although the AtKEA2 protein without the N-terminal domain constitutes an active antiporter (Aranda-Sicilia et al, 2012), it fails to complement the growth defects of the double mutant plant, suggesting that the specific localization of the protein is crucial for its function. The association of oligomers of AtKEA2 could depend on membrane tension or curvature, which is highest at the poles but more relaxed at the midcell, as in bacteria (Laloux and Jacobs-Wagner, 2014;Strahl et al, 2015).…”

Section: The Long N-terminal Domain Attaches Atkea1/2 To Specific Locmentioning

confidence: 99%

Envelope K⁺/H⁺ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

et al. 2016

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It is well established that thylakoid membranes of chloroplasts convert light energy into chemical energy, yet the development of chloroplast and thylakoid membranes is poorly understood. Loss of function of the two envelope K + /H + antiporters AtKEA1 and AtKEA2 was shown previously to have negative effects on the efficiency of photosynthesis and plant growth; however, the molecular basis remained unclear. Here, we tested whether the previously described phenotypes of double mutant kea1kea2 plants are due in part to defects during early chloroplast development in Arabidopsis (Arabidopsis thaliana). We show that impaired growth and pigmentation is particularly evident in young expanding leaves of kea1kea2 mutants. In proliferating leaf zones, chloroplasts contain much lower amounts of photosynthetic complexes and chlorophyll. Strikingly, AtKEA1 and AtKEA2 proteins accumulate to high amounts in small and dividing plastids, where they are specifically localized to the two caps of the organelle separated by the fission plane. The unusually long amino-terminal domain of 550 residues that precedes the antiport domain appears to tether the full-length AtKEA2 protein to the two caps. Finally, we show that the double mutant contains 30% fewer chloroplasts per cell. Together, these results show that AtKEA1 and AtKEA2 transporters in specific microdomains of the inner envelope link local osmotic, ionic, and pH homeostasis to plastid division and thylakoid membrane formation.

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Section: The Long N-terminal Domain Attaches Atkea1/2 To Specific Locmentioning

confidence: 99%

Envelope K⁺/H⁺ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

et al. 2016

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“…Regardless of growth mode, the poles of rod-shaped cells often constitute a distinct subcellular environment for proteins with crucial roles in motility, chemotaxis, pathogenesis, differentiation, and cell cycle progression (15). Proteins that mediate pole identity have been primarily characterized in Caulobacter crescentus as its two poles undergo distinct changes in morphology during its cell cycle, alternating between a motile flagellated cell and a sessile stalked cell.…”

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confidence: 99%

PopZ identifies the new pole, and PodJ identifies the old pole during polar growth in Agrobacterium tumefaciens

Grangeon

Zupan

Anderson-Furgeson

et al. 2015

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

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Agrobacterium tumefaciens elongates by addition of peptidoglycan (PG) only at the pole created by cell division, the growth pole, whereas the opposite pole, the old pole, is inactive for PG synthesis. How Agrobacterium assigns and maintains pole asymmetry is not understood. Here, we investigated whether polar growth is correlated with novel pole-specific localization of proteins implicated in a variety of growth and cell division pathways. The cell cycle of A. tumefaciens was monitored by time-lapse and superresolution microscopy to image the localization of A. tumefaciens homologs of proteins involved in cell division, PG synthesis and pole identity. FtsZ and FtsA accumulate at the growth pole during elongation, and improved imaging reveals FtsZ disappears from the growth pole and accumulates at the midcell before FtsA. The L,D-transpeptidase Atu0845 was detected mainly at the growth pole. A. tumefaciens specific pole-organizing protein (Pop) PopZAt and polar organelle development (Pod) protein PodJAt exhibited dynamic yet distinct behavior. PopZAt was found exclusively at the growing pole and quickly switches to the new growth poles of both siblings immediately after septation. PodJAt is initially at the old pole but then also accumulates at the growth pole as the cell cycle progresses suggesting that PodJAt may mediate the transition of the growth pole to an old pole. Thus, PopZAt is a marker for growth pole identity, whereas PodJAt identifies the old pole.

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“…Several C. crescentus gene products are asymmetrically localized in a cell-cycle-dependent fashion to affect these developmental processes. One polar localizing protein, C. crescentus PopZ (PopZ Cc ), is required for development of the flagellated pole into the stalked pole and for chromosome segregation (14,(16)(17)(18). Another gene product, PodJCc, functions in development of polar organelles such as pili, flagella, and the adhesive holdfast (15) and is involved in the polar localization of cell cycle regulators such as PleC (15,19).…”

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Loss of PodJ in Agrobacterium tumefaciens Leads to Ectopic Polar Growth, Branching, and Reduced Cell Division

et al. 2016

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Agrobacterium tumefaciens is a rod-shaped Gram-negative bacterium that elongates by unipolar addition of new cell envelope material. Approaching cell division, the growth pole transitions to a nongrowing old pole, and the division site creates new growth poles in sibling cells. The A. tumefaciens homolog of the Caulobacter crescentus polar organizing protein PopZ localizes specifically to growth poles. In contrast, the A. tumefaciens homolog of the C. crescentus polar organelle development protein PodJ localizes to the old pole early in the cell cycle and accumulates at the growth pole as the cell cycle proceeds. FtsA and FtsZ also localize to the growth pole for most of the cell cycle prior to Z-ring formation. To further characterize the function of polar localizing proteins, we created a deletion of A. tumefaciens podJ (podJ At ). ⌬podJ At cells display ectopic growth poles (branching), growth poles that fail to transition to an old pole, and elongated cells that fail to divide. In ⌬podJ At cells, A. tumefaciens PopZgreen fluorescent protein (PopZ At -GFP) persists at nontransitioning growth poles postdivision and also localizes to ectopic growth poles, as expected for a growth-pole-specific factor. Even though GFP-PodJ At does not localize to the midcell in the wild type, deletion of podJ At impacts localization, stability, and function of Z-rings as assayed by localization of FtsA-GFP and FtsZ-GFP. Z-ring defects are further evidenced by minicell production. Together, these data indicate that PodJ At is a critical factor for polar growth and that ⌬podJ At cells display a cell division phenotype, likely because the growth pole cannot transition to an old pole. IMPORTANCEHow rod-shaped prokaryotes develop and maintain shape is complicated by the fact that at least two distinct species-specific growth modes exist: uniform sidewall insertion of cell envelope material, characterized in model organisms such as Escherichia coli, and unipolar growth, which occurs in several alphaproteobacteria, including Agrobacterium tumefaciens. Essential components for unipolar growth are largely uncharacterized, and the mechanism constraining growth to one pole of a wild-type cell is unknown. Here, we report that the deletion of a polar development gene, podJ At , results in cells exhibiting ectopic polar growth, including multiple growth poles and aberrant localization of cell division and polar growth-associated proteins. These data suggest that PodJ At is a critical factor in normal polar growth and impacts cell division in A. tumefaciens.

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How do bacteria localize proteins to the cell pole?

Cited by 163 publications

References 119 publications

Envelope K⁺/H⁺ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

Envelope K⁺/H⁺ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

PopZ identifies the new pole, and PodJ identifies the old pole during polar growth in Agrobacterium tumefaciens

Loss of PodJ in Agrobacterium tumefaciens Leads to Ectopic Polar Growth, Branching, and Reduced Cell Division

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How do bacteria localize proteins to the cell pole?

Cited by 163 publications

References 119 publications

Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

Envelope K+/H+ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

PopZ identifies the new pole, and PodJ identifies the old pole during polar growth in Agrobacterium tumefaciens

Loss of PodJ in Agrobacterium tumefaciens Leads to Ectopic Polar Growth, Branching, and Reduced Cell Division

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Envelope K⁺/H⁺ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development

Envelope K⁺/H⁺ Antiporters AtKEA1 and AtKEA2 Function in Plastid Development