Arabidopsis thaliana Leaf Epidermal Guard Cells: A Model for Studying Chloroplast Proliferation and Partitioning in Plants

Fujiwara, Makoto; Sanjaya, Alvin; Itoh, Ryuuichi

doi:10.3389/fpls.2019.01403

Cited by 9 publications

(8 citation statements)

References 73 publications

(98 reference statements)

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“…Supporting this notion, in our preliminary experiments, we observed FtsZ1 ring-associated, constricted leucoplasts in Arabidopsis trichomes (Fujiwara, unpublished data). Similarly, in Arabidopsis guard cells, our data suggest FtsZ1 ring-mediated division of chloroplasts (Fujiwara et al, 2019). We cannot, therefore, exclude the latter possibility mentioned above.…”

Section: Significance Of Parc6 In Plastid Replication and Morphology mentioning

confidence: 51%

Arabidopsis PARC6 Is Critical for Plastid Morphogenesis in Pavement, Trichome, and Guard Cells in Leaf Epidermis

et al. 2020

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Recently, a recessive Arabidopsis thaliana mutant with abundant stromules in leaf epidermal pavement cells was visually screened and isolated. The gene responsible for this mutant phenotype was identified as PARC6, a chloroplast division site regulator gene. The mutant allele parc6-5 carried two point mutations (G62R and W700stop) at the N-and C-terminal ends of the coding sequence, respectively. Here, we further characterized parc6-5 and other parc6 mutant alleles, and showed that PARC6 plays a critical role in plastid morphogenesis in all cell types of the leaf epidermis: pavement cells, trichome cells, and guard cells. Transient expression of PARC6 transit peptide (TP) fused to the green fluorescent protein (GFP) in plant cells showed that the G62R mutation has no or little effect on the TP activity of the PARC6 Nterminal region. Then, plastid morphology was microscopically analyzed in the leaf epidermis of wild-type (WT) and parc6 mutants (parc6-1, parc6-3, parc6-4 and parc6-5) with the aid of stroma-targeted fluorescent proteins. In parc6 pavement cells, plastids often assumed aberrant grape-like morphology, similar to those in severe plastid division mutants, atminE1, and arc6. In parc6 trichome cells, plastids exhibited extreme grape-like aggregations, without the production of giant plastids (>6 µm diameter), as a general phenotype. In parc6 guard cells, plastids exhibited a variety of abnormal phenotypes, including reduced number, enlarged size, and activated stromules, similar to those in atminE1 and arc6 guard cells. Nevertheless, unlike atminE1 and arc6, parc6 exhibited a low number of mini-chloroplasts (< 2 µm diameter) and rarely produced chloroplast-deficient guard cells. Importantly, unlike parc6, the chloroplast division site mutant arc11 exhibited WT-like plastid phenotypes in trichome and guard cells. Finally, observation of parc6 complementation lines expressing a functional PARC6-GFP protein indicated that PARC6-GFP formed a ring-like structure in both constricting and non-constricting chloroplasts, and that PARC6 dynamically changes its configuration during the process of chloroplast division.

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Section: Significance Of Parc6 In Plastid Replication and Morphology mentioning

confidence: 51%

Arabidopsis PARC6 Is Critical for Plastid Morphogenesis in Pavement, Trichome, and Guard Cells in Leaf Epidermis

et al. 2020

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“…These chloroplasts were frequently highly elongated, with a constriction at the mid-point. Based on our previous observation of FtsZ1 ring-mediated chloroplast division in guard cells of expanding leaves [ 75 ], these elongated chloroplasts were predicted to be undergoing binary fission [ 76 ]. However, guard mother cells in both Ar50-33-pg1 and egy1-4 leaves exhibited no (or barely detectable) chlorophyll autofluorescence.…”

Section: Resultsmentioning

confidence: 99%

Arabidopsis EGY1 Is Critical for Chloroplast Development in Leaf Epidermal Guard Cells

Sanjaya

Muramatsu

Sato

et al. 2021

Plants

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In Arabidopsis thaliana, the Ethylene-dependent Gravitropism-deficient and Yellow-green 1 (EGY1) gene encodes a thylakoid membrane-localized protease involved in chloroplast development in leaf mesophyll cells. Recently, EGY1 was also found to be crucial for the maintenance of grana in mesophyll chloroplasts. To further explore the function of EGY1 in leaf tissues, we examined the phenotype of chloroplasts in the leaf epidermal guard cells and pavement cells of two 40Ar17+ irradiation-derived mutants, Ar50-33-pg1 and egy1-4. Fluorescence microscopy revealed that fully expanded leaves of both egy1 mutants showed severe chlorophyll deficiency in both epidermal cell types. Guard cells in the egy1 mutant exhibited permanent defects in chloroplast formation during leaf expansion. Labeling of plastids with CaMV35S or Protodermal Factor1 (PDF1) promoter-driven stroma-targeted fluorescent proteins revealed that egy1 guard cells contained the normal number of plastids, but with moderately reduced size, compared with wild-type guard cells. Transmission electron microscopy further revealed that the development of thylakoids was impaired in the plastids of egy1 mutant guard mother cells, guard cells, and pavement cells. Collectively, these observations demonstrate that EGY1 is involved in chloroplast formation in the leaf epidermis and is particularly critical for chloroplast differentiation in guard cells.

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“…Stomatal guard cells are a useful model for investigating chloroplast proliferation and partitioning (Fujiwara et al ., 2019), as well as the ultrastructures of chloroplasts and stromules (Ishikawa et al ., 2020). Therefore, we examined the guard cells of suba1 in detail by fluorescence microscopy (Figure 9) and TEM (Figure 10).…”

Section: Discussionmentioning

confidence: 99%

TGD5 is required for normal morphogenesis of non‐mesophyll plastids, but not mesophyll chloroplasts, in Arabidopsis

et al. 2021

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Stromules are dynamic membrane-bound tubular structures that emanate from plastids. Stromule formation is triggered in response to various stresses and during plant development, suggesting that stromules may have physiological and developmental roles in these processes. Despite the possible biological importance of stromules and their prevalence in green plants, their exact roles and formation mechanisms remain unclear. To explore these issues, we obtained Arabidopsis thaliana mutants with excess stromule formation in the leaf epidermis by microscopy-based screening. Here, we characterized one of these mutants, stromule biogenesis altered 1 (suba1). suba1 forms plastids with severely altered morphology in a variety of nonmesophyll tissues, such as leaf epidermis, hypocotyl epidermis, floral tissues, and pollen grains, but apparently normal leaf mesophyll chloroplasts. The suba1 mutation causes impaired chloroplast pigmentation and altered chloroplast ultrastructure in stomatal guard cells, as well as the aberrant accumulation of lipid droplets and their autophagic engulfment by the vacuole. The causal defective gene in suba1 is TRIGALAC-TOSYLDIACYLGLYCEROL5 (TGD5), which encodes a protein putatively involved in the endoplasmic reticulum (ER)-to-plastid lipid trafficking required for the ER pathway of thylakoid lipid assembly. These findings suggest that a non-mesophyll-specific mechanism maintains plastid morphology. The distinct mechanisms maintaining plastid morphology in mesophyll versus non-mesophyll plastids might be attributable, at least in part, to the differential contributions of the plastidial and ER pathways of lipid metabolism between mesophyll and non-mesophyll plastids.

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Arabidopsis thaliana Leaf Epidermal Guard Cells: A Model for Studying Chloroplast Proliferation and Partitioning in Plants

Cited by 9 publications

References 73 publications

Arabidopsis PARC6 Is Critical for Plastid Morphogenesis in Pavement, Trichome, and Guard Cells in Leaf Epidermis

Arabidopsis PARC6 Is Critical for Plastid Morphogenesis in Pavement, Trichome, and Guard Cells in Leaf Epidermis

Arabidopsis EGY1 Is Critical for Chloroplast Development in Leaf Epidermal Guard Cells

TGD5 is required for normal morphogenesis of non‐mesophyll plastids, but not mesophyll chloroplasts, in Arabidopsis

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