Isolation and analysis of a stromule‐overproducing <i>Arabidopsis</i> mutant suggest the role of <i>PARC6</i> in plastid morphology maintenance in the leaf epidermis

Itoh, Ryuuichi; Ishikawa, Hiroki; Nakajima, Kohdai P.; Moriyama, Shota; Fujiwara, Makoto

doi:10.1111/ppl.12648

Cited by 15 publications

(46 citation statements)

References 67 publications

(139 reference statements)

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“…The G62R mutation is located in the TP of PARC6 (Glynn et al, 2009), whereas the W700stop mutation is present in the C-terminal region. Additionally, mutant analysis indicated that the enlarged size and excessive stromule proliferation phenotypes of parc6-5 pavement cell plastids are similar to those of other parc6 alleles, including parc6-1, parc6-3, and parc6-4 (Itoh et al, 2018). Our results also indicated that PARC6 interacts with AtMinD1 (also known as ARC11), another chloroplast division site regulator in mesophyll and pavement cells (Marrison et al, 1999;Colletti et al, 2000;Vitha et al, 2003;Fujiwara et al, 2004;Fujiwara et al, 2008;Fujiwara et al, 2009b;Fujiwara et al, 2017).…”

Section: Introductionsupporting

confidence: 66%

“…Our results also indicated that PARC6 interacts with AtMinD1 (also known as ARC11), another chloroplast division site regulator in mesophyll and pavement cells (Marrison et al, 1999;Colletti et al, 2000;Vitha et al, 2003;Fujiwara et al, 2004;Fujiwara et al, 2008;Fujiwara et al, 2009b;Fujiwara et al, 2017). However, unlike parc6, arc11 shows fairly modest pavement cell chloroplast phenotypes (Fujiwara et al, 2017;Itoh et al, 2018).…”

Section: Introductionsupporting

confidence: 59%

“…Seeds of plastid division mutants, parc6-1 (SALK_100009; Glynn et al, 2009;Zhang et al, 2009;Ottesen et al, 2010;generated by Alonso et al, 2003), parc6-3 (Glynn et al, 2009), parc6-4 (SALK_138043; Zhang et al, 2009; generated by Alonso et al, 2003), arc6-3 (CS288; , and arc11-1 (CS281; Marrison et al, 1999) were obtained from the Arabidopsis Biological Resource Center (ABRC), Ohio State University, Columbus, OH, USA. Two transgenic Arabidopsis lines [FL4-4 and FL6-4; Columbia (Col) background] expressing organelle-targeted fluorescent proteins as well as offspring derived from crosses between the transgenic lines and mutants (parc6-1 × FL4-4, parc6-3 × FL4-4, parc6-4 × FL4-4, arc11-1 × FL4-4, and arc6-3 × FL6-4) were used (Chen et al, 2009;Itoh et al, 2010;Fujiwara et al, 2018;Itoh et al, 2018; see summary in Table 1). The parc6-5 (suba2) mutant was isolated from EMS-treated FL4-4 seeds carrying two nucleotide substitutions in the PARC6 coding sequence, resulting in G62R and W700stop mutations at the protein level (Itoh et al, 2018).…”

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

“…Previously, we screened an ethyl methanesulfonate (EMS)mutagenized population of Arabidopsis FL4-4 plants coexpressing a plastid stroma-targeted cyan fluorescent protein (CFP) and mitochondrial matrix-targeted yellow fluorescent protein (YFP) and isolated two independent recessive mutant lines, stromule biogenesis altered1 (suba1) and suba2, with abundant stromules in pavement cells (Itoh et al, 2018). Analysis of suba2 revealed that the causal gene responsible for the mutant phenotype was PARC6 (CDP1/ARC6H), a known chloroplast division-regulator gene (Glynn et al, 2009;Zhang et al, 2009;Ottesen et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…Isolation of the parc6-5 (suba2) mutant from leaf pavement cells (Itoh et al, 2018) provided us with an opportunity to comprehensively study plastid morphology in the leaf epidermis. Our initial investigation (Itoh et al, 2018) raised several questions. In this paper, we attempted to complement our former study and comprehensively understand PARC6mediated plastid morphologies in the leaf epidermis.…”

Section: Introductionmentioning

confidence: 99%

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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: Introductionsupporting

confidence: 66%

Section: Introductionsupporting

confidence: 59%

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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Chloroplasts with clefts and holes: a reassessment of the chloroplast shape using 3D FE-SEM cellular reconstruction of two species of Chlamydomonas

Sato,

Wakazaki

et al. 2024

Protoplasma

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Chloroplasts are usually considered spheroid organelles, but this is not the only shape of chloroplasts. The chloroplast of Chlamydomonas has been typically described as cup-shaped. However, in old studies, it was also modeled as a complex shape with “perforations” or windows. Here, we reconstructed the cellular architecture of Chlamydomonas reinhardtii and C. applanata using an array tomography system installed on a field emission scanning electron microscope. C. reinhardtii chloroplasts resembled a baseball glove or a cup without a side, featuring numerous large and small holes that may facilitate the transport of metabolites and proteins produced in the Golgi apparatus fitted in the holes. In a lipid-accumulating, high-light condition, the chloroplast volume increased by filling the side cleft with an entire wall. Many accumulated large lipid droplets were accommodated within the chloroplast holes, which could have been considered as “chloroplast lipid droplets.” Mitochondrial meshworks surrounded the chloroplast. C. applanata chloroplasts appeared like a folded starfish or a cup with many side clefts and a few holes. There was a single mitochondrion or two that branched in a complex form. Tight contacts of various organelles were also found in C. applanata. These reconstructions illustrate the complexity of chloroplast shape, which necessitates a revised understanding of the localization of lipid droplets and the evolution of chloroplasts: The prevailing image of the spheroid chloroplasts that reminds us of the similarity between chloroplasts and cyanobacteria is no longer tenable.

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Adaptive evolution of chloroplast division mechanisms during plant terrestrialization

Liu,

Yu,

Yang

et al. 2024

Cell Reports

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Isolation and analysis of a stromule‐overproducing Arabidopsis mutant suggest the role of PARC6 in plastid morphology maintenance in the leaf epidermis

Cited by 15 publications

References 67 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

Chloroplasts with clefts and holes: a reassessment of the chloroplast shape using 3D FE-SEM cellular reconstruction of two species of Chlamydomonas

Adaptive evolution of chloroplast division mechanisms during plant terrestrialization

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