Differential impacts of FtsZ proteins on plastid division in the shoot apex of Arabidopsis

Swid, Neora; Nevo, Reinat; Kiss, Vladimir; Kapon, Ruti; Dagan, Shlomi; Snir, Orli; Adam, Zach; Falconet, Denis; Reich, Ziv; Charuvi, Dana

doi:10.1016/j.ydbio.2018.06.010

Cited by 11 publications

(9 citation statements)

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“…To derive the volume, 83, 0.5‐μm‐thick optical sections were collected for each sample. A correction for the distortion along the z ‐axis of the image was implemented as described previously (Swid et al., ). Chlorophyll was excited at 442 nm and the emitted fluorescence was collected using a 655–755 nm bandpass filter.…”

Section: Methodsmentioning

confidence: 99%

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Chlorophyll catabolism precedes changes in chloroplast structure and proteome during leaf senescence

et al. 2019

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The earliest visual changes of leaf senescence occur in the chloroplast as chlorophyll is degraded and photosynthesis declines. Yet, a comprehensive understanding of the sequence of catabolic events occurring in chloroplasts during natural leaf senescence is still missing. Here, we combined confocal and electron microscopy together with proteomics and biochemistry to follow structural and molecular changes during Arabidopsis leaf senescence. We observed that initiation of chlorophyll catabolism precedes other breakdown processes. Chloroplast size, stacking of thylakoids, and efficiency of PSII remain stable until late stages of senescence, whereas the number and size of plastoglobules increase. Unlike catabolic enzymes, whose level increase, the level of most proteins decreases during senescence, and chloroplast proteins are overrepresented among these. However, the rate of their disappearance is variable, mostly uncoordinated and independent of their inherent stability during earlier developmental stages. Unexpectedly, degradation of chlorophyll‐binding proteins lags behind chlorophyll catabolism. Autophagy and vacuole proteins are retained at relatively high levels, highlighting the role of extra‐plastidic degradation processes especially in late stages of senescence. The observation that chlorophyll catabolism precedes all other catabolic events may suggest that this process enables or signals further catabolic processes in chloroplasts.

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Section: Methodsmentioning

confidence: 99%

“…To derive the volume, 83, 0.5μm-thick optical sections were collected for each sample. A correction for the distortion along the z-axis of the image was implemented as described previously (Swid et al, 2018).…”

Section: Confocal Microscopymentioning

confidence: 99%

Chlorophyll catabolism precedes changes in chloroplast structure and proteome during leaf senescence

et al. 2019

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“…Differences in the levels of chloroplast-related gene expression could affect the biogenesis of chloroplast assembly and pigment contents, thus resulting in changes in Chl accumulation, Chl a/b, photosynthetic capacity, and leaf coloration [54,59]. In this regard, FtsZ1 and FtsZ2 in the FtsZ family of protein are key players in the initiation and progression of chloroplast division in plants and green algae [60,61]. The analysis of chloroplast-related DEGs, revealed a downregulated expression of the FtsZ1 gene in ch11 rice, indicating a potential deficiency in chloroplast cell division compared with the wt.…”

Section: Chloroplast-related Differentially Expressed Genes and Photosynthetic Capacitymentioning

confidence: 99%

Transcription Profile Analysis of Chlorophyll Biosynthesis in Leaves of Wild-Type and Chlorophyll b-Deficient Rice (Oryza sativa L.)

et al. 2021

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Photosynthesis is an essential biological process and a key approach for raising crop yield. However, photosynthesis in rice is not fully investigated. This study reported the photosynthetic properties and transcriptomic profiles of chlorophyll (Chl) b-deficient mutant (ch11) and wild-type rice (Oryza sativa L.). Chl b-deficient rice revealed irregular chloroplast development (indistinct membranes, loss of starch granules, thinner grana, and numerous plastoglobuli). Next-generation sequencing approach application revealed that the differential expressed genes were related to photosynthesis machinery, Chl-biosynthesis, and degradation pathway in ch11. Two genes encoding PsbR (PSII core protein), FtsZ1, and PetH genes, were found to be down-regulated. The expression of the FtsZ1 and PetH genes resulted in disrupted chloroplast cell division and electron flow, respectively, consequently reducing Chl accumulation and the photosynthetic capacity of Chl b-deficient rice. Furthermore, this study found the up-regulated expression of the GluRS gene, whereas the POR gene was down-regulated in the Chl biosynthesis and degradation pathways. The results obtained from RT-qPCR analyses were generally consistent with those of transcription analysis, with the exception of the finding that MgCH genes were up-regulated which enhance the important intermediate products in the Mg branch of Chl biosynthesis. These results indicate a reduction in the accumulation of both Chl a and Chl b. This study suggested that a decline in Chl accumulation is caused by irregular chloroplast formation and down-regulation of POR genes; and Chl b might be degraded via the pheophorbide b pathway, which requires further elucidation.

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“…Natural variation in chloroplast size or other aspects of chloroplast morphology has rarely been systematically investigated within a single species (Jellings et al, 1983). However, such differences have been reported between species (Honda et al, 1971;Jellings and Leech, 1984;Pyke and Leech, 1987), in different cell and tissue types within a species (Dengler et al, 1996;Pyke, 1997;Ahmadabadi and Bock, 2012;Stata et al, 2014;Swid et al, 2018), and under different environmental conditions (Boardman, 1977;Tsuji et al, 1979;Possingham et al, 1988;Filek et al, 2010;Li et al, 2013b;Takemura et al, 2017). Chloroplast size differences have been particularly well documented in response to light conditions.…”

Section: Discussionmentioning

confidence: 99%

“…Consequently, the difference in the severity of the mesophyll cell phenotypes in the ftsZ2-1 and ftsZ2-2 mutants was proposed to be attributable to differences in total FtsZ2 level in the two mutants (McAndrew et al, 2008;Schmitz et al, 2009). The three FtsZ proteins in Arabidopsis have also been shown to associate partly with thylakoid membranes (El-Kafafi et al, 2008;Karamoko et al, 2011) and to make distinct contributions to plastid division in the shoot apex (Swid et al, 2018).…”

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confidence: 99%

Allelic Variation in the Chloroplast Division Gene FtsZ2-2 Leads to Natural Variation in Chloroplast Size

et al. 2019

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Chloroplast size varies considerably in nature, but the underlying mechanisms are unknown. By exploiting a near-isogenic line population derived from a cross between the Arabidopsis (Arabidopsis thaliana) accessions Cape Verde Islands (Cvi-1), which has larger chloroplasts, and Landsberg erecta (Ler-0), with smaller chloroplasts, we determined that the large-chloroplast phenotype in Cvi-1 is associated with allelic variation in the gene encoding the chloroplast-division protein FtsZ2-2, a tubulin-related cytoskeletal component of the contractile FtsZ ring inside chloroplasts. Sequencing revealed that the Cvi-1 FtsZ2-2 allele encodes a C-terminally truncated protein lacking a region required for FtsZ2-2 interaction with inner-envelope proteins, and functional complementation experiments in a Columbia-0 ftsZ2-2 null mutant confirmed this allele as causal for the increased chloroplast size in Cvi-1. Comparison of FtsZ2-2 coding sequences in the 1001 Genomes database showed that the Cvi-1 allele is rare and identified additional rare loss-of-function alleles, including a natural null allele, in three other accessions, all of which had enlarged-chloroplast phenotypes. The ratio of nonsynonymous to synonymous substitutions was higher among the FtsZ2-2 genes than among the two other FtsZ family members in Arabidopsis, FtsZ2-1, a close paralog of FtsZ2-2, and the functionally distinct FtsZ1-1, indicating more relaxed constraint on the FtsZ2-2 coding sequence than on those of FtsZ2-1 or FtsZ1-1. Our results establish that allelic variation in FtsZ2-2 contributes to natural variation in chloroplast size in Arabidopsis, and they also demonstrate that natural variation in Arabidopsis can be used to decipher the genetic basis of differences in fundamental cell biological traits, such as organelle size. to K.W.O.) and by the National Science Foundation (grant no.

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Differential impacts of FtsZ proteins on plastid division in the shoot apex of Arabidopsis

Cited by 11 publications

References 60 publications

Chlorophyll catabolism precedes changes in chloroplast structure and proteome during leaf senescence

Chlorophyll catabolism precedes changes in chloroplast structure and proteome during leaf senescence

Transcription Profile Analysis of Chlorophyll Biosynthesis in Leaves of Wild-Type and Chlorophyll b-Deficient Rice (Oryza sativa L.)

Allelic Variation in the Chloroplast Division Gene FtsZ2-2 Leads to Natural Variation in Chloroplast Size

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