Organelle DNA degradation contributes to the efficient use of phosphate in seed plants

Takami, Toshihiro; Ohnishi, Norikazu; Kurita, Yuko; Iwamura, Shoko; Ohnishi, Miwa; Kusaba, Makoto; Mimura, Tetsuro; Sakamoto, Wataru

doi:10.1038/s41477-018-0291-x

Cited by 43 publications

(34 citation statements)

References 65 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Plastid and mitochondrial DNAs in plants cells are organized in nucleoids [ 44 , 45 ]. The organization and distribution of chloroplast nucleoids can indicate chloroplast differentiation or degradation status [ 46 , 47 ] and, as chloroplast nucleoids are important in chloroplast gene expression, development, and phosphate supply, their analysis can provide valuable information regarding leaf physiology [ 48 , 49 , 50 , 51 , 52 ]. Therefore, we questioned whether chloroplast nucleoid formation might be affected in chlorosis-inducing mutants such as Ar50-33-pg1.…”

Section: Resultsmentioning

confidence: 99%

An Argon-Ion-Induced Pale Green Mutant of Arabidopsis Exhibiting Rapid Disassembly of Mesophyll Chloroplast Grana

Sanjaya

Kazama

Ishii

et al. 2021

Plants

View full text Add to dashboard Cite

Argon-ion beam is an effective mutagen capable of inducing a variety of mutation types. In this study, an argon ion-induced pale green mutant of Arabidopsis thaliana was isolated and characterized. The mutant, designated Ar50-33-pg1, exhibited moderate defects of growth and greening and exhibited rapid chlorosis in photosynthetic tissues. Fluorescence microscopy confirmed that mesophyll chloroplasts underwent substantial shrinkage during the chlorotic process. Genetic and whole-genome resequencing analyses revealed that Ar50-33-pg1 contained a large 940 kb deletion in chromosome V that encompassed more than 100 annotated genes, including 41 protein-coding genes such as TYRAAt1/TyrA1, EGY1, and MBD12. One of the deleted genes, EGY1, for a thylakoid membrane-localized metalloprotease, was the major contributory gene responsible for the pale mutant phenotype. Both an egy1 mutant and F1 progeny of an Ar50-33-pg1 × egy1 cross-exhibited chlorotic phenotypes similar to those of Ar50-33-pg1. Furthermore, ultrastructural analysis of mesophyll cells revealed that Ar50-33-pg1 and egy1 initially developed wild type-like chloroplasts, but these were rapidly disassembled, resulting in thylakoid disorganization and fragmentation, as well as plastoglobule accumulation, as terminal phenotypes. Together, these data support the utility of heavy-ion mutagenesis for plant genetic analysis and highlight the importance of EGY1 in the structural maintenance of grana in mesophyll chloroplasts.

show abstract

Section: Resultsmentioning

confidence: 99%

An Argon-Ion-Induced Pale Green Mutant of Arabidopsis Exhibiting Rapid Disassembly of Mesophyll Chloroplast Grana

Sanjaya

Kazama

Ishii

et al. 2021

Plants

View full text Add to dashboard Cite

show abstract

“…Dismissal of the mtDNA in germinative pollen would be because of selective degradation, and several nucleases have been identified that could be involved [71]. The degradation of organellar DNA by exonucleases could be also a mean for rapid access to phosphate when plants are exposed to nutrient-deficient conditions [72].…”

Section: Structure Of Plant Organellar Genomesmentioning

confidence: 99%

DNA Repair and the Stability of the Plant Mitochondrial Genome

Chevigny

Schatz-Daas

Lotfi

et al. 2020

IJMS

120

View full text Add to dashboard Cite

The mitochondrion stands at the center of cell energy metabolism. It contains its own genome, the mtDNA, that is a relic of its prokaryotic symbiotic ancestor. In plants, the mitochondrial genetic information influences important agronomic traits including fertility, plant vigor, chloroplast function, and cross-compatibility. Plant mtDNA has remarkable characteristics: It is much larger than the mtDNA of other eukaryotes and evolves very rapidly in structure. This is because of recombination activities that generate alternative mtDNA configurations, an important reservoir of genetic diversity that promotes rapid mtDNA evolution. On the other hand, the high incidence of ectopic recombination leads to mtDNA instability and the expression of gene chimeras, with potential deleterious effects. In contrast to the structural plasticity of the genome, in most plant species the mtDNA coding sequences evolve very slowly, even if the organization of the genome is highly variable. Repair mechanisms are probably responsible for such low mutation rates, in particular repair by homologous recombination. Herein we review some of the characteristics of plant organellar genomes and of the repair pathways found in plant mitochondria. We further discuss how homologous recombination is involved in the evolution of the plant mtDNA.

show abstract

“…Rowan et al , ; Oldenburg et al , ; Shaver et al , ; Rowan et al , ), starts later, but before symptoms of senescence become visible (Baumgartner et al , ; Sodmergen et al , ) or is rather kept at high copy numbers and remains functionally active until senescence, needs to be resolved (e.g. discussion in Golczyk et al , ; Oldenburg et al , ; Sakamoto and Takami, ; Takami et al , ). Comparably, it needs to be clarified whether or not plastid genes and genomes are inactivated by mutations and degraded to non‐functional fragments in mature, photosynthetically active mesophyll cells (Kumar et al , ; Oldenburg et al , ; Kumar et al , ) or remain intact (e.g.…”

Section: Introductionmentioning

confidence: 99%

Chloroplast nucleoids are highly dynamic in ploidy, number, and structure during angiosperm leaf development

et al. 2020

View full text Add to dashboard Cite

Chloroplast nucleoids are large, compact nucleoprotein structures containing multiple copies of the plastid genome. Studies on structural and quantitative changes of plastid DNA (ptDNA) during leaf development are scarce and have produced controversial data. We have systematically investigated nucleoid dynamics and ptDNA quantities in the mesophyll of Arabidopsis, tobacco, sugar beet, and maize from the early postmeristematic stage until necrosis. DNA of individual nucleoids was quantified by DAPI-based supersensitive epifluorescence microscopy. Nucleoids occurred in scattered, stacked, or ring-shaped arrangements and in recurring patterns during leaf development that was remarkably similar between the species studied. Nucleoids per organelle varied from a few in meristematic plastids to >30 in mature chloroplasts (corresponding to about 20-750 nucleoids per cell). Nucleoid ploidies ranged from haploid to >20-fold even within individual organelles, with average values between 2.6-fold and 6.7-fold and little changes during leaf development. DNA quantities per organelle increased gradually from about a dozen plastome copies in tiny plastids of apex cells to 70-130 copies in chloroplasts of about 7 lm diameter in mature mesophyll tissue, and from about 80 plastome copies in meristematic cells to 2600-3300 copies in mature diploid mesophyll cells without conspicuous decline during leaf development. Pulsed-field electrophoresis, restriction of highmolecular-weight DNA from chloroplasts and gerontoplasts, and CsCl equilibrium centrifugation of singlestranded and double-stranded ptDNA revealed no noticeable fragmentation of the organelle DNA during leaf development, implying that plastid genomes in mesophyll tissues are remarkably stable until senescence.

show abstract

Organelle DNA degradation contributes to the efficient use of phosphate in seed plants

Abstract: DNA retained in the endosymbiotic organelles-chloroplasts and mitochondria-of seed plants influences growth in phosphate-limited conditions through a degradation mechanism implemented by DPD1 exonuclease.

Cited by 43 publications

References 65 publications

An Argon-Ion-Induced Pale Green Mutant of Arabidopsis Exhibiting Rapid Disassembly of Mesophyll Chloroplast Grana

An Argon-Ion-Induced Pale Green Mutant of Arabidopsis Exhibiting Rapid Disassembly of Mesophyll Chloroplast Grana

DNA Repair and the Stability of the Plant Mitochondrial Genome

Chloroplast nucleoids are highly dynamic in ploidy, number, and structure during angiosperm leaf development

Contact Info

Product

Resources

About