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

SummaryChloroplast 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 mesophyll ofArabidopsis, tobacco, sugar beet, and maize from the early post-meristematic 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 remarkably similar between the species studied. Nucleoids per organelle varied from 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- 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 μm diameter in mature mesophyll tissue, and from about 80 plastome copies in meristematic cells to 2,600-3,300 copies in mature diploid mesophyll cells without conspicuous decline during leaf development. Pulsed-field electrophoresis, restriction of high-molecular weight DNA from chloroplasts and gerontoplasts, and CsCl equilibrium centrifugation of single- 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.Significance StatementPlastid DNA is organized in nucleoids that are highly dynamic in organization, structure and amount during leaf development. The present investigation fully resolves now this dynamic and is a precise cytogenetic characterization of nucleoids DNA spanning the entire life cycle of the leaf.

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Leaf development in Lolium temulentum: Gradients of RNA complement and plastid and non-plastid transcripts

Physiologia Plantarum ◽

10.1034/j.1399-3054.1990.790218.x ◽

1990 ◽

Vol 79 (2) ◽

pp. 331-338 ◽

Cited By ~ 3

Author(s):

Helen J. Ougham ◽

T. G. E. Davies

Keyword(s):

Leaf Development ◽

Lolium Temulentum

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Faculty Opinions recommendation of Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1019302.218473 ◽

2004 ◽

Author(s):

Miltos Tsiantis

Keyword(s):

Leaf Development

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Faculty Opinions recommendation of Restoration of DWF4 expression to the leaf margin of a dwf4 mutant is sufficient to restore leaf shape but not size: the role of the margin in leaf development.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1096017.554691 ◽

2007 ◽

Author(s):

Lieven De Veylder

Keyword(s):

Leaf Development ◽

Leaf Shape ◽

Leaf Margin

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Faculty Opinions recommendation of Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.11049958.12003056 ◽

2011 ◽

Author(s):

Tomomichi Fujita

Keyword(s):

Cell Cycle ◽

Cell Proliferation ◽

Osmotic Stress ◽

Cell Cycle Arrest ◽

Leaf Development ◽

Ethylene Signaling ◽

Cycle Arrest

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Faculty Opinions recommendation of A conserved molecular framework for compound leaf development.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1141874.600019 ◽

2009 ◽

Author(s):

David Smyth

Keyword(s):

Leaf Development ◽

Compound Leaf ◽

Molecular Framework

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Transcriptome Analysis of Ginkgo biloba L. Leaves across Late Developmental Stages Based on RNA-Seq and Co-Expression Network

Forests ◽

10.3390/f12030315 ◽

2021 ◽

Vol 12 (3) ◽

pp. 315

Author(s):

Hailin Liu ◽

Xin Han ◽

Jue Ruan ◽

Lian Xu ◽

Bing He

Keyword(s):

Ginkgo Biloba ◽

Leaf Development ◽

Developmental Stages ◽

Leaf Growth ◽

Rna Seq ◽

Final Size ◽

Dioecious Species ◽

Related Factors ◽

New Genes ◽

Gene Modules

The final size of plant leaves is strictly controlled by environmental and genetic factors, which coordinate cell expansion and cell cycle activity in space and time; however, the regulatory mechanisms of leaf growth are still poorly understood. Ginkgo biloba is a dioecious species native to China with medicinally and phylogenetically important characteristics, and its fan-shaped leaves are unique in gymnosperms, while the mechanism of G. biloba leaf development remains unclear. In this study we studied the transcriptome of G. biloba leaves at three developmental stages using high-throughput RNA-seq technology. Approximately 4167 differentially expressed genes (DEGs) were obtained, and a total of 12,137 genes were structure optimized together with 732 new genes identified. More than 50 growth-related factors and gene modules were identified based on DEG and Weighted Gene Co-expression Network Analysis. These results could remarkably expand the existing transcriptome resources of G. biloba, and provide references for subsequent analysis of ginkgo leaf development.

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Genome-wide analysis of changes in miRNA and target gene expression reveals key roles in heterosis for Chinese cabbage biomass

Horticulture Research ◽

10.1038/s41438-021-00474-6 ◽

2021 ◽

Vol 8 (1) ◽

Author(s):

Peirong Li ◽

Tongbing Su ◽

Deshuang Zhang ◽

Weihong Wang ◽

Xiaoyun Xin ◽

...

Keyword(s):

Chinese Cabbage ◽

Leaf Development ◽

Target Genes ◽

Expression Patterns ◽

Seedling Stage ◽

Differentially Expressed ◽

Small Rna Sequencing ◽

Leaf Morphogenesis ◽

Expression Levels ◽

Parental Lines

AbstractHeterosis is a complex phenomenon in which hybrids show better phenotypic characteristics than their parents do. Chinese cabbage (Brassica rapa L. spp. pekinensis) is a popular leafy crop species, hybrids of which are widely used in commercial production; however, the molecular basis of heterosis for biomass of Chinese cabbage is poorly understood. We characterized heterosis in a Chinese cabbage F1 hybrid cultivar and its parental lines from the seedling stage to the heading stage; marked heterosis of leaf weight and biomass yield were observed. Small RNA sequencing revealed 63 and 50 differentially expressed microRNAs (DEMs) at the seedling and early-heading stages, respectively. The expression levels of the majority of miRNA clusters in the F1 hybrid were lower than the mid-parent values (MPVs). Using degradome sequencing, we identified 1,819 miRNA target genes. Gene ontology (GO) analyses demonstrated that the target genes of the MPV-DEMs and low parental expression level dominance (ELD) miRNAs were significantly enriched in leaf morphogenesis, leaf development, and leaf shaping. Transcriptome analysis revealed that the expression levels of photosynthesis and chlorophyll synthesis-related MPV-DEGs (differentially expressed genes) were significantly different in the F1 hybrid compared to the parental lines, resulting in increased photosynthesis capacity and chlorophyll content in the former. Furthermore, expression of genes known to regulate leaf development was also observed at the seedling stage. Arabidopsis plants overexpressing BrGRF4.2 and bra-miR396 presented increased and decreased leaf sizes, respectively. These results provide new insight into the regulation of target genes and miRNA expression patterns in leaf size and heterosis for biomass of B. rapa.

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