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The linear plastid chromosomes of maize: terminal sequences, structures, and implications for DNA replication

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Abstract

The structure of a chromosomal DNA molecule may influence the way in which it is replicated and inherited. For decades plastid DNA (ptDNA) was believed to be circular, with breakage invoked to explain linear forms found upon extraction from the cell. Recent evidence indicates that ptDNA in vivo consists of linear molecules with discrete termini, although these ends were not characterized. We report the sequences of two terminal regions, End1 and End2, for maize (Zea mays L.) ptDNA. We describe structural features of these terminal regions and similarities found in other plant ptDNAs. The terminal sequences are within inverted repeat regions (leading to four genomic isomers) and adjacent to origins of replication. Conceptually, stem-loop structures may be formed following melting of the double-stranded DNA ends. Exonuclease digestion indicates that the ends in maize are unobstructed, but tobacco (Nicotiana tabacum L.) ends may have a 5′-protein. If the terminal structure of ptDNA molecules influences the retention of ptDNA, the unprotected molecular ends in mature leaves of maize may be more susceptible to degradation in vivo than the protected ends in tobacco. The terminal sequences and cumulative GC skew profiles are nearly identical for maize, wheat (Triticum aestivum L.) and rice (Oryza sativa L.), with less similarity among other plants. The linear structure is now confirmed for maize ptDNA and inferred for other plants and suggests a virus-like recombination-dependent replication mechanism for ptDNA. Plastid transformation vectors containing the terminal sequences may increase the chances of success in generating transplastomic cereals.

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Abbreviations

DB:

Dilution buffer

HSB:

High salt buffer

HSV:

Herpes simplex virus

IR:

Inverted repeat

LSC:

Long single copy

mtDNA:

Mitochondrial DNA

OBP:

Origin binding protein

ori :

Origin of replication

PFGE:

Pulsed-field gel electrophoresis

PK:

Proteinase K

ptDNA:

Plastid DNA

RDR:

Recombination-dependent replication

SSBP:

Single-strand binding protein

SSC:

Short single copy

SSA:

Single-strand annealing

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Acknowledgments

This research was funded by the Junat Fund (a private charitable fund).

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Authors and Affiliations

  1. Department of Biology, University of Washington, Box 355325, Seattle, WA, 98195-5325, USA

    Delene J. Oldenburg & Arnold J. Bendich

Authors
  1. Delene J. Oldenburg
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  2. Arnold J. Bendich
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Corresponding author

Correspondence to Arnold J. Bendich.

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Conflict of interest

The authors DO and AB are co-inventers for the patent application: “Plastid Transformation Using Linear DNA Vectors”; application nos. PCT/US2013/030775, WO2014/065857A1. The linear vectors described in this patent are based on the terminal ptDNA sequences reported in this manuscript.

Additional information

Communicated by M. Kupiec.

Electronic supplementary material

Below is the link to the electronic supplementary material.

294_2015_548_MOESM1_ESM.pdf

Supplementary material 1 (PDF 1370 kb) Online Resource 1: Comparisons of maize ptDNA end sequences to sequences from other ptDNAs; sequence alignments and amount of similarity are shown

294_2015_548_MOESM2_ESM.pdf

Supplementary material 2 (PDF 365 kb) Online Resource 2: GC skew plots of the plastid genomes from several land plants and the protist Euglena gracilis and viral genome of herpes simplex

Supplementary material 3 (PDF 855 kb) Online Resource 3: Exonuclease digestion and PFGE of maize and tobacco ptDNAs

294_2015_548_MOESM4_ESM.pdf

Supplementary material 4 (PDF 383 kb) Online Resource 4: Secondary structure prediction of the terminal sequences from maize, rice, and wheat

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Oldenburg, D.J., Bendich, A.J. The linear plastid chromosomes of maize: terminal sequences, structures, and implications for DNA replication. Curr Genet 62, 431–442 (2016). https://doi.org/10.1007/s00294-015-0548-0

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  • DOI: https://doi.org/10.1007/s00294-015-0548-0

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