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Proc Natl Acad Sci U S A. 2016 Oct 25;113(43):12226-12231. Epub 2016 Oct 11.

Germline replications and somatic mutation accumulation are independent of vegetative life span in Arabidopsis.

Author information

1
Gregor Mendel Institute of Plant Molecular Biology, Austrian Academy of Sciences, Vienna Biocenter, 1030 Vienna, Austria.
2
Central European Institute of Technology, Masaryk University, 612 65 Brno, Czech Republic.
3
Gregor Mendel Institute of Plant Molecular Biology, Austrian Academy of Sciences, Vienna Biocenter, 1030 Vienna, Austria; Central European Institute of Technology, Masaryk University, 612 65 Brno, Czech Republic karel.riha@ceitec.muni.cz.

Abstract

In plants, gametogenesis occurs late in development, and somatic mutations can therefore be transmitted to the next generation. Longer periods of growth are believed to result in an increase in the number of cell divisions before gametogenesis, with a concomitant increase in mutations arising due to replication errors. However, there is little experimental evidence addressing how many cell divisions occur before gametogenesis. Here, we measured loss of telomeric DNA and accumulation of replication errors in Arabidopsis with short and long life spans to determine the number of replications in lineages leading to gametes. Surprisingly, the number of cell divisions within the gamete lineage is nearly independent of both life span and vegetative growth. One consequence of the relatively stable number of replications per generation is that older plants may not pass along more somatically acquired mutations to their offspring. We confirmed this hypothesis by genomic sequencing of progeny from young and old plants. This independence can be achieved by hierarchical arrangement of cell divisions in plant meristems where vegetative growth is primarily accomplished by expansion of cells in rapidly dividing meristematic zones, which are only rarely refreshed by occasional divisions of more quiescent cells. We support this model by 5-ethynyl-2'-deoxyuridine retention experiments in shoot and root apical meristems. These results suggest that stem-cell organization has independently evolved in plants and animals to minimize mutations by limiting DNA replication.

KEYWORDS:

germline; mismatch repair; mutation rate; shoot apical meristem; telomeres

PMID:
27729523
PMCID:
PMC5087024
DOI:
10.1073/pnas.1609686113
[Indexed for MEDLINE]
Free PMC Article

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