Advanced

Mitochondrial plasmids, genetic conflicts and sex-determination in Silene vulgaris

Andersson, Helene LU (1999)
Abstract
Plants like all other eukaryotic organisms carry most of their DNA in the nucleus. In addition, plants also have both chloroplasts and mitochondria that contain their own genetic material. The genomes in chloroplasts and mitochondria control certain vital processes, but most often the organelles act under strict nuclear control. Usually the nuclear and organellar genomes live in "harmony", promoting themselves by helping each other. The mitochondrial and nuclear genomes can, however, sometimes end up in a conflict of interest. Cytoplasmic male sterility, is an example, where such a conflict may arise; in this case over the sexual development of carrier plants.



A factor complicating the organization and control of the... (More)
Plants like all other eukaryotic organisms carry most of their DNA in the nucleus. In addition, plants also have both chloroplasts and mitochondria that contain their own genetic material. The genomes in chloroplasts and mitochondria control certain vital processes, but most often the organelles act under strict nuclear control. Usually the nuclear and organellar genomes live in "harmony", promoting themselves by helping each other. The mitochondrial and nuclear genomes can, however, sometimes end up in a conflict of interest. Cytoplasmic male sterility, is an example, where such a conflict may arise; in this case over the sexual development of carrier plants.



A factor complicating the organization and control of the genetic material in plants even more, is the existence of mitochondrial plasmids. Mitochondrial plasmids have been reported to show deviations from strict maternal inheritance and to have effects on the sexual development of their carriers. These extrachromosomal genetic elements can be regarded as a third level of genome organization. In plants carrying mitochondrial plasmids conflicts of interest are therefore possible between three genetic actors: the chromosomes in the nucleus, the mitochondrial genome, and the plasmid DNA/RNA.



Theoretical models were set up to extend our understanding of how such conflicts can develop and to study which parameters are of importance for the spread and maintenance of mitochondrial plasmids in plant populations. They show that some degree of paternal transmission via pollen is important for the spread of mitochondrial plasmids. The analyses also show that the most likely long-term evolutionary direction is towards plasmids with weak phenotypic effects and a strict maternal mode of transmission.



To investigate the parameters for plasmid spread and evolution, we chose to study the naturally occurring weed Silene vulgaris, the bladder campion, a member of the Caryophyllaceae family, which carries mitochondrial plasmids. Three different length variants of mitochondrial plasmids of S. vulgaris could be recognized and they were distributed among populations over the whole investigated area of Skåne, the southernmost county of Sweden. The plasmids of S. vulgaris show no deviation from strict maternal inheritance. Neither were any effects detected on their host plants? fitness or sexual development that could be separated from effects caused by the background cytoplasm. The mitochondrial plasmids of S. vulgaris seem to have reached a state of almost perfect maternal transmission and of weak phenotypic effects, as predicted by the models.



The existence of male sterility in S. vulgaris cannot be explained by the occurrence of mitochondrial plasmids. However, there is evidence for both cytoplasmic and nuclear genes being involved in sex-determination. In S. vulgaris, as in several other gynodioecious species, so called gynomonoecious (i.e. partially male sterile) individuals are sometimes found. The standard explanation for the occurrence of this third gender is incomplete nuclear restoration of male-sterilizing cytoplasms. Here, an alternative interpretation is given to partial male sterility in S. vulgaris: Heteroplasmy of factors involved in sexual development can produce the mosaic of flowers found in gynomonoecious plants, as well as the differences in gender proportions among offspring from flowers of different types on a single plant. (Less)
Please use this url to cite or link to this publication:
author
opponent
  • Prof Hoekstra, Rolf, Wageningen Agricultural University, The Netherlands
organization
publishing date
type
Thesis
publication status
published
subject
keywords
Silene vulgaris, sex-determination, mitochondrial plasmids, genetic conflicts, Botanik, Botany
pages
152 pages
publisher
Department of Genetics, Lund University
defense location
Department of Genetics.
defense date
1999-10-02 10:15
external identifiers
  • Other:ISRN: LUNBDS/NBGE 1037/001-152 (1999)
language
English
LU publication?
yes
id
50d399d6-a8c7-4dd7-bbd6-962ef9576cd1 (old id 39883)
date added to LUP
2007-06-20 09:57:28
date last changed
2016-09-19 08:45:05
@misc{50d399d6-a8c7-4dd7-bbd6-962ef9576cd1,
  abstract     = {Plants like all other eukaryotic organisms carry most of their DNA in the nucleus. In addition, plants also have both chloroplasts and mitochondria that contain their own genetic material. The genomes in chloroplasts and mitochondria control certain vital processes, but most often the organelles act under strict nuclear control. Usually the nuclear and organellar genomes live in "harmony", promoting themselves by helping each other. The mitochondrial and nuclear genomes can, however, sometimes end up in a conflict of interest. Cytoplasmic male sterility, is an example, where such a conflict may arise; in this case over the sexual development of carrier plants.<br/><br>
<br/><br>
A factor complicating the organization and control of the genetic material in plants even more, is the existence of mitochondrial plasmids. Mitochondrial plasmids have been reported to show deviations from strict maternal inheritance and to have effects on the sexual development of their carriers. These extrachromosomal genetic elements can be regarded as a third level of genome organization. In plants carrying mitochondrial plasmids conflicts of interest are therefore possible between three genetic actors: the chromosomes in the nucleus, the mitochondrial genome, and the plasmid DNA/RNA.<br/><br>
<br/><br>
Theoretical models were set up to extend our understanding of how such conflicts can develop and to study which parameters are of importance for the spread and maintenance of mitochondrial plasmids in plant populations. They show that some degree of paternal transmission via pollen is important for the spread of mitochondrial plasmids. The analyses also show that the most likely long-term evolutionary direction is towards plasmids with weak phenotypic effects and a strict maternal mode of transmission.<br/><br>
<br/><br>
To investigate the parameters for plasmid spread and evolution, we chose to study the naturally occurring weed Silene vulgaris, the bladder campion, a member of the Caryophyllaceae family, which carries mitochondrial plasmids. Three different length variants of mitochondrial plasmids of S. vulgaris could be recognized and they were distributed among populations over the whole investigated area of Skåne, the southernmost county of Sweden. The plasmids of S. vulgaris show no deviation from strict maternal inheritance. Neither were any effects detected on their host plants? fitness or sexual development that could be separated from effects caused by the background cytoplasm. The mitochondrial plasmids of S. vulgaris seem to have reached a state of almost perfect maternal transmission and of weak phenotypic effects, as predicted by the models.<br/><br>
<br/><br>
The existence of male sterility in S. vulgaris cannot be explained by the occurrence of mitochondrial plasmids. However, there is evidence for both cytoplasmic and nuclear genes being involved in sex-determination. In S. vulgaris, as in several other gynodioecious species, so called gynomonoecious (i.e. partially male sterile) individuals are sometimes found. The standard explanation for the occurrence of this third gender is incomplete nuclear restoration of male-sterilizing cytoplasms. Here, an alternative interpretation is given to partial male sterility in S. vulgaris: Heteroplasmy of factors involved in sexual development can produce the mosaic of flowers found in gynomonoecious plants, as well as the differences in gender proportions among offspring from flowers of different types on a single plant.},
  author       = {Andersson, Helene},
  keyword      = {Silene vulgaris,sex-determination,mitochondrial plasmids,genetic conflicts,Botanik,Botany},
  language     = {eng},
  pages        = {152},
  publisher    = {ARRAY(0x93ad258)},
  title        = {Mitochondrial plasmids, genetic conflicts and sex-determination in Silene vulgaris},
  year         = {1999},
}