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Shedding light on cytoplasmic male sterility

Georges Pelletier was the first winner of INRA’s Agricultural Research Award in 2006. When asked to describe his most significant contributions, he starts by citing cytoplasmic male sterility: "The research took over 15 years, starting in the 1980s, and was riddled with technical challenges. But when you compare what we thought then and what we know now, you really see how scientific understanding has progressed”.  

Tobacco protoplasts. © INRA, PELLETIER Georges
By Pascale Mollier, translated by Inge Laino
Updated on 04/15/2016
Published on 06/08/2006

Obtaining hybrids thanks to cytoplasmic male sterility

The research began with a practical question: how can hybrids easily be obtained in plants that fertilize themselves? Hybrids, known to boost productivity, are the result of crossing parent plants that are sufficiently genetically distant. A common procedure consists of using sterile male plants whose stamens do not produce viable pollen, thereby preventing self-fertilisation. These sterile male plants only appear spontaneously in certain species, such as maize or radish. Most often, they are the result of combining the cytoplasm of one species with the nuclear genome of another. The two species must be sufficiently similar for the combination to be viable sexually. They transmit male sterility through their cellular cytoplasm, which, in plants as in animals, usually comes from the female gamete during fertilisation.  

Male sterility: it’s all in the mitochondria

At this stage, Georges Pelletier initiated research to understand which cytoplasmic compartment the sterility trait came from. Sterility can be found in the chloroplast genome, the mitochondrial genome, or, like an illness, it can be introduced by a virus. With this in mind, Georges Pelletier had the idea to do in vitro breeding, in which the two partners contribute their cytoplasm. This is possible in plants by fusing protoplasts, cells with no cell wall that are able to generate whole new plants. By fusing the protoplast of normal tobacco and that of sterile male tobacco, he obtained plants with an intermediate morphology: the flowers were abnormal but not as atrophied as the sterile male parent. Therefore, normal cytoplasm played a role, combining with the sterile male cytoplasm. Georges Pelletier and his team showed that in these individual plants, only mitochondria underwent genetic changes. It is therefore in the mitochondrial genome that the cytoplasmic male sterility trait is found - a finding that was published in Nature in 1979.

Sterile male rapeseed

Georges Pelletier then decided to see if this phenomenon was widespread by carrying out the same experiments in another species. He chose rapeseed, a species for which breeders lack efficient sterile male plants. The plants that were then available, rapeseed having cytoplasmic male sterility from radish, were chlorophyll-deficient, because their chloroplasts develop poorly. Moreover, their flowers were so atrophied that they could not produce nectar and did not attract pollinators. Indeed, the rapeseed genome does not work well with radish cytoplasm. Georges Pelletier and his team set out to fuse protoplasts between rapeseed with radish cytoplasm and normal rapeseed. Like with tobacco, they obtained plants with an intermediate morphology that recovered functional chloroplasts, and whose flowers produced nectar. These plants led to the development of many other varieties of cabbage and rapeseed now grown throughout the world.

The male sterility gene identified

From these plants, another decisive step will be taken. Their mitochondrial genome is a combination of mitochondrial genomes from rapeseed and radish. Little by little, Georges Pelletier eliminated the radish part, while retaining the male sterility trait by repeated fusions with rapeseed protoplasts. The result was an unstable plant, some of whose flowers were male and sterile, and others normal. He compared the mitochondrial genomes of these two types of flowers, and showed that they only differed by one single gene, which was unknown until then. His work was therefore ground-breaking in that he revealed, for the first time ever, the molecular support of cytoplasmic male sterility in these species.

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Plant Biology and Breeding
Associated Centre(s):
Versailles-Grignon

References

Belliard G, Vedele F, Pelletier G. 1979. Mitochondrial recombination in cytoplasmic hybrids of Nicotiana by protoplast fusion. Nature 281, 401-403

Pelletier G, Primard C, Vedele F, Chetrit P, Remy R, Rousselle P, Renard M.1983. Intergeneric cytoplasmic hybridization in Cruciferae by protoplast fusion. Mol Gen Genet. 191, 244-250

Bonhomme S., Budar F., Lancelin D., Small I., Defrance M-C., Pelletier G. 1992. Sequence and transcript analysis of the Nco2.5 Ogura-specific fragment correlated with cytoplasmic male sterility in Brassica cybridsMol Gen Genet. Nov 235 , 340-348