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Sexual gene shuffling suppressed in plants
Asexual cell division could hold the key to a breakthrough in plant breeding.

Using a combination of three genetic mutations, plant researchers have disrupted the usual process of genetic shuffling during the formation of reproductive cells — male pollen and female ova. These triple mutant plants instead produce pollen and ova genetically identical to the cells of the parent plant by simple mitotic cell division.

The results, published today in PLoS Biology could bring plant breeders a step closer to generating crops that produce their seeds completely asexually — a process called apomixis[1].

Such crops have long been sought because harnessing apomixis would dramatically accelerate plant breeding. The hybrid offspring of crosses between two different cultivars of a crop plant often tend to produce higher yields. But when hybrids are allowed to self-fertilize to produce the next generation of seeds, the intricate genetic networks that brought about this 'hybrid vigor' are shuffled, generating offspring that are often not as vigorous as their parent.

Some plants, such as grape vines, can be propagated asexually using cuttings — but not crops such as corn or wheat. For plant breeders, it would be much simpler — and cheaper — if the hybrids could simply clone themselves in large numbers by apomixis.

Unfortunately, of the more than 400 flowering plants known to reproduce by apomixis — which include dandelions and blackberries — few are crops. The concept of engineering apomixis in crops is so enticing that it was featured in a 2007 mystery novel called Day of the Dandelion by Peter Pringle, in which a secret agent-cum-botanist hunts for a missing researcher believed to have discovered an apomixis 'supergene'.

In reality, no supergene has ever been found. Instead, researchers believe that a combination of genes or particular mutations will be needed to engineer an apomictic crop plant.

The new work, by Raphaël Mercier of the French National Institute for Agricultural Research in Versailles and his colleagues, addresses one important hurdle in apomixis research: the need to engineer plants that generate their reproductive cells by mitosis rather than by meiosis, the form of cell division that shuffles the genome and passes different selections of genes into each reproductive cell. Their results could dramatically stimulate the field, says plant geneticist Peter van Dijk of Keygene, a plant breeding company based in Wageningen, The Netherlands. "I really think it's a breakthrough."

Day of the Arabidopsis

Mercier and his colleagues searched for genes in the model plant Arabidopsis thaliana that were likely to be associated with meiosis — on the basis of where and when the genes were expressed. They found one that they named omission of second division (OSD1) because plants mutant for this gene lacked the second round of cell division that occurs during meiosis.

When the researchers combined mutations in the OSD1 gene with mutations in two other genes that affect meiosis, the resulting plants lacked meiosis altogether, and produced their reproductive cells by mitosis. Because they lack the reduction division of meiosis, these cells are diploid (containing two copies of the genome), like the body cells of the plant, rather than haploid (containing one copy of the genome) like normal reproductive cells.

The triple mutants are reminiscent of a mutant reported last year by Imran Siddiqi and his colleagues at the Centre for Cellular and Molecular Biology in Hyderabad, India[2]. That mutant, called dyad, also produced female reproductive cells by mitosis rather than meiosis, but only at low frequency, and only rarely produced viable seeds after fertilization. In contrast, the triple mutants created by Mercier and his colleagues produced as many reproductive cells as normal Arabidopsis plants, and fertilization produced viable triploid and tetraploid seeds.

The results are encouraging, says Ueli Grossniklaus, a plant developmental biologist at the University of Zurich, but one practical limitation is the reliance upon mutations in three different genes. "If we want to apply this, eventually we'll have to combine these three traits with other desirable traits," he says. "And the more genes you have to bring together, the harder it will be."

Achieving apomixis is still a distant goal, however. Researchers must first find out how to engineer crop plants to produce viable seeds from diploid reproductive cells without fertilization — a process called parthenogenesis. If there is no meiosis, fertilization causes the chromosome number of the offspring to double in each generation, an undesirable outcome.

About a decade ago, researchers found what appears to be another key component of apomixis: mutants that produced endosperm — the nutritive tissue that surrounds the plant embryo in the seed — without first being fertilized[3]. That finding drove many researchers to enter the field, says van Dijk. "They thought it would be very easy to engineer apomixis," he says. "Now very few of these people are still working in the field — they found out it is quite difficult."

References
1. d’Erfurth, I. et al. PLoS Biol. 7, e1000124 (2009).
2. Ravi, M., Marimuthu, M.P.A. & Siddiqi, I. Nature 451, 1121–1124 (2008).
3. Chaudhury, A.M. et al. Proc. Natl Acad. Sci. USA 94, 4223- 4228 (1997).

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