Mutations in AtPS1 (Arabidopsis thaliana Parallel Spindle 1) Lead to the Production of Diploid Pollen Grains

Abstract

Polyploidy has had a considerable impact on the evolution of many eukaryotes, especially angiosperms. Indeed, most—if not all—angiosperms have experienced at least one round of polyploidy during the course of their evolution, and many important crop plants are current polyploids. The occurrence of 2n gametes (diplogametes) in diploid populations is widely recognised as the major source of polyploid formation. However, limited information is available on the genetic control of diplogamete production. Here, we describe the isolation and characterisation of the first gene, AtPS1 (Arabidopsis thaliana Parallel Spindle 1), implicated in the formation of a high frequency of diplogametes in plants. Atps1 mutants produce diploid male spores, diploid pollen grains, and spontaneous triploid plants in the next generation. Female meiosis is not affected in the mutant. We demonstrated that abnormal spindle orientation at male meiosis II leads to diplogamete formation. Most of the parent's heterozygosity is therefore conserved in the Atps1 diploid gametes, which is a key issue for plant breeding. The AtPS1 protein is conserved throughout the plant kingdom and carries domains suggestive of a regulatory function. The isolation of a gene involved in diplogamete production opens the way for new strategies in plant breeding programmes and progress in evolutionary studies. In the life cycle of sexual organisms, meiosis reduces the number of chromosomes from two sets (2n) to one set (n), while fertilization restores the original chromosome number. However, in case of failure of meiosis to reduce the chromosome number, the fecundation involving the obtained 2n gametes can lead to the formation of an organism with more than two sets of chromosomes (polyploid). Polyploidization occurred widely in the course of evolution of eukaryotes, especially of plants. Besides, many crops are current polyploids, and 2n gametes have been useful for their genetic improvement by allowing crosses between 2n and 4n species. 2n gametes formation is known to be under genetic control but none of the genes involved were identified. We have isolated and characterised a gene (AtPS1) involved in controlling diploid (2n) gamete formation in A. thaliana. In the Atps1 mutant, the second division of meiosis is disturbed, leading to the gathering of chromosomes that had been separated at the first division. Consequently, Atps1 mutants produce 2n male gametes and spontaneous triploid plants in the next generation. The isolation of a gene involved in diplogamete production opens the way for new strategies in plant breeding programmes and progress in evolutionary studies.