A genome-wide association study reveals a novel regulator of ovule number and fertility in Arabidopsis thaliana

Ovules contain the female gametophytes which are fertilized during pollination to initiate seed development. Thus, the number of ovules that are produced during flower development is an important determinant of seed crop yield and plant fitness. Mutants with pleiotropic effects on development often alter the number of ovules, but specific regulators of ovule number have been difficult to identify in traditional mutant screens. We used natural variation in Arabidopsis accessions to identify new genes involved in the regulation of ovule number. The ovule numbers per flower of 189 Arabidopsis accessions were determined and found to have broad phenotypic variation that ranged from 39 ovules to 84 ovules per pistil. Genome-Wide Association tests revealed several genomic regions that are associated with ovule number. T-DNA insertion lines in candidate genes from the most significantly associated loci were screened for ovule number phenotypes. The NEW ENHANCER of ROOT DWARFISM (NERD1) gene was found to have pleiotropic effects on plant fertility that include regulation of ovule number and both male and female gametophyte development. Overexpression of NERD1 increased ovule number per fruit in a background-dependent manner and more than doubled the total number of flowers produced in all backgrounds tested, indicating that manipulation of NERD1 levels can be used to increase plant productivity. Author summary Ovules are the precursors of seeds in flowering plants. Each ovule contains an egg cell and a central cell that fuse with two sperm cells during double fertilization to generate seeds containing an embryo and endosperm. The number of ovules produced during flower development determines the maximum number of seeds that can be produced by a flower. In this paper, we used natural variation in Arabidopsis thaliana accessions to identify regions of the genome that are associated with ovule number. Polymorphisms in the plant-specific NERD1 gene on chromosome 3 were significantly associated with ovule number. Mutant and overexpression analyses revealed that NERD1 is a positive regulator of ovule number, lateral branching, and flower number in Arabidopsis. Manipulation of NERD1 expression levels could potentially be used to increase yield in crop plants.