A TILLING allele of the tomato Aux/IAA9 gene offers new insights into fruit set mechanisms and perspectives for breeding seedless tomatoes

Abstract

Parthenocarpy is a desired trait in fruit crops; it enables fruit set under environmental conditions suboptimal for pollination, and seedless fruits represent a valuable consumer product. We employed TILLING-based screening of a mutant tomato population to find genetic lesions in Aux/IAA9, a negative regulator of the auxin response involved in the control of fruit set. We identified three mutations located in the coding region of this gene, including two singlebase substitutions and one single-base deletion, which leads to a frame shift and premature stop codon. The transcription of IAA9 was strongly reduced in the frame-shift mutant, and partial loss of mutated protein activity was evidenced by an in vitro transactivation assay. Whereas missense mutations were predicted to be tolerated and did not cause mutant phenotypes, the frame-shift mutation-induced phenotypes expected for a loss of IAA9 function, including altered axillary shoot growth, reduced leaf compoundness and a strong tendency to produce parthenocarpic fruits. Mutant flowers showed pleiotropic anther cone defects, a phenotype frequently associated with parthenocarpy in tomato and other species. Mutant fruits were larger than those of the seeded control, with higher brix values and similar firmness. Fruit set was higher in the mutant than in wild type in the greenhouse, but lower in the open field. Facultative expression of parthenocarpy indicated that the mutant is suitable for hybrid seed production and for increasing seeds of parental lines. The results highlight the utility of this novel IAA9 allele for exploiting parthenocarpy by breeding tomato adapted to pollination-limiting growth conditions.