Tomato agamous-like6 parthenocarpy is facilitated by ovule integument reprogramming involving the growth regulator KLUH

Abstract

Abstract Fruit set is established during and soon after fertilization of the ovules inside the quiescent ovary, but the signaling pathways involved remain obscure. The tomato (Solanum lycopersicum) CRISPR loss-of-function mutant of the transcription factor gene AGAMOUS-like6 (SlAGL6; slagl6CR-sg1) is capable of fertilization-independent setting of normal, yet seedless (parthenocarpic), fruit. To gain insight into the mechanism of fleshy fruit set, in this study, we investigated how slagl6CR-sg1 uncouples fruit set from fertilization. We found that mutant ovules were enlarged due to integument over-proliferation and failed to differentiate an endothelium, the integument’s innermost layer, upon maturation. A causal relationship between slagl6 loss-of-function and these abnormal phenotypes is inferred from the observation that SlAGL6 is predominantly expressed in the immature ovule integument, and upon ovule maturation, its expression shifts to the endothelium. The transcriptome of unfertilized mutant ovules profoundly differs from that of wild-type and exhibits substantial overlap with the transcriptomes of fertilized ovules sporophytic tissues. One prominent upregulated gene was the fertilization-induced cytochrome P450 cell proliferation regulator SlKLUH. Indeed, ectopic overexpression of SlKLUH stimulated both integument growth in unfertilized ovules and parthenocarpy, suggesting that its suppression by SlAGL6 is paramount for preventing fertilization-independent fruit set. Taken together, our study informs on the transcriptional programs that are regulated by SlAGL6 and demonstrates that it acts from within the ovule integument to inhibit ovary growth beyond anthesis. That by suppressing components of the fertilization-induced ovule reprogramming underlying fruit set.