Loss of function of the Pad-1 aminotransferase gene, which is involved in auxin homeostasis, induces parthenocarpy in Solanaceae plants

Satoshi Matsuo, Koji Miyatake, Makoto Endo, Soichi Urashimo, Takaaki Kawanishi, Satomi Negoro, Satoshi Shimakoshi, and Hiroyuki Fukuoka

PNAS June 9, 2020 117 (23) 12784-12790

Significance

Parthenocarpy, which is the growth of the ovary into a fruit without pollination and/or fertilization, is a highly attractive agronomic trait for growers to overcome the problems of low fruit yield under unfavorable environmental conditions. Moreover, parthenocarpy is desirable for consumers because the resulting fruits are seedless. Here, we show that suppression of Pad-1 and its orthologous genes that were involved in auxin homeostasis induce parthenocarpy in eggplants, tomatoes, and peppers.

Abstract

Fruit development normally occurs after pollination and fertilization; however, in parthenocarpic plants, the ovary grows into the fruit without pollination and/or fertilization. Parthenocarpy has been recognized as a highly attractive agronomic trait because it could stabilize fruit yield under unfavorable environmental conditions. Although natural parthenocarpic varieties are useful for breeding Solanaceae plants, their use has been limited, and little is known about their molecular and biochemical mechanisms. Here, we report a parthenocarpic eggplant mutant, pad-1, which accumulates high levels of auxin in the ovaries. Map-based cloning showed that the wild-type (WT) Pad-1 gene encoded an aminotransferase with similarity to Arabidopsis VAS1 gene, which is involved in auxin homeostasis. Recombinant Pad-1 protein catalyzed the conversion of indole-3-pyruvic acid (IPyA) to tryptophan (Trp), which is a reverse reaction of auxin biosynthetic enzymes, tryptophan aminotransferases (TAA1/TARs). The RNA level of Pad-1 gene increased during ovary development and reached its highest level at anthesis stage in WT. This suggests that the role of Pad-1 in WT unpollinated ovary is to prevent overaccumulation of IAA resulting in precocious fruit-set. Furthermore, suppression of the orthologous genes of Pad-1 induced parthenocarpic fruit development in tomato and pepper plants. Our results demonstrated that the use of pad-1 genes would be powerful tools to improve fruit production of Solanaceae plants.

See https://www.pnas.org/content/117/23/12784

Figure 2: Map-based cloning of pad-1. (A) In the F₂ population, pad-1 locus is located between markers est_smfl28j21 and eme07D02 on chromosome 3. (B) In the F₃ population, pad-1 locus is mapped between markers ec3110A and ec3077F. (C) A BAC clone, 80K19 is mapped on the pad-1 locus. (D and E) Phenotype and genotype data of the NILs show that the pad-1 locus is mapped between markers 80K19SSR03 and PaSeq128. (F) Gene structure of Pad-1/pad-1.