Xiong Liao, Mengsi Li, Bin Liu, Miaoling Yan, Xiaomin Yu, Hailing Zi, Renyi Liu, and Chizuko Yamamuro

PNAS December 4, 2018 115 (49) E11542-E11550

Significance

Using strawberry fruit as a model system, we uncover the mechanistic interactions between auxin, gibberellic acid (GA), and abscisic acid (ABA) that regulate the entire process of fruit development. Interlinked regulatory loops control ABA levels during fruit development. During the early stages, auxin/GA turns on a feedback loop to activate the removal of ABA via FveCYP707A4a-dependent catabolism needed for fruit growth. Down-regulation of auxin/GA results in the suppression of the feedback loop and the activation of the ABA biosynthesis-dependent feedforward loop, leading to a steep ABA accumulation for fruit ripening. The interlinked regulatory loops provide a conceptual framework that underlies the connection between the regulation of fruit growth and that of ripening as well as a molecular basis for manipulation of fruit sizes and ripening times.

Abstract

Fruit growth and ripening are controlled by multiple phytohormones. How these hormones coordinate and interact with each other to control these processes at the molecular level is unclear. We found in the early stages of Fragaria vesca (woodland strawberry) fruit development, auxin increases both widths and lengths of fruits, while gibberellin [gibberellic acid (GA)] mainly promotes their longitudinal elongation. Auxin promoted GA biosynthesis and signaling by activating GA biosynthetic and signaling genes, suggesting auxin function is partially dependent on GA function. To prevent the repressive effect of abscisic acid (ABA) on fruit growth, auxin and GA suppressed ABA accumulation during early fruit development by activating the expression of FveCYP707A4a encoding cytochrome P450 monooxygenase that catalyzes ABA catabolism. At the onset of fruit ripening, both auxin and GA levels decreased, leading to a steep increase in the endogenous level of ABA that drives fruit ripening. ABA repressed the expression of FveCYP707A4a but promoted that of FveNCED, a rate-limiting step in ABA biosynthesis. Accordingly, altering FveCYP707A4aexpression changed the endogenous ABA levels and affected FveNCED expression. Hence, ABA catabolism and biosynthesis are tightly linked by feedback and feedforward loops to limit ABA contents for fruit growth and to quickly increase ABA contents for the onset of fruit ripening. These results indicate that FveCYP707A4a not only regulates ABA accumulation but also provides a hub to coordinate fruit size and ripening times by relaying auxin, GA, and ABA signals.

See: http://www.pnas.org/content/115/49/E11542

Figure 1: A refined description of Fragaria vesca fruit developmental stages and their relationship with changes in the content of auxin, gibberellin, and ABA. (A) A detailed description of different fruit developmental stages. Fruit development includes early growth and late ripening phases. The early phase, which is further divided into seven stages, S1–S7, is characterized by gradual increase in fruit (receptacle and achene) size, weight, and firmness. S1–S5 were described previously (7). The ripening phase, divided into RS1–RS5. For each stage, the corresponding days after pollination (DAP) are indicated. (Scale bar: 1 cm.) (B) Embryos inside cleared seeds of different developmental stages imaged with DIC optics. (Scale bar: 100 μM.) (C) Quantification of fruit dimension (length and width) and weight in different stages. Error bars represent SD of 20 fruits. (D) Changes in fruit firmness and the expression of PG gene in fruit (receptacle and achene) in different developmental stages. FveACTIN was used as the internal control. Error bars represent SD of three independent replicates (20 fruits were used for each replicate). (E and F) Changes in IAA, GAs (E), and ABA (F) contents of fruit (receptacle and achene) in different developmental stages. Error bars represent SD of three independent replicates (10 fruits were used for each replicate).