Four Class A AUXIN RESPONSE FACTORs Promote Tomato Fruit Growth

For flowering plants, fruit development is a crucial step in the reproductive process. For humans, fruit is an important food source. The process of transition from ovary to fruit is often called fruit initiation or fruit set and is the most important step in fruit development. Plants strictly control the ovary to develop and produce fruit only when fertilization is successful, which allows plants to avoid the waste of resources caused by the production of seedless fruits under unfavorable conditions where anther development is impaired. However, for agricultural production, parthenocarpy can ensure stable yield and quality under different environmental conditions, and is favored by consumers.

Plant hormones play a key role in fruit development. Auxin is one of the main hormones that induce fruit development. After pollination, auxin levels rise in developing seeds, inducing the transition from ovary to fruit development. Auxin also promotes cell division and expansion during fruit growth. In addition, auxin acting on unfertilized ovaries or genetic mutations that lead to elevated auxin signaling can induce seedless fruit formation.

The auxin signaling pathway is well conserved in plants. Key components of early auxin signaling include three protein families: the auxin coreceptors TIR1/AFB, the AUX/IAA transcription repressors, and the AUXIN RESPONSE FACTOR (ARF) transcription factors. When auxin levels are low, IAA binds to the target promoters of ARF and recruits the co-repressor TOPLESS (TPL) to repress the transcription of downstream genes. When the auxin level increases, auxin binds to TIR1/AFB and IAA, leading to the degradation of IAA protein and activation of signaling pathways. This signaling pathway is based on class A ARFs. However, in subsequent studies, class A ARFs were pointed out for their inhibitory role in fruit initiation and growth. Which class A ARFs are the activators that mediate auxin-induced fruit initiation or fruit development remain unknown.

Recently, researchers from Duke University published a research paper entitled "Four class A AUXIN RESPONSE FACTORs promote tomato fruit growth despite suppressing fruit set" in Nature Plants. The researchers characterized four class A ARFs transcription factors highly expressed in the tomato ovary and constructed higher-order tomato mutants. They found that these transcription factors acted as repressors during fruit initiation and changed to act as activators during fruit growth, demonstrating the fine-tuning ability of these four class A ARFs on fruit growth.

The authors first constructed single and double mutants of ARF8A and ARF8B, and found that ARF8A and ARF8B have the functions of inhibiting fruit germination and promoting placenta growth. The functions of the two overlap and can be superimposed. Interestingly, although the parthenocarpic fruit of the mutant was larger than that of the wild type, the overall fruit size of the mutant was smaller than that of the wild type after pollination, while the double mutant could only produce smaller parthenocarpic fruit. ARF5 and ARF7 also have similar inhibitory effects, but weaker than ARF8.

Subsequent further studies on triple and quadruple mutants and transgenic lines found that the four class A ARFs had dual functions, inhibiting the initiation of fruit development and activating fruit growth. The expression profile analysis of the ovary development process and the target genes of ARF8 revealed that ARF and IAA9 repressors have specific roles in regulating the development of different fruit tissues. Moreover, ARF directly binds to the target gene promoter to regulate the expression of downstream genes, and the expression of MADS-BOX also requires IAA9/ARF.

Taken together, this study identifies four class A ARFs that finely regulate tomato fruit development by inhibiting fruit initiation and activating fruit growth in a tissue-specific manner. Before pollination, the IAA9/ARF complex activates the expression of MADS-BOX to inhibit fruit setting. During flowering, ovary auxin levels rise, IAA9 degrades, and ARF activates downstream genes to promote fruit growth. This work demonstrates that the growth of different tissues in tomato is controlled by different combinations of ARFs, which may have implications for fine-tuning crop growth. In addition, the molecular mechanism of ARFs-related parthenocarpic fruit development can be of great value for improving crop yield and stabilizing food security.

Reference:

Hu, J., Li, X. & Sun, Tp. Four class A AUXIN RESPONSE FACTORs promote tomato fruit growth despite suppressing fruit set. Nat. Plants (2023). https://doi.org/10.1038/s41477-023-01396-y