Decoding peach fruit ripening: The pivotal role of PpARF6 in auxin-ethylene cross-talk

Peach, an economically important crop, exhibits varied fruit textures influenced by different genes, affecting ethylene production and flesh firmness. Fruit texture in peach cultivars is highly variable and directly affects consumer behaviour and postharvest storage life. Ethylene biosynthesis, which is crucial for fruit ripening, is regulated by various transcription factors (TFs), with studies in other fruits revealing complex auxin-ethylene crosstalk. However, in peach, the role of ARF TFs in fruit ripening is unclear, and the intricate mechanisms by which auxin signaling intersects with ethylene to regulate fruit ripening at transcriptional and post-transcriptional levels remain largely unexplored.

In July 2023, Horticulture Research published a research entitled by “PpARF6 acts as an integrator of auxin and ethylene signaling to promote fruit ripening in peach”.

Analysis of transcriptome sequencing data from different peach cultivars revealed that PpARF6 and PpARF19 were significantly upregulated during ripening, with significantly higher expression of PpARF6. Treatment of immature 'Summer Golden' peach fruits with NAA (an auxin) accelerated ripening, indicated by increased red pigmentation, ethylene content, and decreased fruit firmness. The treatment also up-regulated the transcription of ethylene biosynthesis genes and PpARF6. The functional role of PpARF6 was validated using a transient expression assay in 'Dongxuemitao' peaches, revealing that PpARF6 infiltration significantly enhanced ethylene biosynthesis gene expression, ethylene content, and reduced fruit firmness. Additionally, yeast one-hybrid and dual-luciferase assays confirmed that PpARF6 binds and activates the promoters of ethylene biosynthesis genes PpACS1 and PpACO1..The study also discovered that PpARF6 can interact with ethylene-insensitive3-like proteins PpEIL2/3 and compete with EIN3-binding F-box proteins PpEBF1/2 for their binding, thus keeping PpEIL2/3 active. This interaction enhances PpEIL2/3-mediated transcription of ethylene biosynthetic genes, integrating auxin and ethylene signaling in peach fruit ripening. To extend these findings, PpARF6 was overexpressed in tomato, a model fruit system. This overexpression led to earlier ripening, higher ACC content, accelerated chlorophyll degradation, and increased carotenoid content, indicating PpARF6's broad regulatory role in fruit ripening processes.

In summary, this comprehensive study using transcriptome analysis, biochemical assays and genetic manipulation in model systems demonstrates the critical role of PpARF6 in integrating auxin and ethylene signaling pathways to regulate peach fruit ripening, providing valuable insights into the complex hormonal regulation during fruit development.

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References

Authors

Xiaomei Chen^1,2, Yudi Liu^1,2, Xian Zhang^1,2, Beibei Zheng^1,3, Yuepeng Han^1,3,* and Ruo-Xi Zhang^1,3,*

Affiliations

¹CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical Garden, The Innovative Academy of Seed Design of Chinese

Academy of Sciences, Wuhan 430074, China

²University of Chinese Academy of Sciences, 19A Yuquanlu, Beijing 100049, China

³Hubei Hongshan Laboratory, Wuhan 430070, China

About Yuepeng Han

Professor, Centre for Resource Plants and Speciality Agricultural Plants, Wuhan Botanical Garden, Chinese Academy of Sciences, China. His research focuses on fruit tree genomics, especially the genetic basis and molecular mechanisms of fruit quality.