ABSTRACT
Roses are among the most popular ornamental plants cultivated worldwide for their great economic, symbolic, and cultural importance. Nevertheless, rapid petal senescence markedly reduces rose (Rosa hybrida) flower quality and value. Petal senescence is a developmental process tightly regulated by various phytohormones. Ethylene accelerates petal senescence, while gibberellic acid (GA) delays this process. However, the molecular mechanisms underlying the crosstalk between these phytohormones in the regulation of petal senescence remain largely unclear. Here, we identified SENESCENCE-ASSOCIATED F-BOX (RhSAF), an ethylene-induced F-box protein gene encoding a recognition subunit of the SCF-type E3 ligase. We demonstrated that RhSAF promotes degradation of the GA receptor GIBBERELLIN INSENSITIVE DWARF1 (RhGID1) to accelerate petal senescence. Silencing RhSAF expression delays petal senescence, while suppressing RhGID1 expression accelerates petal senescence. RhSAF physically interacts with RhGID1s and targets them for ubiquitin/26S proteasome-mediated degradation. Accordingly, ethylene-induced RhGID1C degradation and RhDELLA3 accumulation are compromised in RhSAF-RNAi lines. Our results demonstrate that ethylene antagonizes GA activity through RhGID1 degradation mediated by the E3 ligase RhSAF. These findings enhance our understanding of the phytohormone crosstalk regulating petal senescence and provide insights for improving flower longevity.
Subject(s)
Ethylenes , F-Box Proteins , Flowers , Gene Expression Regulation, Plant , Gibberellins , Plant Proteins , Rosa , Ethylenes/metabolism , Ethylenes/pharmacology , Gibberellins/metabolism , Gibberellins/pharmacology , F-Box Proteins/metabolism , F-Box Proteins/genetics , Plant Proteins/metabolism , Plant Proteins/genetics , Rosa/genetics , Rosa/drug effects , Rosa/metabolism , Flowers/genetics , Flowers/drug effects , Flowers/growth & development , Gene Expression Regulation, Plant/drug effects , Plant Growth Regulators/metabolism , Plant Growth Regulators/pharmacology , Plant Senescence/genetics , Proteasome Endopeptidase Complex/metabolism , Receptors, Cell Surface/metabolism , Receptors, Cell Surface/geneticsABSTRACT
Flower size, a primary agronomic trait in breeding of ornamental plants, is largely determined by petal expansion. Generally, ethylene acts as an inhibitor of petal expansion, but its effect is restricted by unknown developmental cues. In this study, we found that the critical node of ethylene-inhibited petal expansion is between stages 1 and 2 of rose flower opening. To uncover the underlying regulatory mechanism, we carried out a comparative RNA-seq analysis. Differentially expressed genes (DEGs) involved in auxin-signaling pathways were enriched. Therefore, we identified an auxin/indole-3-acetic acid (Aux/IAA) family gene, RhIAA14, whose expression was development-specifically repressed by ethylene. The silencing of RhIAA14 reduced cell expansion, resulting in diminished petal expansion and flower size. In addition, the expressions of cell-expansion-related genes, including RhXTH6, RhCesA2, RhPIP2;1, and RhEXPA8, were significantly downregulated following RhIAA14 silencing. Our results reveal an Aux/IAA that serves as a key player in orchestrating petal expansion and ultimately contributes to flower size, which provides new insights into ethylene-modulated flower opening and the function of the Aux/IAA transcription regulator.
Subject(s)
Rosa , Ethylenes/metabolism , Family , Gene Expression Regulation, Plant , Indoleacetic Acids/metabolism , Plant Breeding , Plant Proteins/genetics , Plant Proteins/metabolism , Rosa/geneticsABSTRACT
In many plant species, including rose (Rosa hybrida), flower senescence is promoted by the gaseous hormone ethylene and inhibited by the cytokinin (CTK) class of hormones. However, the molecular mechanisms underlying these antagonistic effects are not well understood. In this study, we characterized the association between a pathogenesis-related PR-10 family gene from rose (RhPR10.1) and the hormonal regulation of flower senescence. Quantitative reverse transcription PCR analysis showed that RhPR10.1 was expressed at high levels during senescence in different floral organs, including petal, sepal, receptacle, stamen, and pistil, and that expression was induced by ethylene treatment. Silencing of RhPR10.1 expression in rose plants by virus-induced gene silencing accelerated flower senescence, which was accompanied by a higher ion leakage rate in the petals, as well as increased expression of the senescence marker gene RhSAG12 CTK content and the expression of three CTK signaling pathway genes were reduced in RhPR10.1-silenced plants, and the accelerated rate of petal senescence that was apparent in the RhPR10.1-silenced plants was restored to normal levels by CTK treatment. Finally, RhHB6, a homeodomain-Leu zipper I transcription factor, was observed to bind to the RhPR10.1 promoter, and silencing of its expression also promoted flower senescence. Our results reveal an ethylene-induced RhHB6-RhPR10.1 regulatory module that functions as a brake of ethylene-promoted senescence through increasing the CTK content.