A petunia transcription factor, PhOBF1, regulates flower senescence by modulating gibberellin biosynthesis

Authors: JI, XIAOTONG - Northwest Agricultural & Forestry University; XIN, ZIWEI - Northwest Agricultural & Forestry University; YUAN, YANPING - Northwest Agricultural & Forestry University; WANG, MEILING - Northwest Agricultural & Forestry University; LU, XINYI - Northwest Agricultural & Forestry University; LI, JIAQI - Northwest Agricultural & Forestry University; ZHANG, YANLONG - Northwest Agricultural & Forestry University; NIU, LIXIN - Northwest Agricultural & Forestry University; Jiang, Cai-Zhong; SUN, DAOYANG - Northwest Agricultural & Forestry University

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/6/2023
Publication Date: 2/16/2023
Citation: Ji, X., Xin, Z., Yuan, Y., Wang, M., Lu, X., Li, J., Zhang, Y., Niu, L., Jiang, C., Sun, D. 2023. A petunia transcription factor, PhOBF1, regulates flower senescence by modulating gibberellin biosynthesis. Horticulture Research. 10(4). Article uhad022. https://doi.org/10.1093/hr/uhad022.
DOI: https://doi.org/10.1093/hr/uhad022

Interpretive Summary: Senescence is a genetically programmed event that occurs in the terminal phase of individual tissue or organ development in plants. It is typically characterized by wilting, discoloration, and even abscission due to the sequential breakdown of physiological and biochemical activities. Although senescence makes a great contribution to plant survival by allowing nutrient recycling and reallocation, it may cause substantially reduced crop yield and biomass production from an agronomic perspective. The retardation of senescence process is essential for many plant species, especially ornamental plants. The initiation of flower senescence is concomitant with the massive alterations in the cellular components. Plant hormones are considered to impose important influences on the senescence of floral organs. It has been revealed that ethylene serves as a major regulator of flower senescence in ethylene-sensitive plants. Abscisic acid (ABA) is also known as a promoter of flower senescence. Particularly, ABA was thought to be a primary contributor to flower senescence in ethylene-insensitive gladiolus. Another hormone jasmonic acid (JA) was shown to have similar function in accelerating senescence progression of Dendrobium orchid flowers. Contrarily to the senescence-promoting effects of the hormones as mentioned above, cytokinins and gibberellins (GAs) are proposed as important anti-senescence factors in the flowers. It is well recognized that the regulation of flower senescence depends greatly on a complex hormonal crosstalk rather than individual hormone. However, how these hormonal interactions are transcriptionally regulated is largely unclear. The basic leucine zipper (bZIP) transcription factors comprise an extensive and conserved family in plants. Among them, AtbZIP11 from Arabidopsis has been demonstrated to regulate amino acid and sugar metabolism by specifically activating asparagine synthetase and proline dehydrogenase. AtbZIP11 has been identified as a quantitative modulator of auxin-stimulated responses through the regulation of histone acetylation. To date, the roles of bZIP11 and its homologous proteins in flower senescence are still not well understood. Petunia is an important ornamental plant with large showy flowers, short growth period, and high genetic diversity, and has been adopted as a model plant to elucidate the regulatory mechanisms underlying flower senescence. In this study, we characterized one up-regulated gene PhOBF1, belonging to the basic leucine zipper transcription factor family, in senescing petals of petunia (Petunia hybrida). Exogenous treatments with ethylene and GA3 provoked a dramatic increase in PhOBF1 transcripts. Compared with wild-type plants, PhOBF1-RNAi transgenic petunia plants exhibited shortened flower longevity, while overexpression of PhOBF1 resulted in delayed flower senescence. Silencing and overexpression of PhOBF1 affected expression levels of a few genes involved in the GA biosynthesis and signaling pathways, as well as accumulation levels of bioactive GAs GA1 and GA3. Application of GA3 restored the accelerated petal senescence to normal levels in PhOBF1-RNAi transgenic petunia lines, and reduced ethylene release and transcription of ethylene biosynthetic genes. Moreover, PhOBF1 was observed to specifically bind to the promoter of a GA biosynthesis gene. Transient silencing of this GA gene in petunia plants led to accelerated corolla senescence. Our results suggest that PhOBF1 functions as a negative regulator of ethylene-mediated flower senescence by modulating the GA production.

Technical Abstract: Flower senescence is commonly enhanced by the endogenous hormone ethylene and suppressed by the gibberellins (GAs) in plants. However, the detailed mechanism for the antagonism of these hormones during flower senescence remains elusive. In this study, we characterized one up-regulated gene PhOBF1, belonging to the basic leucine zipper transcription factor family, in senescing petals of petunia (Petunia hybrida). Exogenous treatments with ethylene and GA3 provoked a dramatic increase in PhOBF1 transcripts. Compared with wild-type plants, PhOBF1-RNAi transgenic petunia plants exhibited shortened flower longevity, while overexpression of PhOBF1 resulted in delayed flower senescence. Transcript abundances of two senescence-related genes PhSAG12 and PhSAG29 were higher in PhOBF1-silenced plants but lower in PhOBF1-overexpressing plants. Silencing and overexpression of PhOBF1 affected expression levels of a few genes involved in the GA biosynthesis and signaling pathways, as well as accumulation levels of bioactive GAs GA1 and GA3. Application of GA3 restored the accelerated petal senescence to normal levels in PhOBF1-RNAi transgenic petunia lines, and reduced ethylene release and transcription of three ethylene biosynthetic genes PhACO1, PhACS1, and PhACS2. Moreover, PhOBF1 was observed to specifically bind to the PhGA20ox3 promoter containing a G-box motif. Transient silencing of PhGA20ox3 in petunia plants through tobacco rattle virus-based virus-induced gene silencing method led to accelerated corolla senescence. Our results suggest that PhOBF1 functions as a negative regulator of ethylene-mediated flower senescence by modulating the GA production.