Developmental transitions in plants require adequate carbon resources, and organ abscission often occurs due to competition for carbohydrates/assimilates. Physiological studies have indicated that organ abscission may be activated by sucrose deprivation; however, an underlying regulatory mechanism that links sucrose transport to organ shedding has yet to be identified. Here, we report that transport of sucrose and the phytohormone auxin to petals through the phloem of the abscission zone (AZ) decreases during petal abscission in rose (Rosa hybrida), and that auxin regulates sucrose transport into the petals. Expression of the sucrose transporter RhSUC2 decreased in the AZ during rose petal abscission. Similarly, silencing of RhSUC2 reduced the sucrose content in the petals and promotes petal abscission. We established that the auxin signaling protein RhARF7 binds to the promoter of RhSUC2, and that silencing of RhARF7 reduces petal sucrose contents and promotes petal abscission. Overexpression of RhSUC2 in the petal AZ restored accelerated petal abscission caused by RhARF7 silencing. Moreover, treatment of rose petals with auxin and sucrose delayed ethylene-induced abscission, while silencing of RhARF7 and RhSUC2 accelerated ethylene-induced petal abscission. Our results demonstrate that auxin modulates sucrose transport during petal abscission, and that this process is regulated by a RhARF7-RhSUC2 module in the AZ.

cn). † These authors contributed equally to this work. SUMMARYThe timing of plant organ abscission is modulated by the balance of two hormones, ethylene and auxin, while the mechanism of organ shedding depends on the loss of middle lamella pectin in the abscission zone (AZ). However, the mechanisms involved in sensing the balance of auxin and ethylene and that affect pectin degradation during abscission are not well understood. In this study, we identified two members of the APETALA2/ethylene-responsive factor (AP2/ERF) transcription factor family in rose (Rosa hybrida), RhERF1 and RhERF4 which play a role in petal abscission. The expression of RhERF1 and RhERF4 was influenced by ethylene and auxin, respectively. Reduced expression of RhERF1 or RhERF4 was observed to accelerate petal abscission. Global expression analysis and real-time PCR assays revealed that RhERF1 and RhERF4 modulate the expression of genes encoding pectin-metabolizing enzymes. A reduction in the abundance of pectin epitopes was detected in the AZs of RhERF1 and RhERF4-silenced plants by immunofluorescence microscopy analysis. In addition, RhERF1 and RhERF4 were shown to bind to the promoter of the pectin-metabolizing gene b-GALACTOSIDASE 1 (RhBGLA1), and reduced expression of RhBGLA1 delayed petal abscission. We conclude that during petal abscission, RhERF1 and RhERF4 integrate and coordinate ethylene and auxin signals to modulate pectin metabolism, in part by regulating the expression of RhBGLA1.

The phytohormone auxin plays a pivotal role in floral meristem initiation and gynoecium development, but whether and how auxin controls floral organ identity remain largely unknown. Here, we found that auxin levels influence organ specification, and changes in auxin levels influence homeotic transformation between petals and stamens in rose (Rosa hybrida). The PIN-FORMED-LIKES (PILS) gene RhPILS1 governs auxin levels in floral buds during floral organogenesis. RhAUXIN RESPONSE FACTOR 18 (RhARF18), whose expression decreases with increasing auxin content, encodes a transcriptional repressor of the C-class gene RhAGAMOUS (RhAG) and controls stamen–petal organ specification in an auxin-dependent manner. Moreover, RhARF18 physically interacts with the histone deacetylase (HDA) RhHDA6. Silencing of RhHDA6 increases H3K9/K14 acetylation levels at the site adjacent to the RhARF18-binding site in the RhAG promoter and reduces petal number, indicating that RhARF18 might recruit RhHDA6 to the RhAG promoter to reinforce the repression of RhAG transcription. We propose a model for how auxin homeostasis controls floral organ identity via regulating transcription of RhAG.

Petal senescence involves numerous programmed changes in biological and biochemical processes. Ubiquitination plays a critical role in protein degradation, a hallmark of organ senescence. Therefore, we investigated changes in the proteome and ubiquitome of senescing rose (Rosa hybrida) petals to better understand their involvement in petal senescence. Of 3859 proteins quantified in senescing petals, 1198 were upregulated, and 726 were downregulated during senescence. We identified 2208 ubiquitinated sites, including 384 with increased ubiquitination in 298 proteins and 1035 with decreased ubiquitination in 674 proteins. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses revealed that proteins related to peptidases in proteolysis and autophagy pathways were enriched in the proteome, suggesting that protein degradation and autophagy play important roles in petal senescence. In addition, many transporter proteins accumulated in senescing petals, and several transport processes were enriched in the ubiquitome, indicating that transport of substances is associated with petal senescence and regulated by ubiquitination. Moreover, several components of the brassinosteroid (BR) biosynthesis and signaling pathways were significantly altered at the protein and ubiquitination levels, implying that BR plays an important role in petal senescence. Our data provide a comprehensive view of rose petal senescence at the posttranslational level.

In many plant species, petal abscission can be considered the final step of petal senescence. Cytokinins (CKs) are powerful suppressors of petal senescence; however, their role in petal abscission is ambiguous.Here, we observed that, in rose (Rosa hybrida), biologically active CK is accumulated during petal abscission and acts as an accelerator of the abscission process. Using a combination of reverse genetics, and molecular and biochemical techniques, we explored the roles of a LESION SIMULATING DISEASE1 (LSD1) family member RhLOL1 interacting with a bHLH transcription factor RhILR3 in CK-induced petal abscission.Silencing RhLOL1 delays rose petal abscission, while the overexpression of its ortholog SlLOL1 in tomato (Solanum lycopersicum) promotes pedicel abscission, indicating the conserved function of LOL1 in activating plant floral organ abscission. In addition, we identify a bHLH transcription factor, RhILR3, that interacts with RhLOL1. We show that RhILR3 binds to the promoters of the auxin signaling repressor auxin/indole-3-acetic acid (Aux/IAA) genes to inhibit their expression; however, the interaction of RhLOL1 with RhILR3 activates the expression of the Aux/IAA genes including RhIAA4-1. Silencing RhIAA4-1 delays rose petal abscission.Our results thus reveal a RhLOL1-RhILR3 regulatory module involved in CK-induced petal abscission via the regulation of the expression of the Aux/IAA genes.