The RhLOL1-RhILR3 module mediates cytokinin-induced petal abscission in rose

Authors: JIANG, CHUYAN - China Agriculture University; LIANG, YUE - China Agriculture University; DENG, SHUNING - China Agriculture University; LIU, YANG - China Agriculture University; ZHAU, HAOHAO - China Agriculture University; LI, SUSU - China Agriculture University; Jiang, Cai-Zhong; GAO, JUNPING - China Agriculture University; MA, CHAO - China Agriculture University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/8/2022
Publication Date: 10/20/2022
Citation: Jiang, C., Liang, Y., Deng, S., Liu, Y., Zhau, H., Li, S., Jiang, C., Gao, J., Ma, C. 2022. The RhLOL1-RhILR3 module mediates cytokinin-induced petal abscission in rose. New Phytologist. 237(2):483-496. https://doi.org/10.1111/nph.18556.
DOI: https://doi.org/10.1111/nph.18556

Interpretive Summary: Abscission (falling leaves and fruit/flower drops) is a physiological process directly linked to senescence (death). In the context of senescence, the final phase of flower life cessation can be divided into three types: petal wilting, withering, or abscission of turgid petal. Therefore, petal abscission is considered as a type of the terminal phase of flower senescence. Petal senescence and abscission are closely coordinated, and are precisely regulated by phytohormones. In most cases, hormones have the similar effects on petal abscission and senescence, which occur simultaneously. Ethylene is a critical accelerator that regulates petal senescence and abscission processes. Exogenous ethylene treatment accelerates petal senescence and abscission in a majority of the abscission-prone flowers. On the other hand, auxin is a pivotal inhibitor of petal abscission and senescence. The molecular mechanisms of auxin in both processes have been well investigated. Intriguingly, previous studies suggest that cytokinin (CTK) may play distinct regulatory roles between organ senescence and abscission. CTK has been widely proved to be a suppressor of flower senescence. In rose, varieties with long flower longevity contain higher CTK contents in petals compared with those with shorter lived flowers. Exogenous CTK treatment can delay petal senescence in several plant species, including carnation (Dianthus caryophyllus), petunia (Petunia hybrida), and rose. On the contrary, several studies indicated that CTK plays the part of accelerator in organ abscission. A synthetic CTK-like molecule, thidiazuron (TDZ) has been widely used as defoliant in agriculture to facilitate mechanical harvesting for many crops, especially cotton. In apple, application of synthetic CTK-like compounds can significantly promote fruitlet abscission. However, the role of CTK in petal abscission is still ambiguous. LESION SIMULATING DISEASE1 (LSD1)-like genes encode a small plant specific family of zinc finger proteins that contain zinc finger LSD domains. In Arabidopsis, function analyses of LSD1 mutations demonstrated LSD1-like genes participate in programmed cell death, and abiotic and biotic stresses. Zinc finger LSD domains have been suggested responsible for DNA/protein binding, indicating LSD1-like proteins might act as transcription factors or scaffold proteins. However, to date, the molecular basis of LSD1-like protein function is still largely unknown. Rose (Rosa hybrida) is an important ornamental crop worldwide, and the commercial value depends on the flower vase life. Here, we observed that in rose (Rosa hybrida), biologically active CTK is accumulated during petal abscission, and CTK is an accelerator of petal abscission. We identified a LESION SIMULATING DISEASE1 (LSD1) family member RhLOL1, of which the expression is induced by CTK treatment and during petal abscission. Silencing of RhLOL1 in rose delays petal abscission, while overexpression of its ortholog SlLOL1 in tomato promotes pedicel abscission, indicating the conserved function of LOL1 in activating plant floral organ abscission. In addition, we establish a bHLH transcription factor RhILR3 interacting with RhLOL1. Silencing of RhILR3 promotes rose petal abscission. RhILR3 binds to the promoters of auxin signaling repressor Aux/IAA genes, and represses their expression. But RhLOL1 interacting with RhILR3 activates the expression of Aux/IAA genes. Our results reveal a RhLOL1-RhILR3 regulatory module involved in CTK-induced petal abscission via regulating the expression of Aux/IAA genes. Our data demonstrate that CTK plays an important role on accelerating petal abscission, and provide a foundation for crop quality improvement.

Technical Abstract: In many plant species, petal abscission is closely tied to petal senescence, and can be considered as the final step of petal senescence. Cytokinin (CTK) is a powerful suppressor of petal senescence. However, the role of CTK in petal abscission is ambiguous. Here, we observed that in rose (Rosa hybrida), biologically active CTK is accumulated during petal abscission, and CTK is an accelerator of petal abscission. We identify a LESION SIMULATING DISEASE1 (LSD1) family member RhLOL1, of which the expression is induced by CTK treatment and during petal abscission. Silencing of RhLOL1 in rose delays petal abscission, while overexpression of its ortholog SlLOL1 in tomato promotes pedicel abscission, indicating the conserved function of LOL1 in activating plant floral organ abscission. In addition, we establish a bHLH transcription factor RhILR3 interacting with RhLOL1. Silencing of RhILR3 promotes rose petal abscission. RhILR3 binds to the promoters of auxin signaling repressor Aux/IAA genes, and represses their expression. But RhLOL1 interacting with RhILR3 activates the expression of Aux/IAA genes. Our results reveal a RhLOL1-RhILR3 regulatory module involved in CTK-induced petal abscission via regulating the expression of Aux/IAA genes.