Ethylene-regulated asymmetric growth of the petal base promotes flower opening in rose (Rosa hybrida)

Authors: CHENG, CHENXIA - China Agricultural University; YU, QIN - China Agricultural University; WANG, YARU - China Agricultural University; WANG, HONG - China Agricultural University; DONG, YUHAN - China Agricultural University; JI, YUQI - China Agricultural University; ZHOU, XIAOFENG - China Agricultural University; LI, YONGHONG - The Hong Kong Polytechnic University Shenzhen Institute; Jiang, Cai-Zhong; GAN, SU-SHENG - Cornell University; ZHAO, LIANGJUN - China Agricultural University; FEI, ZHANGJUN - US Department Of Agriculture (USDA); GAO, JUNPING - China Agricultural University; MA, CHAO - China Agricultural University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/26/2021
Publication Date: 2/2/2021
Citation: Cheng, C., Yu, Q., Wang, Y., Wang, H., Dong, Y., Ji, Y., Zhou, X., Li, Y., Jiang, C., Gan, S., Zhao, L., Fei, Z., Gao, J., Ma, C. 2021. Ethylene-regulated asymmetric growth of the petal base promotes flower opening in rose (Rosa hybrida). The Plant Cell. 33(4):1229-1251. https://doi.org/10.1093/plcell/koab031.
DOI: https://doi.org/10.1093/plcell/koab031

Interpretive Summary: Flowers are the unique structures in angiosperms which facilitate reproduction by provide a mechanism for the union of sperm with eggs. The time of flower opening, with anthers and pistils showing, indicate the onset of a period for pollinators attracting and consequent pollination. There are plenty of reports concerning the mechanism of flower initiation and organ differentiation, the study of flower opening is much less though. Basically, flower opening promotes pollination and is driven by the coordinated development and movements of floral organs, particularly. This process can involve substantial growth and development. Despite their sessile nature, plants are capable of moving to achieve specific development purposes and/or in response to environmental stimuli. More than a century ago, Darwin noted that the stems of all tested seedlings showed continuous circumnutation. He also described several typical movements in details, including the sleep movement of leaves in legumes, and phototropism and gravitropism of seedlings. Due to the lack of muscle cells, plant movement is usually driven either by irreversible differential growth, or by reversible changes in turgor on different sides of organs. Tropic movement, like phototropism and gravitropism, are achieved through irreversible differential growth that reorient organs to directional stimuli, such as light or gravity. In contrast, plant movements that are induced by non-directional factors, such as temperature, humidity or touch, are called nastic responses and are achieved through turgor-driven reversible movements. The phenomenon in ‘sleep movement of leaves’ legumes involves unfolding leaves or leaflets in the day and folding them at night, and is a typical nastic response called nyctinasty. Plant movement is controlled by multiple internal and external factors, one example being in shoot phototropism, where unequal redistribution of auxin across organs drives the movement. In legumes, the nyctinastic movement of leaves or leaflets relies on a specialized structure: the so-called motor organ, or pulvinus, located at the base of the petiole of single leaves, or the petiolule of compound leaf leaflets. Recent studies showed that formation of the pulvinus is controlled by ELONGATED PETIOLUTE 1 (ELP1), a LATERAL ORGAN BOUNDARIES (LBD) transcription factor (TF) gene. However, compared to shoot tropism and leaf nastic movement, the mechanism of petal movement and flower opening is not well understood, although the flower opening process has been extensively described for various species. To date, the regulatory mechanism of flower opening has not been well characterized, and we chose rose (R. hybrida) as a model to investigate the regulatory network of flower opening and petal movement. Unexpectedly, we found that asymmetric growth of the petal base, rather than expansion of the petal lamina, drives petal movement. We showed that the phytohormone ethylene can accelerate petal movement by enhancing asymmetric growth of the petal base. A HD-Zip I subfamily transcript factor (TF), RhPMP1 (PETAL MOVEMENT-RELATED PROTEIN 1) acts as a direct target of the ETHYLENE INSENSITIVE 3 (EIN3) protein, the primary TF in ethylene signaling. RhPMP1 induces expression of ANAPHASE-PROMOTING COMPLEX 3b (RhAPC3b), thereby increasing the endoreduplication level of parenchyma cells on the adaxial side, resulting in asymmetric growth of the petal base. We conclude that in rose, petal movement is driven by asymmetric growth of the petal base and is controlled by an RhPMP1-RhAPC3b module in an ethylene-dependent manner. These findings provide insights into the pathway regulating petal movement and shed light on the underlying mechanism of regulated flower opening.

Technical Abstract: Flowers are the core reproductive structures and key distinguishing features of angiosperms. Flower opening to expose stamens and gynoecia is important in cases where pollinators much be attracted to promote cross-pollination, which can enhance reproductive success and species preservation. The floral opening process is accompanied by coordinated movement of various floral organs, particularly the petals. However, the mechanisms underlying petal movement and flower opening are still not well understood. Here, we integrated anatomical, physiological and molecular approaches to determine the petal movement regulatory network, using rose (Rosa hybrida) as a model. We found that PETAL MOVEMENT-RELATED PROTEIN 1 (RhPMP1), a homeodomain transcription factor gene is a direct target of ETHYLENE INSENSITIVE 3 (EIN3), a transcription factor downstream to ethylene signaling. RhPMP1 expression was upregulated by ethylene and specifically activated cell endoreduplication on the adaxial side parenchyma at the petal base through induction of RhAPC3b expression, a gene encoding the core subunit of the APC complex. Eventually, cell expansion of adaxial side parenchyma was enhanced and thus resulted in asymmetric growth of the petal base, leading to a typical epinastic movement of petals and flower opening. These findings provide insights into the pathway regulating petal movement and associated flower opening mechanisms.