AUXIN RESPONSE FACTOR 18–HISTONE DEACETYLASE 6 module regulates floral organ identity in rose (Rosa hybrida)

Authors: CHEN, JIWEI - China Agricultural University; LI, YANG - China Agricultural University; LI, YONGHONG - The Hong Kong Polytechnic University Shenzhen Institute; JI, YUQI - China Agricultural University; WANG, YI - China Agricultural University; JIANG, CHUYAN - China Agricultural University; CHOISY, PATRICK - Lvmh Research Center; XU, TAO - Lvmh Research Center; CAI, YOUMING - Shanghai Academy Of Agricultural Sciences; PEI, DONG - Chinese Academy Of Forestry; Jiang, Cai-Zhong; GAN, SU-SHENG - Cornell University; GAO, JUNPING - China Agricultural University; MA, NAN - Chinese Agricultural University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/1/2021
Publication Date: 3/17/2021
Citation: Chen, J., Li, Y., Li, Y., Ji, Y., Wang, Y., Jiang, C., Choisy, P., Xu, T., Cai, Y., Pei, D., Jiang, C., Gan, S., Gao, J., Ma, N. 2021. AUXIN RESPONSE FACTOR 18–HISTONE DEACETYLASE 6 module regulates floral organ identity in rose (Rosa hybrida). Plant Physiology. 186(2):1074-1087. https://doi.org/10.1093/plphys/kiab130.
DOI: https://doi.org/10.1093/plphys/kiab130

Interpretive Summary: Rather than being single organs (like leaves or roots), flowers are composite structures, composed of multiple organs arranged in an ordered pattern. A typical angiosperm flower consists of four types of organ: sepal, petal, stamen, and pistil. The number (merosity) and the arrangement (phyllotaxy) of floral organs vary in different species. Floral organs may differ in their position within a flower and in specific characteristics, or their identity, both of which are important criteria for homology. Although different floral organs have different structures and functions, they all initiate from the floral meristem. Flower patterning and determinacy is tightly controlled by a set of homeotic genes, whose functions are classified in the ABCE model. All ABCE genes encode members of the MADS-box family, except APETALA2 (AP2), which encodes a member of the AP2/EREBP family. Floral organ initiation and determination are also controlled by hormones, especially auxin. Auxin plays an indispensable role in floral organ initiation. Local biosynthesis, metabolism and 80 transport of auxin are regulated coordinately to generate auxin maxima. Establishment of a local auxin maximum is required for initiation of a flower primordium in Arabidopsis thaliana. So far, however, whether and how auxin distribution and signaling are involved in controlling floral organ identity remains unknown. Here, we found that changes in auxin levels induce homeotic transformation between petals and stamens in rose (Rosa hybrida). RhPILS1, a rose PILS1-type protein, governs auxin levels in floral buds during floral organogenesis. RhARF18 is an auxin-regulated gene encoding a transcriptional repressor of RhAG and thus plays a role in stamen–petal specification in an auxin-dependent manner. Moreover, we found that RhARF18 physically interacts with a histone deacetylase, RhHDA6. Therefore, we propose a model for how auxin homeostasis controls floral organ identity via regulating transcription of RhAG.

Technical Abstract: The phytohormone auxin plays a pivotal role in floral meristem initiation and gynoecium development, but whether and how auxin controls floral organ identity remains 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 (ARF18), whose expression decreases with increasing auxin content, encodes a transcriptional repressor of the C-class gene RhAGAMOUS (RhAG) and governs 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.