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The Circadian-Controlled PIF8-BBX28 Module Regulates Petal Senescence in Rose Flowers by Governing Mitochondrial ROS Homeostasis

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The Circadian-Controlled PIF8-BBX28 Module Regulates Petal Senescence in Rose Flowers by Governing Mitochondrial ROS Homeostasis doi:10.1093/plcell/koab152 THE PLANT CELL 2021: 33: 2716–2735 The circadian-controlled PIF8–BBX28 module regulates petal senescence in rose flowers by governing mitochondrial ROS homeostasis at night Downloaded from https://academic.oup.com/plcell/article/33/8/2716/6287073 by guest on 28 September 2021 Yi Zhang ,1,‡ Zhicheng Wu ,1,‡ Ming Feng ,1 Jiwei Chen ,1 Meizhu Qin ,1 Wenran Wang,1 Ying Bao ,2 Qian Xu ,1 Ying Ye ,1 Chao Ma ,1 Cai-Zhong Jiang ,3,4 Su-Sheng Gan ,5 Hougao Zhou ,6 Youming Cai,7 Bo Hong ,1 Junping Gao 1 and Nan Ma 1,*,† 1 Department of Ornamental Horticulture, State Key Laboratory of Agrobiotechnology, Beijing Key Laboratory of Development and Quality Control of Ornamental Crops, College of Horticulture, China Agricultural University, Beijing, 100193, China Research Article 2 Faculty of Life Science, Tangshan Normal University, Tangshan, 063000, Hebei, China 3 United States Department of Agriculture, Crop Pathology and Genetic Research Unit, Agricultural Research Service, University of California, Davis, CA, USA 4 Department of Plant Sciences, University of California, Davis, CA, USA 5 Plant Biology Section, School of Integrative Plant Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, NY, USA 6 College of Agriculture and Biology, Zhongkai University of Agriculture and Engineering, Guangzhou, 510225, China 7 Shanghai Academy of Agricultural Sciences, Shanghai, 201403, China *Author for correspondence: [email protected] †Senior author ‡These authors contributed equally to this article (Y.Z, Z.W.). Y.Z.,Z.W.,M.F.,J.C.,M.Q.,W.W.,Y.B.,Q.X.,andY.Y.performedtheexperiments.N.M.andJ.G.designedtheresearch.C.M,C.J.,S.G.,H.Z.,Y.C.,B.H., and N.M. provided technical support, conceptual advice, and data analysis. Y.Z., Z.W., N.M., and J.G. wrote the manuscript. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (https://academic.oup.com/plcell) is: Nan Ma ([email protected]). Abstract Reactive oxygen species (ROS) are unstable reactive molecules that are toxic to cells. Regulation of ROS homeostasis is cru- cial to protect cells from dysfunction, senescence, and death. In plant leaves, ROS are mainly generated from chloroplasts and are tightly temporally restricted by the circadian clock. However, little is known about how ROS homeostasis is regu- lated in nonphotosynthetic organs, such as petals. Here, we showed that hydrogen peroxide (H2O2) levels exhibit typical circadian rhythmicity in rose (Rosa hybrida) petals, consistent with the measured respiratory rate. RNA-seq and functional screening identified a B-box gene, RhBBX28, whose expression was associated with H2O2 rhythms. Silencing RhBBX28 accelerated flower senescence and promoted H2O2 accumulation at night in petals, while overexpression of RhBBX28 had the opposite effects. RhBBX28 influenced the expression of various genes related to respiratory metabolism, including the TCA cycle and glycolysis, and directly repressed the expression of SUCCINATE DEHYDROGENASE 1, which plays a central role in mitochondrial ROS (mtROS) homeostasis. We also found that PHYTOCHROME-INTERACTING FACTOR8 (RhPIF8) could activate RhBBX28 expression to control H2O2 levels in petals and thus flower senescence. Our results indicate that the circadian-controlled RhPIF8–RhBBX28 module is a critical player that controls flower senescence by governing mtROS homeostasis in rose. Received November 23, 2020. Accepted May 19, 2021. Advance access publication May 27, 2021 VC The Author(s) 2021. Published by Oxford University Press on behalf of American Society of Plant Biologists. Open Access This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re- use, please contact [email protected] The Plant Cell, 2021 Vol. 33, No. 8 THE PLANT CELL 2021: 33: 2716–2735 | 2717 Downloaded from https://academic.oup.com/plcell/article/33/8/2716/6287073 by guest on 28 September 2021 Introduction metabolic activity or an intense rate of electron flow, such as chloroplasts, mitochondria, peroxisomes, and microbodies Senescence is the final stage in the development of a plant in plant cells (Foyer et al., 1994; Apel and Hirt, 2004; Mittler organ and usually leads to programmed death of all constit- et al., 2004; Navrot et al., 2007). ROS are commonly toxic to uent cells. Accordingly, senescence is a tightly controlled cells, although some, such as H O , are important regulatory process during which plants remobilize nutrients from sen- 2 2 escing leaves or petals to other developing organs, such as molecules that are broadly involved in multiple cell signaling seeds, stems, or roots (van Doorn and Woltering, 2004; pathways (Cezary et al., 2018). Therefore, cellular ROS ho- Rogers, 2006; Lim et al., 2007; Schippers et al., 2015; Rogers meostasis must be tightly controlled to protect cells from and Munne´-Bosch, 2016; Kim et al., 2017). This important dysfunction and death. and unique process is coordinately regulated by various in- In leaves, chloroplasts are the main source of ROS, which ternal and external factors, including developmental status, are generated in chloroplast thylakoids through electron reactive oxygen species (ROS) signaling, phytohormones, the transfer from photosynthetic chain components (Asada, circadian clock, and light (Gan and Amasino, 1995; Lim et 2006; Foyer and Noctor, 2013; Ishida et al., 2014). al., 2007; van Doorn and Woltering, 2008; Rogers, 2013; Accumulating evidence shows that ROS homeostasis is Liebsch and Keech, 2016; Rogers and Munne´-Bosch, 2016; governed by the circadian clock. The circadian clock is an Kim et al., 2017; Ma et al., 2018). endogenous timekeeping mechanism that controls a wide ROS play a key role in regulating plant organ senescence range of developmental and metabolic processes in most (Apel and Hirt, 2004; van Doorn and Woltering, 2008; organisms (McClung, 2006; Edgar et al., 2012).In Khanna-Chopra, 2012; Guo et al., 2017). Precocious leaf se- Arabidopsis leaves, ROS homeostasis and expression of ROS- nescence is a typical phenotype seen in the Arabidopsis responsive genes are circadian-regulated (Covington et al., (Arabidopsis thaliana) constitutive expression of pr genes5 2008; Lai et al., 2012). For example, their H2O2 levels exhibit and jungbrunnen1 mutants, which produce excessive a typical diurnal oscillation, with a peak in the afternoon amounts of hydrogen peroxide (H2O2)(Jing et al., 2008; and a trough at midnight, consistent with the expression dy- Wu et al., 2012). Conversely, age-dependent leaf senes- namics of photosynthetic genes (Lai et al., 2012). Mutation cence is delayed in nac with transmembrane motif 1-like4, in the key circadian clock component gene CIRCADIAN ARABIDOPSIS A-FIFTEEN knockout,andwrky75 mutants CLOCK ASSOCIATED1 (CCA1) abolishes the rhythmicity of that generate lower than normal amounts of H2O2 (Olsen both H2O2 level and the expression of catalase genes, which et al., 2005; Chen et al., 2012; Lee et al., 2012; Guo et al., encode the key enzyme for H2O2 scavenging, indicating 2017). that ROS homeostasis is tightly linked to the fluctuation of ROS are generated as byproducts of various metabolic light-harvesting capacity in leaves (Harmer et al., 2000; Lai et processes that occur in organelles with a highly oxidizing al., 2012). Moreover, leaf senescence is also significantly 2718 | THE PLANT CELL 2021: 33: 2716–2735 Y. Zhang et al. accelerated in various mutants of circadian clock compo- Zeitgeber Time (ZT) 0, and dipped in the afternoon at nent genes, including cca1, late elongated hypocotyl, early- ZT8 (Figure 1A), in a pattern opposite to that seen in leaves flowering 3 (elf3), elf4,andlux arrhythmo, suggesting that (Lai et al., 2012). disrupting ROS rhythmicity may lead to senescence (Song et We next investigated whether the observed pattern per- al., 2018; Zhang et al., 2018). sisted in constant light (LL) and dark (DD) conditions by Generally, petals are considered to share common evolu- transferring rose plants grown in LD conditions to LL or DD tionary origins with leaves, although they have very different conditions to monitor H2O2 levels in the absence of entrain- functions (Friedman et al., 2004; Rogers and Munne´-Bosch, ing cues. H2O2 production rhythms in petals persisted in LL 2016). Petals are a specialized form of leaves that have and DD conditions as in LD conditions, but were higher in different colors and shapes to attract pollinators while lack- DD than in LL conditions (Figure 1, A–C). In addition, we ing photosynthetic ability (Glover and Martin, 1998). Petal monitored the respiration dynamic in petals. Notably, the senescence is tightly regulated by various developmental sig- respiration rate of petals also exhibited a circadian rhythm, Downloaded from https://academic.oup.com/plcell/article/33/8/2716/6287073 by guest on 28 September 2021 nals and is less affected by environmental stimuli than leaf with the same phase as the pattern of H2O2 production senescence (Rogers, 2006; van Doorn and Woltering, 2008). (Figure 1D). As for leaves, a rise in ROS levels and an imbalance in redox It has been reported that respiration
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