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Leaf Senescence: Progression, Regulation, and Application Yongfeng Guo1†, Guodong Ren2†, Kewei Zhang3†, Zhonghai Li4†, Ying Miao5* and Hongwei Guo6*

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Leaf Senescence: Progression, Regulation, and Application Yongfeng Guo1†, Guodong Ren2†, Kewei Zhang3†, Zhonghai Li4†, Ying Miao5* and Hongwei Guo6* Guo et al. Molecular Horticulture (2021) 1:5 Molecular Horticulture https://doi.org/10.1186/s43897-021-00006-9 REVIEW Open Access Leaf senescence: progression, regulation, and application Yongfeng Guo1†, Guodong Ren2†, Kewei Zhang3†, Zhonghai Li4†, Ying Miao5* and Hongwei Guo6* Abstract Leaf senescence, the last stage of leaf development, is a type of postmitotic senescence and is characterized by the functional transition from nutrient assimilation to nutrient remobilization which is essential for plants’ fitness. The initiation and progression of leaf senescence are regulated by a variety of internal and external factors such as age, phytohormones, and environmental stresses. Significant breakthroughs in dissecting the molecular mechanisms underpinning leaf senescence have benefited from the identification of senescence-altered mutants through forward genetic screening and functional assessment of hundreds of senescence-associated genes (SAGs) via reverse genetic research in model plant Arabidopsis thaliana as well as in crop plants. Leaf senescence involves highly complex genetic programs that are tightly tuned by multiple layers of regulation, including chromatin and transcription regulation, post-transcriptional, translational and post-translational regulation. Due to the significant impact of leaf senescence on photosynthesis, nutrient remobilization, stress responses, and productivity, much effort has been made in devising strategies based on known senescence regulatory mechanisms to manipulate the initiation and progression of leaf senescence, aiming for higher yield, better quality, or improved horticultural performance in crop plants. This review aims to provide an overview of leaf senescence and discuss recent advances in multi-dimensional regulation of leaf senescence from genetic and molecular network perspectives. We also put forward the key issues that need to be addressed, including the nature of leaf age, functional stay-green trait, coordination between different regulatory pathways, source-sink relationship and nutrient remobilization, as well as translational researches on leaf senescence. Keywords: Leaf senescence, Chlorophyll degradation, Phytohormones, Abiotic stress, Chromatin remodeling, Nutrient remobilization, Yield Introduction 1997; Guo and Gan 2005). Mitotic senescence occurs in Senescence is the final stage of plant development and is shoot apical meristem (SAM) containing multipotent characterized by a series of programmed disassembly stem cells, similar to replicative senescence in mamma- and degenerative events (Guo and Gan 2005; Lim et al. lian cell cultures and yeast (Gan and Amasino 1997; 2007). In plants, there are two types of senescence: mi- Guo and Gan 2005). In contrast, post-mitotic senescence totic and post-mitotic senescence (Gan and Amasino occurs in organs such as leaves and flowers. Leaves are organs that characterize plants as autotrophic organisms * Correspondence: [email protected]; [email protected] and perhaps the primary source of food on earth which †Yongfeng Guo, Guodong Ren, Kewei Zhang and Zhonghai Li contributed equally to this work. use light energy to fix carbon. As leaves age, chloroplast 5Fujian Provincial Key Laboratory of Plant Functional Biology, Fujian degeneration is initiated, paralleled by catabolism of Agriculture and Forestry University, Fuzhou 350002, Fujian, China macromolecules, including nucleic acids, proteins and 6Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Department of Biology, Southern University of lipids. The released nutrients are exported to other de- Science and Technology (SUSTech), Shenzhen 518055, Guangdong, China veloping organs, such as new buds, young leaves, flowers Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Guo et al. Molecular Horticulture (2021) 1:5 Page 2 of 25 or seeds, which leads to increased reproductive success of senescence. Ethylene, jasmonic acid (JA), salicylic acid (Lim et al. 2007). In perennial plants, such as deciduous (SA), abscisic acid (ABA), and strigolactones (SLs) pro- trees, nutrients disassembled from senescent leaves are mote leaf senescence, while cytokinins (CKs), gibberellic relocated to form bark storage proteins (BSP) in phloem acid (GA), and auxin delay leaf senescence (Gan and tissues, stored over the winter, and then remobilized and Amasino 1995, 1997; Lim et al. 2007; Miao and Zentgraf reutilized for shoot or flower growth during the next 2007; Li et al. 2013; Zhang et al. 2013). Multiple envir- growing season (Cooke and Weih 2005; Keskitalo et al. onmental factors, including abiotic stresses such as 2005). Therefore, the appropriate initiation and progres- drought, salt, DNA damage, high or low temperature, sion of leaf senescence are essential for plant fitness darkness and nutrient deficiency, and biotic stresses (Uauy et al. 2006). Efficient senescence is critical for such as pathogen infection and phloem-feeding insects maximizing viability in the next generation or season, are also critical in regulating senescence (Lim et al. while premature senescence induced by numerous envir- 2007; Guo and Gan 2012; Sade et al. 2018). Recent stud- onmental factors decreases the yield and fresh product ies reveal that DNA damage, caused by endogenous in- quality of crop plants (Hortensteiner and Feller 2002). sults or exogenous genotoxic stresses, might be one of These insights suggest that leaf senescence evolves as a the main determinants of leaf senescence (Li et al. 2020; life history strategy and is of substantial biological sig- Zhang et al. 2020c). Cellular calcium acts as a universal nificance. Understanding the regulatory mechanisms of second messenger, which has allosteric effects on nu- leaf senescence will provide valuable clues and a theoret- merous enzymes and proteins in a variety of cellular re- ical basis for manipulation of this trait in agronomically sponses. In plants, calcium signaling is evoked by important plants (Guo and Gan 2014). endogenous and environmental factors. Ca2+ ions play Leaf senescence is not a passive but a highly coordinated an important role in plant senescence, and exogenous process regulated by hundreds of senescence-associated genes application of Ca2+ delays the senescence process of de- (SAGs), whose transcripts increase as leaves age (Guo and tached leaves (Poovaiah and Leopold 1973). Elevated Gan 2005; Lim et al. 2007). Many breakthroughs in dissect- CO2 usually leads to the accumulation of sugars and the ing the regulatory mechanisms underpinning leaf senescence decrease of nitrogen content in plant leaves, resulting in have benefited from the identification and functional assess- the imbalance of C/N ratio in mature leaves, which is ment of hundreds of SAGs and their corresponding mutants also one of the main factors causing premature leaf sen- in Arabidopsis thaliana,tomato(Solanum lycopersicon), to- escence (Wingler et al. 2004; Agüera and De la Haba bacco (Nicotiana tabaccum), rice (Oryza sativa)orwheat 2018). For plants, stress-induced premature senescence (Triticum aestivum)(Breezeetal.2011;Wooetal.2016;Li may not be a passive choice, but is an evolutionary fit- et al. 2018, 2020). Forward genetic studies by screening for ness strategy, which speeds up the reproduction of the mutants affected in senescence and reverse genetic analysis next generation under unfavorable living conditions of SAGs provide insights into the molecular mechanisms of (Sade et al. 2018). However, each factor does not work leaf senescence. Currently, 5853 SAGs and 617 mutants from independently, but has mutual promotion or inhibition 68 species have been identified and manually curated and ex- (Guo and Gan 2012). Environmental stress factors trig- tensively annotated, which facilitate the systematical and ger the changes of endogenous hormones, and then comparative investigation of leaf senescence (Li et al. 2020). affect leaf senescence through a complex regulatory net- It is now clear that leaf senescence is a highly complex gen- work instead of a linear way. etic program strictly controlled by multiple layers of regula- Although continuously increasing efforts have been tion, including transcriptional, post-transcriptional, devoted to leaf senescence research, many issues remain translational and post-translational regulation (Woo et al. to be addressed on this topic (Woo et al. 2013). When 2013, 2019). Moreover, the successful
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