Leaf senescence: progression, regulation, and application

1 REVIEWOpen AccessLeaf senescence: progression, regulation, and applicationYongfeng Guo1 , Guodong Ren2 , Kewei Zhang3 , Zhonghai Li4 , Ying Miao5*and Hongwei Guo6*AbstractLeaf senescence, the last stage of leaf development, is a type of postmitotic senescence and is characterized by thefunctional transition from nutrient assimilation to nutrient remobilization which is essential for plants fitness. Theinitiation 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 mechanismsunderpinning leaf senescence have benefited from the identification of senescence-altered mutants throughforward genetic screening and functional assessment of hundreds ofsenescence-associated genes(SAGs)viareversegenetic research in model plantArabidopsis thalianaas well as in crop plants.

2 Leaf senescence involves highlycomplex genetic programs that are tightly tuned by multiple layers of regulation, including chromatin andtranscription regulation, post-transcriptional, translational and post-translational regulation. Due to the significantimpact of leaf senescence on photosynthesis, nutrient remobilization, stress responses, and productivity, mucheffort has been made in devising strategies based on known senescence regulatory mechanisms to manipulate theinitiation and progression of leaf senescence, aiming for higher yield, better quality, or improved horticulturalperformance in crop plants. This review aims to provide an overview of leaf senescence and discuss recentadvances in multi-dimensional regulation of leaf senescence from genetic and molecular network perspectives.

3 Wealso put forward the key issues that need to be addressed, including the nature of leaf age, functional stay-greentrait, coordination between different regulatory pathways, source-sink relationship and nutrient remobilization, aswell as translational researches on leaf :Leaf senescence, Chlorophyll degradation, Phytohormones, Abiotic stress, Chromatin remodeling,Nutrient remobilization, YieldIntroductionSenescence is the final stage of plant development and ischaracterized by a series of programmed disassemblyand degenerative events (Guo and Gan2005; Lim et ). In plants, there are two types of senescence: mi-totic and post-mitotic senescence (Gan and Amasino1997; Guo and Gan2005). Mitotic senescence occurs inshoot apical meristem (SAM) containing multipotentstem cells, similar to replicative senescence in mamma-lian cell cultures and yeast (Gan and Amasino1997;Guo and Gan2005).

4 In contrast, post-mitotic senescenceoccurs in organs such as leaves and flowers. Leaves areorgans that characterize plants as autotrophic organismsand perhaps the primary source of food on earth whichuse light energy to fix carbon. As leaves age, chloroplastdegeneration is initiated, paralleled by catabolism ofmacromolecules, including nucleic acids, proteins andlipids. The released nutrients are exported to other de-veloping organs, such as new buds, young leaves, flowers The Author(s). 2021 Open AccessThis article is licensed under a Creative Commons Attribution International License,which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you giveappropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate ifchanges were made.

5 The images or other third party material in this article are included in the article's Creative Commonslicence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commonslicence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtainpermission directly from the copyright holder. To view a copy of this licence, Creative Commons Public Domain Dedication waiver ( ) applies to thedata made available in this article, unless otherwise stated in a credit line to the data.* Yongfeng Guo, Guodong Ren, Kewei Zhang and Zhonghai Li contributedequally to this Provincial Key Laboratory of Plant Functional Biology, FujianAgriculture and Forestry University, Fuzhou 350002, Fujian, China6 Key Laboratory of Molecular Design for Plant Cell Factory of GuangdongHigher Education Institutes, Department of Biology, Southern University ofScience and Technology (SUSTech), Shenzhen 518055, Guangdong, ChinaFull list of author information is available at the end of the articleMolecular HorticultureGuoet al.

6 Molecular Horticulture (2021) 1:5 seeds, which leads to increased reproductive success(Lim et ). In perennial plants, such as deciduoustrees, nutrients disassembled from senescent leaves arerelocated to form bark storage proteins (BSP) in phloemtissues, stored over the winter, and then remobilized andreutilized for shoot or flower growth during the nextgrowing season (Cooke and Weih2005; Keskitalo et ). Therefore, the appropriate initiation and progres-sion of leaf senescence are essential for plant fitness(Uauy et ). Efficient senescence is critical formaximizing viability in the next generation or season,while premature senescence induced by numerous envir-onmental factors decreases the yield and fresh productquality of crop plants (Hortensteiner and Feller2002).

7 These insights suggest that leaf senescence evolves as alife history strategy and is of substantial biological sig-nificance. Understanding the regulatory mechanisms ofleaf senescence will provide valuable clues and a theoret-ical basis for manipulation of this trait in agronomicallyimportant plants (Guo and Gan2014).Leaf senescence is not a passive but a highly coordinatedprocess regulated by hundreds ofsenescence-associated genes(SAGs), whose transcripts increase as leaves age (Guo andGan2005 ; Lim et ). Many breakthroughs in dissect-ing the regulatory mechanisms underpinning leaf senescencehave benefited from the identification and functional assess-ment of hundreds of SAGs and their corresponding mutantsinArabidopsis thaliana,tomato(Solanum lycopersicon), to-bacco (Nicotiana tabaccum), rice (Oryza sativa)orwheat(Triticum aestivum)( ; ;Liet , 2020 ).

8 Forward genetic studies by screening formutants affected in senescence and reverse genetic analysisof SAGs provide insights into the molecular mechanisms ofleaf senescence. Currently, 5853 SAGs and 617 mutants from68 species have been identified and manually curated and ex-tensively annotated, which facilitate the systematical andcomparative investigation of leaf senescence (Li et ).It is now clear that leaf senescence is a highly complex gen-etic program strictly controlled by multiple layers of regula-tion, including transcriptional, post-transcriptional,translational and post-translational regulation (Woo et , 2019 ). Moreover, the successful use of multi-omicsmethods has enabled the study of the complex process of leafsenescence, replacing the component-based static view witha network-based spatial-temporal understanding (Breezeet ;Guo2013 ; Kim et ).

9 Leaf senescence is a genetically controlled develop-mental process (Gan and Amasino1997; Lim et ;Kim et ). However, the initiation of leaf senes-cence is regulated by an array of external and internalsignals that are integrated into the age information (Guoand Gan2005; Lim et ). Plant hormones aremajor players influencing each stage of leaf senescence,including the initiation, progression and terminal phaseof senescence. Ethylene, jasmonic acid (JA), salicylic acid(SA), abscisic acid (ABA), and strigolactones (SLs) pro-mote leaf senescence, while cytokinins (CKs), gibberellicacid (GA), and auxin delay leaf senescence (Gan andAmasino1995, 1997; Lim et ; Miao and Zentgraf2007; Li et ; Zhang et ). Multiple envir-onmental factors, including abiotic stresses such asdrought, salt, DNA damage, high or low temperature,darkness and nutrient deficiency, and biotic stressessuch as pathogen infection and phloem-feeding insectsare also critical in regulating senescence (Lim et ; Guo and Gan2012; Sade et ).

10 Recent stud-ies reveal that DNA damage, caused by endogenous in-sults or exogenous genotoxic stresses, might be one ofthe main determinants of leaf senescence (Li et ;Zhang et ). Cellular calcium acts as a universalsecond messenger, which has allosteric effects on nu-merous enzymes and proteins in a variety of cellular re-sponses. In plants, calcium signaling is evoked byendogenous and environmental factors. Ca2+ions playan important role in plant senescence, and exogenousapplication of Ca2+delays the senescence process of de-tached leaves (Poovaiah and Leopold1973). ElevatedCO2usually leads to the accumulation of sugars and thedecrease of nitrogen content in plant leaves, resulting inthe imbalance of C/N ratio in mature leaves, which isalso one of the main factors causing premature leaf sen-escence (Wingler et ; Ag era and De la Haba2018).