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Enigmas of senescence: a reappraisal on the hormonal crosstalk and the molecular mechanisms

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Abstract

Due to the already strained and severely challenged agricultural ecosystems of the modern world, predicted changes in life cycle of plants, including leaf senescence are receiving significant attention from stakeholders. The onset, progression and terminal phases of leaf senescence are greatly influenced by plant hormones. The senescence of leaves is accelerated by ethylene, jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), brassinosteroids and strigolactones (SLs), whereas it is postponed by cytokinins (CKs), gibberellic acid (GA) and auxins. The crosstalk and signal transduction pathways between these growth regulators have been found to regulate leaf senescence by orchestrating various developmental and environmental factors. Premature leaf senescence lessens the plant’s nutritional capacity and shortens the vegetative production schedule, prompting an early transition from the vegetative to the reproductive stage and diminishing crop potential. As a result, a complete understanding of leaf senescence and finding novel ways to delay it is crucial for agricultural productivity. The ability to manipulate leaf senescence for agricultural enhancement has been made possible by significant advances in physiological and molecular awareness of leaf senescence. Although studies pertaining to leaf senescence have been given steadily more attention, there are still numerous challenges that need to be resolved. In this perspective, this review focuses on current advances in understanding the leaf senescence by molecular and genetic analyses with an emphasis on hormonal regulation of leaf senescence. We also hypothesize future research to better comprehend leaf senescence by employing various current technologies.

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References

  • Abeed AH, Eissa MA, Abdel-Wahab DA (2020) Effect of exogenously applied jasmonic acid and kinetin on drought tolerance of wheat cultivars based on morpho-physiological evaluation. J Soil Sci Plant Nutr 21(1):131–144

    Google Scholar 

  • Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60(4):1085–1092

    CAS  PubMed  Google Scholar 

  • Adie BA, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defences in Arabidopsis. Plant Cell 19(5):1665–1681

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alharbi B, Hunt JD, Dimitrova S, Spadafora ND, Cort AP, Colombo D et al (2020) Mutation of Arabidopsis copper-containing amine oxidase gene AtCuAOδ alters polyamines, reduces gibberellin content and affects development. Int J Molecular Sci 21(20):7789

    CAS  Google Scholar 

  • Altaf F, Parveen S, Farooq S, Ul Haq A et al (2022) Polyamines effectively mitigate senescence in persistent leaves of Berginia ciliata–a novel model system. Func Plant Biol. https://doi.org/10.1071/FP21273

    Article  Google Scholar 

  • Altaf F, Parveen S, Lone ML, Haq AU, Farooq S, Tahir I et al (2023) Modulation of leaf senescence in Bergenia ciliata (haw.) Sternb. through the supplementation of kinetin and methyl jasmonate. Pak J Bot 56:2

    Google Scholar 

  • An JP, Zhang XW, Liu YJ, Zhang JC, Wang XF, You CX, Hao YJ (2021) MdABI5 works with its interaction partners to regulate abscisic acid-mediated leaf senescence in apple. Plant J 105(6):1566–1581

    CAS  PubMed  Google Scholar 

  • Balibrea Lara ME, Gonzalez Garcia MC, Fatima T, Ehneß R, Lee TK et al (2004) Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16(5):1276–1287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bassham DC, Laporte M, Marty F et al (2006) Autophagy in development and stress responses of plants. Autophagy 2(1):2–11

    CAS  PubMed  Google Scholar 

  • Bengoa Luoni S, Astigueta FH, Nicosia S, Moschen S, Fernandez P, Heinz R (2019) Transcription factors associated with leaf senescence in crops. Plants 8(10):411

    PubMed  PubMed Central  Google Scholar 

  • Besseau S, Li J, Palva ET (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J Exp Bot 63:2667–2679

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhardwaj S, Sharma D, Jan S, Singh R, Bhardwaj R, Kapoor D (2022) Crosstalk of ethylene and other phytohormones in the regulation of plant development. Ethylene Plant Biol. https://doi.org/10.1002/9781119744719.ch2

    Article  Google Scholar 

  • Bian Z, Gao H, Wang C (2020) NAC transcription factors as positive or negative regulators during ongoing battle between pathogens and our food crops. Int J Mol Sci 22(1):81

    PubMed  PubMed Central  Google Scholar 

  • Blume YB, Krasylenko YA, Yemets AI (2017) The role of the plant cytoskeleton in phytohormone signaling under abiotic and biotic stresses. Mech Plant Hormone Signal under Stress 2:127–185

    Google Scholar 

  • Breeze E, Harrison E, McHattie S et al (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23(3):873–894

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brenner WG, Ramireddy E, Heyl A, Schmülling T (2012) Gene regulation by cytokinin in Arabidopsis. Front Plant Sci 3:8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brusslan JA, Bonora G, Rus-Canterbury AM, Tariq F, Jaroszewicz A, Pellegrini M (2015) A genome-wide chronological study of gene expression and two histone modifications, H3K4me3 and H3K9ac, during developmental leaf senescence. Plant Physiol 168:1246–1261

    CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42(4):567–585

    CAS  PubMed  Google Scholar 

  • Buet A, Costa ML, Martínez DE, Guiamet JJ (2019) Chloroplast protein degradation in senescing leaves: proteases and lytic compartments. Front Plant Sci 10:747

    PubMed  PubMed Central  Google Scholar 

  • Carrión CA, Costa ML, Martinez DE et al (2013) In vivo inhibition of cysteine proteases provides evidence for the involvement of ‘senescence-associated vacuoles’ in chloroplast protein degradation during dark-induced senescence of tobacco leaves. J Exp Bot 64:4967–4980. https://doi.org/10.1093/jxb/ert285

    Article  CAS  PubMed  Google Scholar 

  • Cha JY, Kim MR, Jung IJ, Kang SB, Park HJ et al (2016) The thiol reductase activity of YUCCA6 mediates delayed leaf senescence by regulating genes involved in auxin redistribution. Front Plant Sci 7:626

    PubMed  PubMed Central  Google Scholar 

  • Chai J, Liu J, Zhou J, Xing D (2014) Mitogen-activated protein kinase 6 regulates NPR1 gene expression and activation during leaf senescence induced by salicylic acid. J Exp Bot 65(22):6513–6528

    CAS  PubMed  Google Scholar 

  • Chen M, Maodzeka A, Zhou L, Ali E, Wang Z, Jiang L (2014) Removal of DELLA repression promotes leaf senescence in Arabidopsis. Plant Sci 219:26–34

    PubMed  Google Scholar 

  • Chen X, Lu L, Mayer KS, Scalf M, Qian S, Lomax A, Smith LM, Zhong X (2016) POWERDRESS interacts with HISTONE DEACETYLASE 9 to promote aging in Arabidopsis. Elife. https://doi.org/10.7554/eLife.17214

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen L, Xiang S, Chen Y, Li D, Yu D (2017) Arabidopsis WRKY45 interacts with the DELLA protein RGL1 to positively regulate age-triggered leaf senescence. Mol Plant 10(9):1174–1189

    CAS  PubMed  Google Scholar 

  • Chen K, Li GJ, Bressan RA, Song CP, Zhu JK, Zhao Y (2020) Abscisic acid dynamics, signaling, and functions in plants. J Integ Plant Biol 62(1):25–54

    CAS  Google Scholar 

  • Cho EJ, Choi SH, Kim JH, Kim JE, Lee MH, Chung BY, Woo HR, Kim JH (2016) A mutation in plant-specific SWI2/SNF2-like chromatin-remodeling proteins, DRD1 and DDM1, delays leaf senescence in Arabidopsis thaliana. PLoS ONE 11:e0146826

    PubMed  PubMed Central  Google Scholar 

  • Christ B, Hörtensteiner S (2014) Mechanism and significance of chlorophyll breakdown. J Plant Growth Regul 33:4–20

    CAS  Google Scholar 

  • Crane RA, Cardénas Valdez M, Castaneda N, Jackson CL, Riley CJ, Mostafa I et al (2019) Negative regulation of age-related developmental leaf senescence by the IAOx pathway, PEN1, and PEN3. Front Plant Sci 10:1202

    PubMed  PubMed Central  Google Scholar 

  • Danilova MN, Doroshenko AS, Kudryakova NV et al (2020) The crosstalk between cytokinin and auxin signaling pathways in the control of natural senescence of Arabidopsis thaliana Leaves. Russ J Plant Physiol 67:1028–1035

    CAS  Google Scholar 

  • De Vleesschauwer D, Yang Y, Cruz CV, Hofte M (2010) Abscisic acid-induced resistance against the brown spot pathogen Cochliobolus miyabeanus in rice involves MAP kinase-mediated repression of ethylene signaling. Plant Physiol 152:2036–2052

    PubMed  PubMed Central  Google Scholar 

  • Ding F, Wang C, Xu N, Zhang S, Wang M (2022) SlMYC2 mediates jasmonate-induced tomato leaf senescence by promoting chlorophyll degradation and repressing carbon fixation. Plant Physiol Biochem 180:27–34

    CAS  PubMed  Google Scholar 

  • Domínguez F, Cejudo FJ (2021) Chloroplast dismantling in leaf senescence. J Exp Bot 72(16):5905–5918

    PubMed  PubMed Central  Google Scholar 

  • Dubois M, Van den Broeck L, Inzé D (2018) The pivotal role of ethylene in plant growth. Trends in Plant Sci 23(4):311–323

    CAS  Google Scholar 

  • Fan ZQ, Tan XL, Shan W, Kuang JF, Lu WJ, Chen JY (2018) Characterization of a transcriptional regulator, BrWRKY6, associated with gibberellin-suppressed leaf senescence of Chinese flowering cabbage. J Agric Food Chem 66(8):1791–1799

    CAS  PubMed  Google Scholar 

  • Fan ZQ, Tan XL, Shan W, Kuang JF, Lu WJ, Lin HT et al (2020) Involvement of BrNAC041 in ABA-GA antagonism in the leaf senescence of Chinese flowering cabbage. Postharvest Biol Technol 168:111254

    CAS  Google Scholar 

  • Fan ZQ, Wei W, Tan XL, Shan W, Kuang JF, Lu WJ et al (2021) A NAC transcription factor BrNAC087 is involved in gibberellin-delayed leaf senescence in Chinese flowering cabbage. Postharvest Biol Technol 181:111673

    CAS  Google Scholar 

  • Fang C, Zhang H, Wan J, Wu Y et al (2016) Control of leaf senescence by an MeOH-jasmonates cascade that is epigenetically regulated by OsSRT1 in rice. Mol Plant 9(10):1366–1378

    CAS  PubMed  Google Scholar 

  • Floyd BE, Pu Y, Soto-Burgos J, Bassham DC (2015) To live or Die: autophagy in plants. In: Gunawardena AN, McCabe PF (eds) Plant programmed cell death. Springer International Publishing, Cham, pp 269–300

    Google Scholar 

  • Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X, Kuai B (2016) ABF2, ABF3 and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in Arabidopsis. Mol Plant 9(9):1272–1285

    CAS  PubMed  Google Scholar 

  • Gao F, Mei X, Li Y, Guo J, Shen Y (2021) Update on the roles of polyamines in fleshy fruit ripening. Senes Quality Front Plant Sci 12:610313

    Google Scholar 

  • Goyal P, Devi R, Verma B et al (2023) WRKY transcription factors: evolution, regulation, and functional diversity in plants. Protoplasma 260:331–348

    CAS  PubMed  Google Scholar 

  • Grbić V, Bleecker AB (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. The Plant J 8(4):595–602

    Google Scholar 

  • Griffiths CA, Gaff DF, Neale AD (2014) Drying without senescence in resurrection plants. Front Plant Sci 5:36

    PubMed  PubMed Central  Google Scholar 

  • Guo Y, Gan S (2005) Leaf senescence: signals, execution and regulation. Curr Top Dev Biol 71:83–112

    CAS  PubMed  Google Scholar 

  • Guo Y, Gan SS (2014) Translational researches on leaf senescence for enhancing plant productivity and quality. J Exp Bot 65:3901–3913

    PubMed  Google Scholar 

  • Guo P, Li Z, Huang P, Li B, Fang S, Chu J, Guo H (2017) A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid and reactive oxygen species accelerates leaf senescence. Plant Cell 29(11):2854–2870

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Ren G, Zhang K, Li Z, Miao Y, Guo H (2021) Leaf senescence: Progression, regulation and application. Mol Horticul 1(1):1–25

    Google Scholar 

  • Hall BP, Shakeel SN, Amir M, Haq NU, Qu X, Schaller GE (2012) Histidine kinase activity of the ethylene receptor ETR1 facilitates the ethylene response in Arabidopsis. Plant Physiol 159(2):682–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hallmark HT, Rashotte AM (2020) Cytokinin isopentenyladenine and its glucoside isopentenyladenine-9G delay leaf senescence through activation of cytokinin-associated genes. Plant Direct 4(12):e00292

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan SA, Hayat S, Ahmad A (2011) Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 84:1446–1451

    CAS  PubMed  Google Scholar 

  • He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hou K, Wu W, Gan SS (2013) SAUR36, a small auxin up RNA gene, is involved in the promotion of leaf senescence in Arabidopsis. Plant Physiol 161(2):1002–1009

    CAS  PubMed  Google Scholar 

  • Hu Y, Jiang Y, Han X, Wang H, Pan J, Yu D (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J Exp Bot 68(6):1361–1369

    CAS  PubMed  Google Scholar 

  • Hu Q, Ding F, Li M, Zhang X, Zhang S, Huang B (2021) Strigolactone and ethylene inhibitor suppressing dark-induced leaf senescence in perennial ryegrass involving transcriptional downregulation of chlorophyll degradation. J Am Soc Hortic Sci 146(2):79–86

    CAS  Google Scholar 

  • Huang Y, Chen CT, Kao CH (1990) Senescence of rice leaves XXIV. Involvement of calcium and calmodulin in the regulation of senescence. Plant Cell Physiol 31:1015–1020

    CAS  Google Scholar 

  • Huang W, Chen Q, Zhu Y, Hu F, Zhang L, Ma Z, He Z, Huang J (2013) Arabidopsis thylakoid formation 1 is a critical regulator for dynamics of PSII– LHCII complexes in leaf senescence and excess light. Mol Plant 6:673–691

    Google Scholar 

  • Huang CK, Lo PC, Huang LF, Wu SJ, Yeh CH, Lu CA (2015) A single-repeat MYB transcription repressor, MYBH, participates in regulation of leaf senescence in Arabidopsis. Plant Mol Biol 88:269–286

    CAS  PubMed  Google Scholar 

  • Huang Y, Jiao Y, Xie N, Guo Y, Zhang F, Xiang Z et al (2019) OsNCED5, a 9-cis-epoxycarotenoid dioxygenase gene, regulates salt and water stress tolerance and leaf senescence in rice. Plant Sci 287:110188

    CAS  PubMed  Google Scholar 

  • Hung KT, Hsu YT, Kao CH (2006) Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol Plant 127(2):293–303

    CAS  Google Scholar 

  • James M, Poret M, Masclaux-Daubresse C (2018) SAG12, a major cysteine protease involved in nitrogen allocation during senescence for seed production in Arabidopsis thaliana. Plant Cell Physiol 59:2052–2063

    CAS  PubMed  Google Scholar 

  • Jan S, Abbas N, Ashraf M, Ahmad P (2019) Roles of potential plant hormones and transcription factors in controlling leaf senescence and drought tolerance. Protoplasma 256(2):313–329

    CAS  PubMed  Google Scholar 

  • Janečková H, Husičková A, Lazár D, Ferretti U, Pospíšil P, Špundová M (2019) Exogenous application of cytokinin during dark senescence eliminates the acceleration of photosystem II impairment caused by chlorophyll b deficiency in barley. Plant Physiol Biochem 136:43–51

    PubMed  Google Scholar 

  • Jia M, Liu X, Xue H, Wu Y, Shi L, Wang R et al (2019) Noncanonical ATG8–ABS3 interaction controls senescence in plants. Nature Plants 5(2):212–224

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Liang G, Yang S, Yu D (2014) Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid– and auxin-mediated signaling in jasmonic acid–induced leaf senescence. Plant Cell 26:230–245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jibran RA, Hunter D, Dijkwel P (2013) Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol 82:547–561

    CAS  PubMed  Google Scholar 

  • Jing Y, Liu J, Liu P, Ming D, Sun J (2019) Overexpression of TaJAZ1 increases powdery mildew resistance through promoting reactive oxygen species accumulation in bread wheat. Sci Rep 95:691

    Google Scholar 

  • Joshi S, Choukimath A, Isenegger D, Panozzo J, Spangenberg G, Kant S (2019) Improved wheat growth and yield by delayed leaf senescence using developmentally regulated expression of a cytokinin biosynthesis gene. Front in Plant Sci 10:1285

    Google Scholar 

  • Kang S, Shin KD, Kim JH, Chung T (2018) Autophagy-related (ATG) 11, ATG9 and the phosphatidylinositol 3-kinase control ATG2-mediated formation of autophagosomes in Arabidopsis. Plant Cell Rep 37(4):653–664

    CAS  PubMed  Google Scholar 

  • Khan M, Rozhon W, Poppenberger B (2014) The role of hormones in the aging of plants – a mini-review. Gerontology 60:49–55

    CAS  PubMed  Google Scholar 

  • Khanna-Chopra R (2012) Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 249(3):469–481

    CAS  PubMed  Google Scholar 

  • Kikuchi Y, Nakamura S, Woodson JD et al (2020) Chloroplast autophagy and ubiquitination combine to manage oxidative damage and starvation responses. Plant Physiol 183(4):1531–1544

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J (2019) Sugar metabolism as input signals and fuel for leaf senescence. Genes Genomics 41(7):737–746

    CAS  PubMed  Google Scholar 

  • Kim JH, Woo HR, Kim J, Lim PO, Lee IC, Choi SH, Nam HG (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323(5917):1053–1057

    CAS  PubMed  Google Scholar 

  • Kim JI, Murphy AS, Baek D, Lee SW, Yun DJ et al (2011) YUCCA6 over-expression demonstrates auxin function in delaying leaf senescence in Arabidopsis thaliana. J Exp Bot 62:3981–3992

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J, Woo HR, Nam HG (2016) Towards systems understanding of leaf senescence: an integrated multi-omics perspective on leaf senescence research. Mol Plant 9(6):813–825

    CAS  PubMed  Google Scholar 

  • Kim J, Kim JH, Lyu JI, Woo HR, Lim PO (2018) New insights into the regulation of leaf senescence in Arabidopsis. J Exp Bot 69(4):787–799

    CAS  PubMed  Google Scholar 

  • Kim Y, Park SU, Shin DM, Pham G, Jeong YS, Kim SH (2020) ATBS1-INTERACTING FACTOR 2 negatively regulates dark-and brassinosteroid-induced leaf senescence through interactions with INDUCER OF CBF EXPRESSION 1. J Exp Bot 71(4):1475–1490

    CAS  PubMed  Google Scholar 

  • Köllmer I, Werner T, Schmülling T (2011) Ectopic expression of different cytokinin-regulated transcription factor genes of Arabidopsis thaliana alters plant growth and development. J Plant Physiol 168(12):1320–1327

    PubMed  Google Scholar 

  • Kovtun IS, Kukharenko NE et al (2021) Effect of lactone-and ketone-containing brassinosteroids on photosynthetic activity of barley leaves during aging. Russian J Plant Physiol 68(3):440–450

    CAS  Google Scholar 

  • Koyama T (2018) A hidden link between leaf development and senescence. Plant Sci 276:105–110

    CAS  PubMed  Google Scholar 

  • Kumar S, Shah SH, Vimala Y, Jatav HS, Ahmad P, Chen Y, Siddique KH (2022) Abscisic acid: metabolism, transport, crosstalk with other plant growth regulators, and its role in heavy metal stress mitigation. Front Plant Sci 13:972856

    PubMed  PubMed Central  Google Scholar 

  • Lei W, Li Y, Yao X et al (2020) NAP is involved in GA-mediated chlorophyll degradation and leaf senescence by interacting with DELLAs in Arabidopsis. Plant Cell Rep 39(1):75–87. https://doi.org/10.1007/s00299-019-02474-2

    Article  CAS  PubMed  Google Scholar 

  • Li QF, Wang C, Jiang L, Li S, Sun SS, He JX (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5(244):72–72

    Google Scholar 

  • Li FQ, Chung T, Vierstra RD (2014) AUTOPHAGY-RELATED11 plays a critical role in general autophagy- and senescence-induced mitophagy in Arabidopsis. Plant Cell 26:788–807

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Chang Y, Zhao C, Yang H, Ren D (2016) Expression of the inactive ZmMEK1 induces salicylic acid accumulation and salicylic acid-dependent leaf senescence. J Integr Plant Biol 58(8):724–736

    CAS  PubMed  Google Scholar 

  • Li L, Nelson CJ, Trösch J, Castleden I, Huang S, Millar AH (2017) Protein degradation rate in Arabidopsis thaliana leaf growth and development. Plant Cell 29:207–228

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li A, Sun X, Liu L (2022) Action of salicylic acid on plant growth. Front Plant Sci 13:878076

    PubMed  PubMed Central  Google Scholar 

  • Liebers M, Grübler B, Chevalier F, Lerbs-Mache S, Merendino L, Blanvillain R, Pfannschmidt T (2017) Regulatory shifts in plastid transcription play a key role in morphological conversions of plastids during plant development. Front Plant Sci 8:23

    PubMed  PubMed Central  Google Scholar 

  • Liebsch D, Juvany M, Li Z, Wang HL, Ziolkowska A, Chrobok D et al (2022) Metabolic control of arginine and ornithine levels paces the progression of leaf senescence. Plant Physiol 189(4):1943–1960

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    CAS  PubMed  Google Scholar 

  • Lim PO, Lee IC, Kim J et al (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J Exp Bot 61:1419–1430

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lim C, Kang K, Shim Y, Sakuraba Y, An G, Paek NC (2020) Rice ETHYLENE RESPONSE FACTOR 101 promotes leaf senescence through jasmonic acid-mediated regulation of OsNAP and OsMYC2. Front Plant Sci 11:1096

    PubMed  PubMed Central  Google Scholar 

  • Liu YM, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5(7):954–963

    CAS  PubMed  Google Scholar 

  • Liu X, Mao K, Yu AYH, Omairi-Nasser A, Austin J, Glick BS, Yip CK, Klionsky DJ (2016) The ATG17-ATG31-ATG29 complex coordinates with Atg11 to recruit the Vam7 SNARE and mediate autophagosome-vacuole fusion. Curr Biol 26:150–160

    PubMed  PubMed Central  Google Scholar 

  • Liu Y, Qi Z, Wei J, Yu J, Xia X (2022) Brassinosteroids promote starch synthesis and the implication in low-light stress tolerance in Solanum lycopersicum. Environ Exp Bot 201:104990

    CAS  Google Scholar 

  • Lumba S, Tsuchiya Y, Delmas F, Hezky J, Provart NJ, Shi LuQ, McCourt P, Gazzarrini S (2012) The embryonic leaf identity gene FUSCA3 regulates vegetative phase transitions by negatively modulating ethylene-regulated gene expression in Arabidopsis. BMC Biol 10:8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Luo L, Li Z, Tang MY, Cheng BZ, Zeng WH, Peng Y et al (2020) Metabolic regulation of polyamines and γ-aminobutyric acid in relation to spermidine-induced heat tolerance in white clover. Plant Biol 22(5):794–804

    CAS  PubMed  Google Scholar 

  • Lyousfi N, Lahlali R, Letrib C, Belabess Z, Ouaabou R, Ennahli S et al (2021) Improving the biocontrol potential of bacterial antagonists with salicylic acid against brown rot disease and impact on nectarine fruits quality. Agron 11(2):209

    CAS  Google Scholar 

  • Mae T (2004) Leaf senescence and nitrogen metabolism. In: Noodén LD (ed) Senescence and programmed cell death in plants. Academic Press, San Diego, pp 157–168

    Google Scholar 

  • Manghwar H, Hussain A, Ali Q, Liu F (2022) Brassinosteroids (BRs) role in plant development and coping with different stresses. Int J Mol Sci 23(3):1012

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez DE, Bartoli C, Grbic V, Guiamet JJ (2007) Vacuolar cysteine proteases of wheat (Triticum aestivum L.) are common to leaf senescence induced by different factors. J Exp Bot 58(5):1099–1107. https://doi.org/10.1093/jxb/erl270

    Article  PubMed  Google Scholar 

  • Martínez DE, Costa ML, Gomez FM, Otegui MS, Guiamet JJ (2008) ‘Senescence-associated vacuoles’ are involved in the degradation of chloroplast proteins in tobacco leaves. Plant J 56(2):196–206

    PubMed  Google Scholar 

  • Masood J, Zhu W, Fu Y, Li Z, Zhou Y, Zhang D et al (2023) Scaffold protein RACK1A positively regulates leaf senescence by coordinating the EIN3-miR164-ORE1 transcriptional cascade in Arabidopsis. J Integ Plant Biol. https://doi.org/10.1111/jipb.13483

    Article  Google Scholar 

  • Mattoo AK, Sobieszczuk-Nowicka E (2019) Polyamine as signaling molecules and leaf senescence. Senescence signaling and control in plants. Elsevier, Amsterdam, pp 125–138

    Google Scholar 

  • Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Curr Opin Plant Biol 8:409–414

    CAS  PubMed  Google Scholar 

  • Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126(5):969–980

    CAS  PubMed  Google Scholar 

  • Michaeli S, Galili G, Genschik P, Fernie AR, Avin-Wittenberg T (2016) Autophagy in plants-what’s new on the menu? Trends Plant Sci 21:134–144. https://doi.org/10.1016/j.tplants.2015.10.008

    Article  CAS  PubMed  Google Scholar 

  • Minina EA, Moschou PN, Vetukuri RR et al (2018) Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness. J Exp Bot 69(6):1415–1432

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mlynarova L, Nap JP, Bisseling T (2007) The SWI/SNF chromatin-remodeling gene AtCHR12 mediates temporary growth arrest in Arabidopsis thaliana upon perceiving environmental stress. Plant J 51:874–885

    CAS  PubMed  Google Scholar 

  • Mozgova I, Mikulski P, Pecinka A, Farrona S (2019) Epigenetic mechanisms of abiotic stress response and memory in plants. Epigenetics in plants of agronomic importance: fundamentals and applications. Springer, Berlin, pp 1–64

    Google Scholar 

  • Mustafavi SH, Badi HN, Sękara A, Mehrafarin A, Janda T, Ghorbanpour M, Rafiee H (2018) Polyamines and their possible mechanisms involved in plant physiological processes and elicitation of secondary metabolites. Acta Physiol Plant 40:1–19

    CAS  Google Scholar 

  • Nath K, Phee K, Jeong S, Lee SY, Tateno Y, Allakhverdiev SI, Lee CH, Nam HG (2013) Age-dependent changes in the functions and compositions of photosynthetic complexes in the thylakoid membranes of Arabidopsis thaliana. Photosynth Res 117:547–556

    CAS  PubMed  Google Scholar 

  • Niu F, Cui X, Zhao P, Sun M et al (2020) WRKY42 transcription factor positively regulates leaf senescence through modulating SA and ROS synthesis in Arabidopsis thaliana. The Plant J 104(1):171–184

    CAS  PubMed  Google Scholar 

  • Ostrowska-Mazurek A, Kasprzak P, Kubala S, Zaborowska M, Sobieszczuk-Nowicka E (2020) Epigenetic landmarks of leaf senescence and crop improvement. Int J Mol Sci 21(14):5125

    CAS  PubMed  PubMed Central  Google Scholar 

  • Otegui MS (2018) Vacuolar degradation of chloroplast components: autophagy and beyond. J Exp Bot 69:741–750

    CAS  PubMed  Google Scholar 

  • Park SH, Jeong JS, Seo JS, Park BS, Chua NH (2019) Arabidopsis ubiquitin-specific proteases UBP12 and UBP13 shape ORE1 levels during leaf senescence induced by nitrogen deficiency. New Phytol 223(3):1447–1460

    CAS  PubMed  Google Scholar 

  • Park SH, Jeong JS, Zhou Y, Mustafa NFB, Chua NH (2022) Deubiquitination of BES1 by UBP12/UBP13 promotes brassinosteroid signaling and plant growth. Plant Commun. https://doi.org/10.1016/j.xplc.2022.100348

    Article  PubMed  PubMed Central  Google Scholar 

  • Peerzada YY, Iqbal M (2021) Leaf senescence and ethylene signaling. Plant growth regulators: signaling under stress conditions. Springer, Berlin, pp 153–171

    Google Scholar 

  • Piao W, Kim SH, Lee BD, An G, Sakuraba Y, Paek NC (2019) Rice transcription factor OsMYB102 delays leaf senescence by down-regulating abscisic acid accumulation and signaling. J Exp Bot 70(10):2699–2715

    CAS  PubMed  PubMed Central  Google Scholar 

  • Poret M, Chandrasekard B, van der Hoorn RAL, Avice JC (2016) Characterization of senescence-associated protease activities involved in the efficient protein remobilization during leaf senescence of winter oilseed rape. Plant Sci 246:139–153. https://doi.org/10.1016/j.plantsci.2016.02.011

    Article  CAS  PubMed  Google Scholar 

  • Poret M, Chandrasekar B et al (2017) Proteomic investigations of proteases involved in cotyledon senescence: a model to explore the genotypic variability of proteolysis machinery associated with nitrogen remobilization efficiency during the leaf senescence of oilseed rape. Proteomes 5(4):29. https://doi.org/10.3390/proteomes5040029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi T, Wang J, Huang H, Liu B et al (2015) Regulation of jasmonate-induced leaf senescence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis. Plant Cell 27(6):1634–1649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qin J, Ma X, Yi Z, Tang Z, Meng Y (2016) A transcriptome-wide study on the micro RNA-and the Argonaute 1-enriched small RNA-mediated regulatory networks involved in plant leaf senescence. Plant Biol 18(2):197–205

    CAS  PubMed  Google Scholar 

  • Qiu K, Li Z, Yang Z, Chen J, Wu S, Zhu X, Gao S, Gao J, Ren G, Kuai B, Zhou X (2015) EIN3 and ORE1 accelerate degreening during ethylene-mediated leaf senescence by directly activating chlorophyll catabolic genes in Arabidopsis. PLoS Genet 11(7):e1005399

    PubMed  PubMed Central  Google Scholar 

  • Qu Y, Jiang L, Wuyun T, Mu S, Xie F, Chen Y, Zhang L (2020) Effects of exogenous putrescine on delaying senescence of cut foliage of Nephrolepis cordifolia. Front Plant Sci 11:566824

    PubMed  PubMed Central  Google Scholar 

  • Rai S, Sindhu V, Sarkar RK, Santhoshkumar G (2020) Role of polyamines in vegetable crop production: a review. J Pharm Phytochem 9:466–476

    CAS  Google Scholar 

  • Raines T, Shanks C, Cheng CY, McPherson D, Argueso CT, Kim HJ, Schaller GE (2016) The cytokinin response factors modulate root and shoot growth and promote leaf senescence in Arabidopsis. Plant J 85(1):134–147

    CAS  PubMed  Google Scholar 

  • Ren B, Zhang J, Dong S, Liu P, Zhao B (2018) Exogenous 6-benzyladenine improves antioxidative system and carbon metabolism of summer maize waterlogged in the field. J Agron and Crop Sci 204(2):175–184

    CAS  Google Scholar 

  • Richmond AE, Lang A (1957) Effect of kinetin on protein content and survival of detached Xanthium leaves. Sci 125(3249):650–651

    CAS  Google Scholar 

  • Richter R, Behringer C, Müller IK, Schwechheimer C (2010) The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes Dev 24(18):2093–2104

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuraba Y, Schelbert S, Park SY, Han SH et al (2012) STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24(2):507–518

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuraba Y, Han SH, Lee SH, Hörtensteiner S, Paek NC (2016) Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription. Plant Cell Rep 35(1):155–166

    CAS  PubMed  Google Scholar 

  • Sakuraba Y, Kim D, Han SH, Kim SH, Piao W, Yanagisawa S et al (2020) Multilayered regulation of membrane-bound ONAC054 is essential for abscisic acid-induced leaf senescence in rice. Plant Cell 32(3):630–649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sarwat M, Naqvi AR, Ahmad P, Ashraf M, Akram NA (2013) Phytohormones and microRNAs as sensors and regulators of leaf senescence: assigning macro roles to small molecules. Biotechnol Adv 31(8):1153–1171

    CAS  PubMed  Google Scholar 

  • Sasi JM, Gupta S, Singh A et al (2022) Know when and how to die: gaining insights into the molecular regulation of leaf senescence. Physiol Mol Biol Plants 28:1515–1534. https://doi.org/10.1007/s12298-022-01224-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schommer C, Palatnik JF, Aggarwal P, Chetelat A, Cubas P, Farmer EE, Nath U, Weigel D (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6:e230

    PubMed  PubMed Central  Google Scholar 

  • Selivankina SY, Karavaiko NN, Kuiper D, Novikova GV, Kulaeva ON (2001) Cytokinin activity of zeatin allylic phosphate, a natural compound. Plant Growth Regul 33:157–164

    CAS  Google Scholar 

  • Sequera-Mutiozabal MI, Erban A, Kopka J et al (2016) Global metabolic profiling of Arabidopsis polyamine oxidase 4 (AtPAO4) loss-of-function mutants exhibiting delayed dark-induced senescence. Front Plant Sci 7:173

    PubMed  PubMed Central  Google Scholar 

  • Shan X, Wang J, Chua L, Jiang D, Peng W, Xie D (2011) The role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant Physiol 155:751–764

    CAS  PubMed  Google Scholar 

  • Sharma S, Pareek S, Sagar NA, Valero D, Serrano M (2017) Modulatory effects of exogenously applied polyamines on postharvest physiology, antioxidant system and shelf life of fruits: a review. Int J Mol Sci 18(8):1789

    PubMed  PubMed Central  Google Scholar 

  • Shen Y, Lei T, Cui X, Liu X, Zhou S, Zheng Y et al (2019) Arabidopsis histone deacetylase HDA 15 directly represses plant response to elevated ambient temperature. Plant J 100(5):991–1006

    CAS  PubMed  Google Scholar 

  • Shi Q, Zhang H, Song X, Jiang YE, Liang R, Li G (2018) Functional characterization of the maize phytochrome-interacting factors PIF4 and PIF5. Front Plant Sci 8:2273

    PubMed  PubMed Central  Google Scholar 

  • Shin JH, Yoshimoto K, Ohsumi Y, Jeon JS, An G (2009) OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice. Mol Cells 27:67–74

    CAS  PubMed  Google Scholar 

  • Singh S, Singh M, Bisht S, Sharma JG (2022) Leaf senescence and its regulation with phytohormones and essential elements: an overview. J App Biol and Biotechnol 10(2):1–9

    Google Scholar 

  • Skutnik E, Rabiza-Świder J, Wachowicz M, Łukaszewska A (2004) Senescence of cut leaves of Zantedeschia aethiopica and Z. elliottiana. Part I. Chlorophyll degradation. Acta Sci Pol Hortorum Cultus 3(2):57–65

    Google Scholar 

  • Sobieszczuk-Nowicka E (2017) Polyamine catabolism adds fuel to leaf senescence. Amino Acids 49:49–56

    CAS  PubMed  Google Scholar 

  • Song Y, Xiang F, Zhang G, Miao Y, Miao C, Song CP (2016) Abscisic acid as an internal integrator of multiple physiological processes modulates leaf senescence onset in Arabidopsis thaliana. Front Plant Sci 7:181

    PubMed  PubMed Central  Google Scholar 

  • Song S, Huang H, Wang J, Liu B, Qi T, Xie D (2017) MYC5 is involved in jasmonate-regulated plant growth, leaf senescence and defence responses. Plant and Cell Physiol 58(10):1752–1763

    CAS  Google Scholar 

  • Spormann S, Soares C, Teixeira J, Fidalgo F (2021) Polyamines as key regulatory players in plants under metal stress—A way for an enhanced tolerance. Ann Appl Biol 178(2):209–226

    CAS  Google Scholar 

  • Su T, Li X, Yang M, Shao Q, Zhao Y, Ma C, Wang P (2020) Autophagy: an intracellular degradation pathway regulating plant survival and stress response. Front Plant Sci 11:164

    PubMed  PubMed Central  Google Scholar 

  • Sun D, Ji X, Jia Y, Huo D, Si S, Zeng L et al (2020a) LreEF1A4, a translation elongation factor from lilium regale, is pivotal for cucumber mosaic virus and tobacco rattle virus infections and tolerance to salt and drought. Int J Mol Sci 21:6. https://doi.org/10.3390/ijms21062083

    Article  CAS  Google Scholar 

  • Sun X, Li X, Zhu J et al (2020b) Polyamines and ethylene metabolism during cold acclimation in zoysiagrass (Zoysia japonica Steud.). Acta Physiol Plant 42(8):1–10

    Google Scholar 

  • Süssenbacher I, Menghini D, Scherzer G et al (2019) Cryptic chlorophyll breakdown in non-senescent green Arabidopsis thaliana leaves. Photosynth Res 142(1):69–85

    PubMed  Google Scholar 

  • Suzuki G, Lucob-Agustin N, Kashihara K, Fujii Y, Inukai Y, Gomi K (2021) Rice MEDIATOR25, OsMED25, is an essential subunit for jasmonate-mediated root development and OsMYC2-mediated leaf senescence. Plant Sci 306:110853

    CAS  PubMed  Google Scholar 

  • Takacs Z, Poór P, Szepesi Á, Tari I (2017) In vivo inhibition of polyamine oxidase by a spermine analogue, MDL-72527, in tomato exposed to sublethal and lethal salt stress. Funct Plant Biol 44(5):480–492

    CAS  PubMed  Google Scholar 

  • Takacs Z, Poór P, Tari I (2021) Interaction between polyamines and ethylene in the response to salicylic acid under normal photoperiod and prolonged darkness. Plant Physiol Biochem 167:470–480

    CAS  PubMed  Google Scholar 

  • Tan XL, Fan ZQ, Shan W, Yin XR, Kuang JF, Lu WJ, Chen JY (2018) Association of BrERF72 with methyl jasmonate-induced leaf senescence of Chinese flowering cabbage through activating JA biosynthesis-related genes. Hortic Res 5:22

    PubMed  PubMed Central  Google Scholar 

  • Tang S, Zhang H, Li L, Liu X, Chen L, Chen W, Ding Y (2018) Exogenous spermidine enhances the photosynthetic and antioxidant capacity of rice under heat stress during early grain-filling period. Funct Plant Biol 45(9):911–921

    CAS  PubMed  Google Scholar 

  • Ueda H, Kusaba M (2015) Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol 169(1):138–147

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Schippers JH (2019) The role and regulation of autophagy and the proteasome during aging and senescence in plants. Genes 10(4):267

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Sun X, Jia X, Ma F (2017) Apple autophagy-related protein MdATG3s afford tolerance to multiple abiotic stresses. Plant Sci 256:53–64

    CAS  PubMed  Google Scholar 

  • Wang M, Zhang T, Ding F (2019) Exogenous melatonin delays methyl jasmonate-Triggered senescence in tomato leaves. Agron 9(12):795

    Google Scholar 

  • Wang L, Xu Q, Yu H et al (2020) Strigolactone and karrikin signaling pathways elicit ubiquitination and proteolysis of SMXL2 to regulate hypocotyl elongation in Arabidopsis. Plant Cell 32:2251–2270

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Dai S, Zhang ZL, Lao W, Wang R, Meng X, Zhou X (2021) Ethylene and salicylic acid synergistically accelerate leaf senescence in Arabidopsis. J Integ Plant Biol 63(5):828–833

    CAS  Google Scholar 

  • Wang YQ, Song JN, Yang HB (2022) DNA methylation regulates the expression of salt tolerance gene FtNHX1 in Tartary buckwheat. Theor Exp Plant Physiol 34:185–195. https://doi.org/10.1007/s40626-022-00241-5

    Article  CAS  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111(6):1021–1058

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wen Z, Mei Y, Zhou J, Cui Y, Wang D, Wang NN (2020) SAUR49 can positively regulate leaf senescence by suppressing SSPP in Arabidopsis. Plant Cell Physiol 61(3):644–658

    CAS  PubMed  Google Scholar 

  • Woo HR, Kim JH, Nam HG, Lim PO (2004) The delayed leaf senescence mutants of Arabidopsis, ore1, ore3 and ore9 are tolerant to oxidative stress. Plant Cell Physiol 45(7):923–932

    CAS  PubMed  Google Scholar 

  • Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death – regulation by multiple layers of control and implications for aging in general. J Cell Sci 126(21):4823–4833

    CAS  PubMed  Google Scholar 

  • Woo HR, Masclaux-Daubresse C, Lim PO (2018) Plant senescence: how plants know when and how to die. J Exp Bot 69(4):715–718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Woo HR, Kim HJ, Lim PO, Nam HG (2019) Leaf senescence: systems and dynamics aspects. Ann Rev Plant Biol 70:347–376

    CAS  Google Scholar 

  • Wu K, Zhang L, Zhou C, Yu CW, Chaikam V (2008) HDA6 is required for jasmonate response, senescence and flowering in Arabidopsis. J Exp Bot 59:225–234

    CAS  PubMed  Google Scholar 

  • Wu X, Zhu Z, Li X, Zha D (2012a) Effects of cytokinin on photosynthetic gas exchange, chlorophyll fluorescence parameters and antioxidative system in seedlings of eggplant (Solanum melongena L.) under salinity stress. Acta Physiol Plant 34:2105–2114

    CAS  Google Scholar 

  • Wu XY, Kuai BK, Jing JJZ, HC, (2012b) Regulation of leaf senescence and crop genetic improvement F. J Integ Plant Biol 54(12):936–952

    CAS  Google Scholar 

  • Xiao S, Dai L, Liu F, Wang Z, Peng W, Xie D (2004) COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defence and senescence. Plant Cell 16:1132–1142

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao XO, Zeng YM, Cao BH, Lei JJ, Chen QH, Meng CM, Cheng YJ (2017) PSAG12-IPT overexpression in eggplant delays leaf senescence and induces abiotic stress tolerance. J Horticul Sci Biotech 92(4):349–357

    CAS  Google Scholar 

  • Xu F, Meng T, Li P, Yu Y, Cui Y, Wang Y et al (2011a) A Soybean dual-specificity kinase, GmSARK, and its Arabidopsis homolog, AtSARK, regulate leaf senescence through synergistic actions of auxin and ethylene. Plant Physiol 157(4):2131–2153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu L, Xing S, Sun X (2014) Effects of polyamines on hormones contents and the relationship with the flower bud differentiation in chrysanthemum. Plant Physiol J 50:1195–1202

    CAS  Google Scholar 

  • Xu YM, Xiao XM, Zeng ZX, Tan XL et al (2019) BrTCP7 transcription factor is associated with MeJA-promoted leaf senescence by activating the expression of BrOPR3 and BrRCCR. Int J Mol Sci 20(16):3963

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada Y, Umehara M (2015) Possible roles of strigolactones during leaf senescence. Plants 4(3):664–677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240:399–408

    CAS  PubMed  Google Scholar 

  • Yan H, Saika H, Maekawa M, Takamure I, Tsutsumi N, Kyozuka J, Nakazono M (2007) Rice tillering dwarf mutant dwarf3 has increased leaf longevity during darkness-induced senescence or hydrogen peroxide-induced cell death. Genes Genet Syst 82:361–366

    CAS  PubMed  Google Scholar 

  • Yan H, Liu Y, Zhang K, Song J, Xu W, Su Z (2019) Chromatin state-based analysis of epigenetic H3K4me3 marks of Arabidopsis in response to dark stress. Front Genet 10:306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SD, Seo PJ, Yoon HK, Park CM (2011) The Arabidopsis NAC transcription factor VNI2 integrates abscisic acid signals into leaf senescence via the COR/RD genes. Plant Cell 23:2155–2168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Worley E, Udvardi M (2014) A NAP-AAO3 regulatory module promotes chlorophyll degradation via ABA biosynthesis in Arabidopsis leaves. Plant Cell 26:4862–4874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang DQ, Luo YL, Dong WH, Yin YP, Li Y, Wang ZL (2018) Response of photosystem II performance and antioxidant enzyme activities in stay-green wheat to cytokinin. Photosynthetica 56(2):567–577

    CAS  Google Scholar 

  • Yang T, Zhang M, Yang Q, Liu K, Cui J, Chen J et al (2022) The S40 family members delay leaf senescence by promoting cytokinin synthesis. Plant Physiol Biochem 191:99–109

    CAS  PubMed  Google Scholar 

  • Yin W, Dong N, Niu M, Zhang X et al (2019) Brassinosteroid-regulated plant growth and development and gene expression in soybean. The Crop J 7(3):411–418

    Google Scholar 

  • Yin R, Liu X, Yu J, Ji Y, Liu J, Cheng L, Zhou J (2020) Up-regulation of autophagy by low concentration of salicylic acid delays methyl jasmonate-induced leaf senescence. Sci Rep 10(1):11472

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoneyama K, Brewer PB (2021) Strigolactones, how are they synthesized to regulate plant growth and development? Curr Opin Plant Biol 63:102072

    CAS  PubMed  Google Scholar 

  • Yu K, Wang Y, Wei J, Ma Q, Yu D, Li J (2009) Improving rhizome yield and quality of Paris polyphylla through gibberellic acid-induced retardation of senescence of aerial parts. Plant Signal Behav 4(5):413–415

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Qi Y, Xu J, Dai X, Chen J, Dong CH, Xiang F (2021) Arabidopsis WRKY71 regulates ethylene-mediated leaf senescence by directly activating EIN2, ORE1 and ACS2 genes. Plant J 107(6):1819–1836

    CAS  PubMed  Google Scholar 

  • Zavaleta-Mancera HA, López-Delgado H, Loza-Tavera H et al (2007) Cytokinin promotes catalase and ascorbate peroxidase activities and preserves the chloroplast integrity during dark-senescence. J Plant Physiol 164:1572–1582

    CAS  PubMed  Google Scholar 

  • Zeng ZX, Wang CM, Zhao YT et al (2022) Molecular characterization of leaf senescence-associated autophagy genes in postharvest Chinese flowering cabbage and identifying their transcriptional activator BrMYB108. Postharvest Biol Technol 185:111785

    CAS  Google Scholar 

  • Zhang K, Gan SS (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158(2):961–969

    CAS  PubMed  Google Scholar 

  • Zhang H, Zhou C (2013) Signal transduction in leaf senescence. Plant Mol Biol 82:539–545

    CAS  PubMed  Google Scholar 

  • Zhang X, Ju HW, Chung MS, Huang P, Ahn SJ, Kim CS (2011) The R-R-type MYB-like transcription factor, AtMYBL, is involved in promoting leaf senescence and modulates an abiotic stress response in Arabidopsis. Plant Cell Physiol 52(1):138–148

    CAS  PubMed  Google Scholar 

  • Zhang K, Halitschke R, Yin C, Liu CJ, Gan SS (2013) Salicylic acid 3-hydroxylase regulates Arabidopsis leaf longevity by mediating salicylic acid catabolism. Proc Natl Acad Sci USA 114:E426–E435

    Google Scholar 

  • Zhang S, Li C, Wang R et al (2017a) The Arabidopsis mitochondrial protease FtSH4 is involved in leaf senescence via regulation of WRKY-dependent salicylic acid accumulation and signaling. Plant Physiol 173(4):2294–2307

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Xu X, Zhang Z, Jiang G, Feng L, Duan X, Jiang Y (2018a) Benzylaminopurine improves the quality of harvested litchi fruit. Postharvest Biol Technol 143:137–142

    CAS  Google Scholar 

  • Zhang Y, Li Z, Li YP, Zhang XQ et al (2018b) Chitosan and spermine enhance drought resistance in white clover, associated with changes in endogenous phytohormones and polyamines and antioxidant metabolism. Func Plant Biol 45(12):1205–1222

    CAS  Google Scholar 

  • Zhang Y, Wang HL, Li Z, Guo H (2020) Genetic network between leaf senescence and plant immunity: crucial regulatory nodes and new insights. Plants 9(4):495

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Zhu Z, Gao J, Zhou X et al (2021a) The NPR1-WRKY46-WRKY6 signaling cascade mediates probenazole/salicylic acid-elicited leaf senescence in Arabidopsis thaliana. J Integ Plant Biol 63(5):924–936

    CAS  Google Scholar 

  • Zhang H, Zhang L, Wu S, Chen Y, Yu D, Chen L (2021b) AtWRKY75 positively regulates age-triggered leaf senescence through gibberellin pathway. Plant Diversity 43(4):331–340

    CAS  PubMed  Google Scholar 

  • Zhang J, Zhang Y, Khan R, Wu X et al (2021c) Exogenous application of brassinosteroids regulates tobacco leaf size and expansion via modulation of endogenous hormones content and gene expression. Physiol Mol Biol Plants 27:847–860

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Peng K, Cui F, Wang D, Zhao J, Zhang Y et al (2021d) Cytokinin oxidase/dehydrogenase OsCKX11 coordinates source and sink relationship in rice by simultaneous regulation of leaf senescence and grain number. Plant Biotech J 19(2):335–350

    CAS  Google Scholar 

  • Zhang Y, Tan S, Gao Y, Kan C, Wang HL, Yang Q et al (2022) CLE42 delays leaf senescence by antagonizing ethylene pathway in Arabidopsis. New Phytol 235(2):550–562

    CAS  PubMed  Google Scholar 

  • Zhao XY, Wang JG, Song SJ, Wang Q, Kang H, Zhang Y, Li S (2016) Precocious leaf senescence by functional loss of PROTEIN S-ACYL TRANSFERASE14 involves the NPR1-dependent salicylic acid signaling. Sci Rep 6(1):20309

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Zhang W, Song Q, Xuan Y, Li K, Cheng L et al (2020) A WRKY transcription factor, TaWRKY40-D, promotes leaf senescence associated with jasmonic acid and abscisic acid pathways in wheat. Plant Biol 22(6):1072–1085

    CAS  PubMed  Google Scholar 

  • Zhao H, Yin CC, Ma B, Chen SY, Zhang JS (2021a) Ethylene signaling in rice and Arabidopsis: new regulators and mechanisms. J Integrative Plant Biol 63(1):102–125

    CAS  Google Scholar 

  • Zhao YQ, Zhang ZW, Chen YE, Ding CB, Yuan S, Reiter RJ, Yuan M (2021b) Melatonin: a potential agent in delaying leaf senescence. Crit Rev Plant Sci 40(1):1–22

    CAS  Google Scholar 

  • Zhu Z, Li G, Yan C, Liu L, Zhang Q, Han Z, Li B (2019) DRL1, encoding a NAC transcription factor, is involved in leaf senescence in grapevine. Int J Mol Sci 20(11):2678

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuang XH, Chung KP, Cui Y, Lin WL, Gao CJ, Kang BH, Jiang LW (2017) ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis. Proc Natl Acad Sci USA 114:E426–E435

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuo M, Sakuraba Y, Yanagisawa S (2020) A jasmonate-activated MYC2–Dof2. 1–MYC2 transcriptional loop promotes leaf senescence in Arabidopsis. Plant Cell 32(1):242–262

    CAS  PubMed  Google Scholar 

  • Zwack PJ, Rashotte AM (2013) Cytokinin inhibition of leaf senescence. Plant Signal Behav 8(7):e24737

    PubMed  PubMed Central  Google Scholar 

  • Zwack PJ, Robinson BR, Risley MG, Rashotte AM (2013) Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to cytokinin and numerous abiotic stresses. Plant Cell Physiol 54(6):971–981

    CAS  PubMed  Google Scholar 

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Altaf, F., Parveen, S., Farooq, S. et al. Enigmas of senescence: a reappraisal on the hormonal crosstalk and the molecular mechanisms. Theor. Exp. Plant Physiol. 36, 51–81 (2024). https://doi.org/10.1007/s40626-024-00308-5

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