Leaf Senescence: The Chloroplast Connection Comes of Age
Abstract
:1. Introduction
2. Leaf Senescence Is Modulated by Multiple Inputs
3. Senescence and Cell Death
4. Senescence and Chloroplasts
5. Degradation of Chloroplast Components in Senescing Leaves Provides Most of the Nitrogen Required for Reproductive Development
6. Senescence in Nonphotosynthetic Plant Organs
7. Redox Signaling and the Chloroplast Connection
8. Concluding Remarks
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Gregersen, P.L.; Culetic, A.; Boschian, L.; Krupinska, K. Plant senescence and crop productivity. Plant Mol. Biol. 2013, 82, 603–622. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Zhou, C. Signal transduction in leaf senescence. Plant Mol. Biol. 2013, 82, 539–545. [Google Scholar] [CrossRef] [PubMed]
- Schippers, J.H.; Schmidt, R.; Wagstaff, C.; Jing, H.-C. Living to die and dying to live: The survival strategy behind leaf senescence. Plant Physiol. 2015, 169, 914–930. [Google Scholar] [CrossRef] [PubMed]
- Tamary, E.; Nevo, R.; Naveh, L.; Levin-Zaidman, S.; Kiss, V.; Savidor, A.; Levin, Y.; Eyal, Y.; Reich, Z.; Adam, Z. Chlorophyll catabolism precedes changes in chloroplast structure and proteome during leaf senescence. Plant Direct 2019, 3, 1–18. [Google Scholar] [CrossRef] [PubMed]
- Hörtensteiner, S.; Kräutler, B. Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 2011, 1807, 977–988. [Google Scholar] [CrossRef] [PubMed]
- Woo, H.R.; Kim, H.J.; Lim, P.O.; Nam, H.G. Leaf senescence: Systems and dynamics aspects. Annu. Rev. Plant Biol. 2019, 70, 347–376. [Google Scholar] [CrossRef] [PubMed]
- Thomas, H. Senescence, ageing and death of the whole plant. New Phytol. 2013, 197, 696–711. [Google Scholar] [CrossRef] [PubMed]
- Buet, A.; Costa, M.L.; Martínez, D.E.; Guiamet, J.J. Chloroplast protein degradation in senescing leaves: Proteases and lytic compartments. Front. Plant Sci. 2019, 10, 747. [Google Scholar] [CrossRef] [PubMed]
- Uzelac, B.; Janošević, D.; Simonović, A.; Motyka, V.; Dobrev, P.I.; Budimir, S. Characterization of natural leaf senescence in tobacco (Nicotiana tabacum) plants grown in vitro. Protoplasma 2016, 253, 259–275. [Google Scholar] [CrossRef] [PubMed]
- Zentgraf, U. Tug-of-war during senescence. Nat. Plants 2019, 5, 129–130. [Google Scholar] [CrossRef] [PubMed]
- Thomas, H.; Ougham, H.; Canter, P.; Donnison, I. What stay-green mutants tell us about nitrogen remobilization in leaf senescence. J. Exp. Bot. 2002, 53, 801–808. [Google Scholar] [CrossRef] [PubMed]
- Ramkumar, M.; Senthil Kumar, S.; Gaikwad, K.; Pandey, R.; Chinnusamy, V.; Singh, N.K.; Singh, A.K.; Mohapatra, T.; Sevanthi, A.M. A novel stay-green mutant of rice with delayed leaf senescence and better harvest index confers drought tolerance. Plants 2019, 8, 375. [Google Scholar] [CrossRef] [PubMed]
- Sekhon, R.S.; Saski, C.; Kumar, R.; Flinn, B.S.; Luo, F.; Beissinger, T.M.; Ackerman, A.J.; Breitzman, M.W.; Bridges, W.C.; de Leon, N. Integrated genome-scale analysis identifies novel genes and networks underlying senescence in maize. Plant Cell 2019, 31, 1968–1989. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Huang, R. Modulation of ethylene and ascorbic acid on reactive oxygen species scavenging in plant salt response. Front. Plant Sci. 2019, 10, 319. [Google Scholar] [CrossRef] [PubMed]
- Thomas, H.; Howarth, C.J. Five ways to stay green. J. Exp. Bot. 2000, 51, 329–337. [Google Scholar] [CrossRef] [PubMed]
- Thomas, H.; Ougham, H. The stay-green trait. J. Exp. Bot. 2014, 65, 3889–3900. [Google Scholar] [CrossRef] [PubMed]
- Myers, J.R.; Aljadi, M.; Brewer, L. The importance of cosmetic stay-green in specialty crops. In Plant Breeding Reviews; Goldman, I., Ed.; John Wiley & Sons, Inc.: Hoboken, NJ, USA, 2018; Volume 42, pp. 219–256. [Google Scholar]
- Jibran, R.; Hunter, D.A.; Dijkwel, P.P. Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol. Biol. 2013, 82, 547–561. [Google Scholar] [CrossRef] [PubMed]
- Ay, N.; Janack, B.; Humbeck, K. Epigenetic control of plant senescence and linked processes. J. Exp. Bot. 2014, 65, 3875–3887. [Google Scholar] [CrossRef] [PubMed]
- Häffner, E.; Konietzki, S.; Diederichsen, E. Keeping control: The role of senescence and development in plant pathogenesis and defense. Plants 2015, 4, 449–488. [Google Scholar] [CrossRef] [PubMed]
- Bhattacharjee, S. ROS in aging and senescence. In Reactive Oxygen Species in Plant Biology; Springer: New Delhi, India, 2019; pp. 65–79. [Google Scholar]
- Shi, X.; Xu, S.; Mu, D.; Sadeghnezhad, E.; Li, Q.; Ma, Z.; Zhao, L.; Zhang, Q.; Wang, L. Exogenous melatonin delays dark-induced grape leaf senescence by regulation of antioxidant system and senescence associated genes (SAGs). Plants 2019, 8, 366. [Google Scholar] [CrossRef] [PubMed]
- Sade, N.; del Mar Rubio-Wilhelmi, M.; Umnajkitikorn, K.; Blumwald, E. Stress-induced senescence and plant tolerance to abiotic stress. J. Exp. Bot. 2017, 69, 845–853. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.; Zhang, W.; Zheng, N.; Zhai, W.; Qi, F. Study of cotton leaf senescence induced by Alternaria alternata infection. In Plant Senescence, Methods in Molecular Biology; Guo, Y., Ed.; Humana Press: New York, NY, USA, 2018; Volume 1744, pp. 161–171. [Google Scholar]
- Wu, A.; Allu, A.D.; Garapati, P.; Siddiqui, H.; Dortay, H.; Zanor, M.-I.; Asensi-Fabado, M.A.; Munné-Bosch, S.; Antonio, C.; Tohge, T. JUNGBRUNNEN1, a reactive oxygen species–responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 2012, 24, 482–506. [Google Scholar] [CrossRef] [PubMed]
- Xie, Y.; Huhn, K.; Brandt, R.; Potschin, M.; Bieker, S.; Straub, D.; Doll, J.; Drechsler, T.; Zentgraf, U.; Wenkel, S. REVOLUTA and WRKY53 connect early and late leaf development in Arabidopsis. Development 2014, 141, 4772–4783. [Google Scholar] [CrossRef] [PubMed]
- Biswas, M.S.; Mano, J.I. Lipid peroxide-derived short-chain carbonyls mediate hydrogen peroxide-induced and salt-induced programmed cell death in plants. Plant Physiol. 2015, 168, 885–898. [Google Scholar] [CrossRef] [PubMed]
- Garapati, P.; Xue, G.-P.; Munné-Bosch, S.; Balazadeh, S. Transcription factor ATAF1 in Arabidopsis promotes senescence by direct regulation of key chloroplast maintenance and senescence transcriptional cascades. Plant Physiol. 2015, 168, 1122–1139. [Google Scholar] [CrossRef] [PubMed]
- Circu, M.L.; Aw, T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48, 749–762. [Google Scholar] [CrossRef] [PubMed]
- Rogers, H.; Munné-Bosch, S. Production and scavenging of reactive oxygen species and redox signaling during leaf and flower senescence: Similar but different. Plant Physiol. 2016, 171, 1560–1568. [Google Scholar] [CrossRef] [PubMed]
- Muñoz, P.; Munné-Bosch, S. Photo-oxidative stress during leaf, flower and fruit development. Plant Physiol. 2018, 176, 1004–1014. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Blumwald, E. Stress-induced chloroplast degradation in Arabidopsis is regulated via a process independent of autophagy and senescence-associated vacuoles. Plant Cell 2014, 26, 4875–4888. [Google Scholar] [CrossRef] [PubMed]
- Noctor, G.; Foyer, C.H. Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol. 2016, 171, 1581–1592. [Google Scholar] [CrossRef] [PubMed]
- Penfold, C.A.; Buchanan-Wollaston, V. Modelling transcriptional networks in leaf senescence. J. Exp. Bot. 2014, 65, 3859–3873. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Antonietta, M.; Acciaresi, H.; Guiamet, J. Responses to N deficiency in stay green and non-stay green argentinean hybrids of maize. J. Agron. Crop Sci. 2016, 202, 231–242. [Google Scholar] [CrossRef]
- Moschen, S.; Higgins, J.; Di Rienzo, J.A.; Heinz, R.A.; Paniego, N.; Fernández, P. Network and biosignature analysis for the integration of transcriptomic and metabolomic data to characterize leaf senescence process in sunflower. BMC Bioinform. 2016, 17, 174. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jan, S.; Abbas, N.; Ashraf, M.; Ahmad, P. Roles of potential plant hormones and transcription factors in controlling leaf senescence and drought tolerance. Protoplasma 2019, 256, 313–329. [Google Scholar] [CrossRef] [PubMed]
- Talla, S.K.; Panigrahy, M.; Kappara, S.; Nirosha, P.; Neelamraju, S.; Ramanan, R. Cytokinin delays dark-induced senescence in rice by maintaining the chlorophyll cycle and photosynthetic complexes. J. Exp. Bot. 2016, 67, 1839–1851. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, G.; Casaretto, J.A.; Ying, S.; Mahmood, K.; Liu, F.; Bi, Y.-M.; Rothstein, S.J. Overexpression of OsGATA12 regulates chlorophyll content, delays plant senescence and improves rice yield under high density planting. Plant Mol. Biol. 2017, 94, 215–227. [Google Scholar] [CrossRef] [PubMed]
- Mueller-Roeber, B.; Balazadeh, S. Auxin and its role in plant senescence. J. Plant Growth Regul. 2014, 33, 21–33. [Google Scholar] [CrossRef]
- Kim, J.I.; Murphy, A.S.; Baek, D.; Lee, S.-W.; Yun, D.-J.; Bressan, R.A.; Narasimhan, M.L. YUCCA6 over-expression demonstrates auxin function in delaying leaf senescence in Arabidopsis thaliana. J. Exp. Bot. 2011, 62, 3981–3992. [Google Scholar] [CrossRef] [PubMed]
- van der Graaff, E.; Schwacke, R.; Schneider, A.; Desimone, M.; Flügge, U.-I.; Kunze, R. Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol. 2006, 141, 776–792. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yu, K.; Wei, J.; Ma, Q.; Yu, D.; Li, J. Senescence of aerial parts is impeded by exogenous gibberellic acid in herbaceous perennial Paris polyphylla. J. Plant Physiol. 2009, 166, 819–830. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.; Chang, C.; Tucker, M.L. To grow old: Regulatory role of ethylene and jasmonic acid in senescence. Front. Plant Sci. 2015, 6, 20. [Google Scholar] [CrossRef] [PubMed]
- Schommer, C.; Palatnik, J.F.; Aggarwal, P.; Chételat, A.; Cubas, P.; Farmer, E.E.; Nath, U.; Weigel, D. Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol. 2008, 6, e230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- He, Y.; Gan, S. A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. Plant Cell 2002, 14, 805–815. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merewitz, E.B.; Gianfagna, T.; Huang, B. Photosynthesis, water use, and root viability under water stress as affected by expression of SAG12-ipt controlling cytokinin synthesis in Agrostis stolonifera. J. Exp. Bot. 2011, 62, 383–395. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Merewitz, E.; Xu, Y.; Huang, B. Differentially expressed genes associated with improved drought tolerance in creeping bentgrass overexpressing a gene for cytokinin biosynthesis. PLoS ONE 2016, 11, e0166676. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Song, Y.; Yang, C.; Gao, S.; Zhang, W.; Li, L.; Kuai, B. Age-triggered and dark-induced leaf senescence require the bHLH transcription factors PIF3, 4, and 5. Mol. Plant 2014, 7, 1776–1787. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosenwasser, S.; Belausov, E.; Riov, J.; Holdengreber, V.; Friedman, H. Gibberellic acid (GA3) inhibits ROS increase in chloroplasts during dark-induced senescence of pelargonium cuttings. J. Plant Growth Regul. 2010, 29, 375–384. [Google Scholar] [CrossRef]
- Jajic, I.; Sarna, T.; Strzalka, K. Senescence, stress, and reactive oxygen species. Plants 2015, 4, 393–411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guo, P.; Li, Z.; Huang, P.; Li, B.; Fang, S.; Chu, J.; Guo, H. A tripartite amplification loop involving the transcription factor WRKY75, salicylic acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 2017, 29, 2854–2870. [Google Scholar] [CrossRef] [PubMed]
- El-Showk, S.; Ruonala, R.; Helariutta, Y. Crossing paths: Cytokinin signalling and crosstalk. Development 2013, 140, 1373–1383. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, J.; Chen, L.; Sun, H.; Wusiman, N.; Sun, W.; Li, B.; Gao, Y.; Kong, J.; Zhang, D.; Zhang, X. Crosstalk between cytokinin and ethylene signaling pathways regulates leaf abscission in cotton in response to chemical defoliants. J. Exp. Bot. 2019, 70, 1525–1538. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gepstein, S.; Glick, B.R. Strategies to ameliorate abiotic stress-induced plant senescence. Plant Mol. Biol. 2013, 82, 623–633. [Google Scholar] [CrossRef] [PubMed]
- Senthil-Kumar, M.; Mysore, K.S. Nonhost resistance against bacterial pathogens: Retrospectives and prospects. Annu. Rev. Phytopathol. 2013, 51, 407–427. [Google Scholar] [CrossRef] [PubMed]
- Rossi, F.R.; Krapp, A.R.; Bisaro, F.; Maiale, S.J.; Pieckenstain, F.L.; Carrillo, N. Reactive oxygen species generated in chloroplasts contribute to tobacco leaf infection by the necrotrophic fungus Botrytis cinerea. Plant J. 2017, 92, 761–773. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pierella Karlusich, J.J.; Zurbriggen, M.D.; Shahinnia, F.; Sonnewald, S.; Sonnewald, U.; Hosseini, S.A.; Hajirezaei, M.-R.; Carrillo, N. Chloroplast redox status modulates genome-wide plant responses during the non-host interaction of tobacco with the hemibiotrophic bacterium Xanthomonas campestris pv. vesicatoria. Front. Plant Sci. 2017, 8, 1158. [Google Scholar] [CrossRef] [PubMed]
- Petrov, V.; Hille, J.; Mueller-Roeber, B.; Gechev, T.S. ROS-mediated abiotic stress-induced programmed cell death in plants. Front. Plant Sci. 2015, 6, 69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- You, J.; Chan, Z. ROS regulation during abiotic stress responses in crop plants. Front. Plant Sci. 2015, 6, 1092. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jwa, N.-S.; Hwang, B.K. Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Front. Plant Sci. 2017, 8, 1687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suzuki, N.; Katano, K. Coordination between ROS regulatory systems and other pathways under heat stress and pathogen attack. Front. Plant Sci. 2018, 9, 490. [Google Scholar] [CrossRef] [PubMed]
- Su, J.; Yang, L.; Zhu, Q.; Wu, H.; He, Y.; Liu, Y.; Xu, J.; Jiang, D.; Zhang, S. Active photosynthetic inhibition mediated by MPK3/MPK6 is critical to effector-triggered immunity. PLoS Biol. 2018, 16, e2004122. [Google Scholar] [CrossRef] [PubMed]
- Kozuleva, M.A.; Ivanov, B.N. The mechanisms of oxygen reduction in the terminal reducing segment of the chloroplast photosynthetic electron transport chain. Plant Cell Physiol. 2016, 57, 1397–1404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pospíšil, P. Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Front. Plant Sci. 2016, 7, 1950. [Google Scholar] [CrossRef] [PubMed]
- Das, K.; Roychoudhury, A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2014, 2, 53. [Google Scholar] [CrossRef] [Green Version]
- Mignolet-Spruyt, L.; Xu, E.; Idänheimo, N.; Hoeberichts, F.A.; Mühlenbock, P.; Brosché, M.; Van Breusegem, F.; Kangasjärvi, J. Spreading the news: Subcellular and organellar reactive oxygen species production and signalling. J. Exp. Bot. 2016, 67, 3831–3844. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sewelam, N.; Kazan, K.; Schenk, P.M. Global plant stress signaling: Reactive oxygen species at the cross-road. Front. Plant Sci. 2016, 7, 187. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ambastha, V.; Tripathy, B.C.; Tiwari, B.S. Programmed cell death in plants: A chloroplastic connection. Plant Signal. Behav. 2015, 10, e989752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mur, L.A.; Aubry, S.; Mondhe, M.; Kingston-Smith, A.; Gallagher, J.; Timms-Taravella, E.; James, C.; Papp, I.; Hörtensteiner, S.; Thomas, H. Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol. 2010, 188, 161–174. [Google Scholar] [CrossRef] [PubMed]
- Samuilov, V.D.; Lagunova, E.M.; Kiselevsky, D.B.; Dzyubinskaya, E.V.; Makarova, Y.V.; Gusev, M.V. Participation of chloroplasts in plant apoptosis. Biosci. Rep. 2003, 23, 103–117. [Google Scholar] [CrossRef] [PubMed]
- Doyle, S.M.; Diamond, M.; McCabe, P.F. Chloroplast and reactive oxygen species involvement in apoptotic-like programmed cell death in Arabidopsis suspension cultures. J. Exp. Bot. 2009, 61, 473–482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Q.-L.; Chen, J.-H.; He, N.-Y.; Guo, F.-Q. Metabolic reprogramming in chloroplasts under heat stress in plants. Int. J. Mol. Sci. 2018, 19, 849. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, K.P.; Kim, C.; Landgraf, F.; Apel, K. EXECUTER1-and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2007, 104, 10270–10275. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karpinski, S.; Gabrys, H.; Mateo, A.; Karpinska, B.; Mullineaux, P.M. Light perception in plant disease defence signalling. Curr. Opin. Plant Biol. 2003, 6, 390–396. [Google Scholar] [CrossRef]
- Liu, Y.; Ren, D.; Pike, S.; Pallardy, S.; Gassmann, W.; Zhang, S. Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J. 2007, 51, 941–954. [Google Scholar] [CrossRef] [PubMed]
- Zurbriggen, M.D.; Carrillo, N.; Tognetti, V.B.; Melzer, M.; Peisker, M.; Hause, B.; Hajirezaei, M.-R. Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria. Plant J. 2009, 60, 962–973. [Google Scholar] [CrossRef] [PubMed]
- Van Aken, O.; Van Breusegem, F. Licensed to kill: Mitochondria, chloroplasts, and cell death. Trends Plant Sci. 2015, 20, 754–766. [Google Scholar] [CrossRef] [PubMed]
- Gutiérrez, J.; González-Pérez, S.; García-García, F.; Daly, C.T.; Lorenzo, Ó.; Revuelta, J.L.; McCabe, P.F.; Arellano, J.B. Programmed cell death activated by Rose Bengal in Arabidopsis thaliana cell suspension cultures requires functional chloroplasts. J. Exp. Bot. 2014, 65, 3081–3095. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, C.; Meskauskiene, R.; Zhang, S.; Lee, K.P.; Ashok, M.L.; Blajecka, K.; Herrfurth, C.; Feussner, I.; Apel, K. Chloroplasts of Arabidopsis are the source and a primary target of a plant-specific programmed cell death signaling pathway. Plant Cell 2012, 24, 3026–3039. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zapata, J.; Guera, A.; Esteban-Carrasco, A.; Martin, M.; Sabater, B. Chloroplasts regulate leaf senescence: Delayed senescence in transgenic ndhF-defective tobacco. Cell Death Differ. 2005, 12, 1277–1284. [Google Scholar] [CrossRef] [PubMed]
- Shikanai, T.; Endo, T.; Hashimoto, T.; Yamada, Y.; Asada, K.; Yokota, A. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl. Acad. Sci. USA 1998, 95, 9705–9709. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnson, G.N. Physiology of PSI cyclic electron transport in higher plants. Biochim. Biophys. Acta 2011, 1807, 384–389. [Google Scholar] [CrossRef] [PubMed]
- Murphy, M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2008, 417, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Krieger-Liszkay, A.; Krupinska, K.; Shimakawa, G. The impact of photosynthesis on initiation of leaf senescence. Physiol. Plant. 2019, 166, 148–164. [Google Scholar] [CrossRef] [PubMed]
- Abbasi, A.R.; Saur, A.; Hennig, P.; Tschiersch, H.; Hajirezaei, M.; Hofius, D.; Sonnewald, U.; Voll, L.M. Tocopherol deficiency in transgenic tobacco (Nicotiana tabacum L.) plants leads to accelerated senescence. Plant Cell Environ. 2009, 32, 144–157. [Google Scholar] [CrossRef] [PubMed]
- Gou, J.-Y.; Li, K.; Wu, K.; Wang, X.; Lin, H.; Cantu, D.; Uauy, C.; Dobon-Alonso, A.; Midorikawa, T.; Inoue, K. Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. Plant Cell 2015, 27, 1755–1770. [Google Scholar] [CrossRef] [PubMed]
- Van Buer, J.; Prescher, A.; Baier, M. Cold-priming of chloroplast ROS signalling is developmentally regulated and is locally controlled at the thylakoid membrane. Sci. Rep. 2019, 9, 3022. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Gallie, D.R. Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol. 2006, 142, 775–787. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barth, C.; Moeder, W.; Klessig, D.F.; Conklin, P.L. The timing of senescence and response to pathogens is altered in the ascorbate-deficient Arabidopsis mutant vitamin c-1. Plant Physiol. 2004, 134, 1784–1792. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kotchoni, S.O.; Larrimore, K.E.; Mukherjee, M.; Kempinski, C.F.; Barth, C. Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. Plant Physiol. 2009, 149, 803–815. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ding, S.; Wang, L.; Yang, Z.; Lu, Q.; Wen, X.; Lu, C. Decreased glutathione reductase2 leads to early leaf senescence in Arabidopsis. J. Integr. Plant Biol. 2016, 58, 29–47. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schöttler, M.A.; Tóth, S.Z. Photosynthetic complex stoichiometry dynamics in higher plants: Environmental acclimation and photosynthetic flux control. Front. Plant Sci. 2014, 5, 188. [Google Scholar] [PubMed]
- Gómez, R.; Vicino, P.; Carrillo, N.; Lodeyro, A.F. Manipulation of oxidative stress responses as a strategy to generate stress-tolerant crops. From damage to signaling to tolerance. Crit. Rev. Biotechnol. 2019, 39, 693–708. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Leister, D.; Bolle, C. Photosynthetic lesions can trigger accelerated senescence in Arabidopsis thaliana. J. Exp. Bot. 2015, 66, 6891–6903. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Szechyńska-Hebda, M.; Karpiński, S. Light intensity-dependent retrograde signalling in higher plants. J. Plant Physiol. 2013, 170, 1501–1516. [Google Scholar] [CrossRef] [PubMed]
- Mayta, M.L.; Lodeyro, A.F.; Guiamet, J.J.; Tognetti, V.B.; Melzer, M.; Hajirezaei, M.-R.; Carrillo, N. Expression of a plastid-targeted flavodoxin decreases chloroplast reactive oxygen species accumulation and delays senescence in aging tobacco leaves. Front. Plant Sci. 2018, 9, 1039. [Google Scholar] [CrossRef] [PubMed]
- Pierella Karlusich, J.J.; Lodeyro, A.F.; Carrillo, N. The long goodbye: The rise and fall of flavodoxin during plant evolution. J. Exp. Bot. 2014, 65, 5161–5178. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pierella Karlusich, J.J.; Ceccoli, R.D.; Graña, M.; Romero, H.; Carrillo, N. Environmental selection pressures related to iron utilization are involved in the loss of the flavodoxin gene from the plant genome. Genome Biol. Evol. 2015, 7, 750–767. [Google Scholar] [CrossRef] [PubMed]
- Tognetti, V.B.; Palatnik, J.F.; Fillat, M.F.; Melzer, M.; Hajirezaei, M.-R.; Valle, E.M.; Carrillo, N. Functional replacement of ferredoxin by a cyanobacterial flavodoxin in tobacco confers broad-range stress tolerance. Plant Cell 2006, 18, 2035–2050. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- John, I.; Hackett, R.; Cooper, W.; Drake, R.; Farrell, A.; Grierson, D. Cloning and characterization of tomato leaf senescence-related cDNAs. Plant Mol. Biol. 1997, 33, 641–651. [Google Scholar] [CrossRef] [PubMed]
- Fuchs, Y.; Steller, H. Programmed cell death in animal development and disease. Cell 2011, 147, 742–758. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peters, J.; Chin, C. Evidence for cytochrome f involvement in eggplant cell death induced by palmitoleic acid. Cell Death Differ. 2005, 12, 405. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zuppini, A.; Gerotto, C.; Moscatiello, R.; Bergantino, E.; Baldan, B. Chlorella saccharophila cytochrome f and its involvement in the heat-shock response. J. Exp. Bot. 2009, 60, 4189–4200. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Allu, A.D.; Soja, A.M.; Wu, A.; Szymanski, J.; Balazadeh, S. Salt stress and senescence: Identification of cross-talk regulatory components. J. Exp. Bot. 2014, 65, 3993–4008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosenwasser, S.; Rot, I.; Sollner, E.; Meyer, A.J.; Smith, Y.; Leviatan, N.; Fluhr, R.; Friedman, H. Organelles contribute differentially to reactive oxygen species-related events during extended darkness. Plant Physiol. 2011, 156, 185–201. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ishida, H.; Izumi, M.; Wada, S.; Makino, A. Roles of autophagy in chloroplast recycling. Biochim. Biophys. Acta 2014, 1837, 512–521. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otegui, M.S. Vacuolar degradation of chloroplast components: Autophagy and beyond. J. Exp. Bot. 2017, 69, 741–750. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guyer, L.; Hofstetter, S.S.; Christ, B.; Lira, B.S.; Rossi, M.; Hörtensteiner, S. Different mechanisms are responsible for chlorophyll dephytylation during fruit ripening and leaf senescence in tomato. Plant Physiol. 2014, 166, 44–56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rottet, S.; Devillers, J.; Glauser, G.; Douet, V.; Besagni, C.; Kessler, F. Identification of plastoglobules as a site of carotenoid cleavage. Front. Plant Sci. 2016, 7, 1855. [Google Scholar] [CrossRef] [PubMed]
- Van Wijk, K.J. Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes. Annu. Rev. Plant Biol. 2015, 66, 75–111. [Google Scholar] [CrossRef] [PubMed]
- Nishimura, K.; Kato, Y.; Sakamoto, W. Chloroplast proteases: Updates on proteolysis within and across suborganellar compartments. Plant Physiol. 2016, 171, 2280–2293. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kato, Y.; Murakami, S.; Yamamoto, Y.; Chatani, H.; Kondo, Y.; Nakano, T.; Yokota, A.; Sato, F. The DNA-binding protease, CND41, and the degradation of ribulose-1, 5-bisphosphate carboxylase/oxygenase in senescent leaves of tobacco. Planta 2004, 220, 97–104. [Google Scholar] [CrossRef] [PubMed]
- Castillo-Olamendi, L.; Bravo-García, A.; Morán, J.; Rocha-Sosa, M.; Porta, H. AtMCP1b, a chloroplast-localised metacaspase, is induced in vascular tissue after wounding or pathogen infection. Funct. Plant Biol. 2007, 34, 1061–1071. [Google Scholar] [CrossRef] [Green Version]
- Carrión, C.A.; Costa, M.L.; Martínez, D.E.; Mohr, C.; Humbeck, K.; Guiamet, J.J. 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. 2013, 64, 4967–4980. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhuang, X.; Jiang, L. Chloroplast degradation: Multiple routes into the vacuole. Front. Plant Sci. 2019, 10, 359. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Otegui, M.S.; Noh, Y.S.; Martínez, D.E.; Vila Petroff, M.G.; Staehelin, L.A.; Amasino, R.M.; Guiamet, J.J. Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 2005, 41, 831–844. [Google Scholar] [CrossRef] [PubMed]
- Nakamura, S.; Izumi, M. Regulation of chlorophagy during photoinhibition and senescence: Lessons from mitophagy. Plant Cell Physiol. 2018, 59, 1135–1143. [Google Scholar] [CrossRef] [PubMed]
- Izumi, M.; Nakamura, S.; Li, N. Autophagic turnover of chloroplasts: Its roles and regulatory mechanisms in response to sugar starvation. Front. Plant Sci. 2019, 10, 280. [Google Scholar] [CrossRef] [PubMed]
- Spitzer, C.; Li, F.; Buono, R.; Roschzttardtz, H.; Chung, T.; Zhang, M.; Osteryoung, K.W.; Vierstra, R.D.; Otegui, M.S. The endosomal protein CHARGED MULTIVESICULAR BODY PROTEIN1 regulates the autophagic turnover of plastids in Arabidopsis. Plant Cell 2015, 27, 391–402. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sedigheh, H.G.; Mortazavian, M.; Norouzian, D.; Atyabi, M.; Akbarzadeh, A.; Hasanpoor, K.; Ghorbani, M. Oxidative stress and leaf senescence. BMC Res. Notes 2011, 4, 477. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Marano, M.R.; Carrillo, N. Chromoplast formation during tomato fruit ripening. No evidence for plastid DNA methylation. Plant Mol. Biol. 1991, 16, 11–19. [Google Scholar] [CrossRef] [PubMed]
- Marano, M.R.; Serra, E.C.; Orellano, E.G.; Carrillo, N. The path of chromoplast development in fruits and flowers. Plant Sci. 1993, 94, 1–17. [Google Scholar] [CrossRef]
- Aros, D.; González, V.; Allemann, R.K.; Müller, C.T.; Rosati, C.; Rogers, H.J. Volatile emissions of scented Alstroemeria genotypes are dominated by terpenes, and a myrcene synthase gene is highly expressed in scented Alstroemeria flowers. J. Exp. Bot. 2012, 63, 2739–2752. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gechev, T.; Minkov, I.; Hille, J. Hydrogen peroxide-induced cell death in Arabidopsis: Transcriptional and mutant analysis reveals a role of an oxoglutarate-dependent dioxygenase gene in the cell death process. IUBMB Life 2005, 57, 181–188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jones, M.L. Mineral nutrient remobilization during corolla senescence in ethylene-sensitive and-insensitive flowers. AoB Plants 2013, 5, plt023. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Doorn, W.G.; Çelikel, F.G.; Pak, C.; Harkema, H. Delay of Iris flower senescence by cytokinins and jasmonates. Physiol. Plant. 2013, 148, 105–120. [Google Scholar] [CrossRef] [PubMed]
- Iqbal, N.; Khan, N.A.; Ferrante, A.; Trivellini, A.; Francini, A.; Khan, M. Ethylene role in plant growth, development and senescence: Interaction with other phytohormones. Front. Plant Sci. 2017, 8, 475. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Keech, O. The conserved mobility of mitochondria during leaf senescence reflects differential regulation of the cytoskeletal components in Arabidopsis thaliana. Plant Signal. Behav. 2011, 6, 147–150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mattila, H.; Khorobrykh, S.; Havurinne, V.; Tyystjärvi, E. Reactive oxygen species: Reactions and detection from photosynthetic tissues. J. Photochem. Photobiol. B 2015, 152, 176–214. [Google Scholar] [CrossRef] [PubMed]
- Popović-Bijelić, A.; Mojović, M.; Stamenković, S.; Jovanović, M.; Selaković, V.; Andjus, P.; Bačić, G. Iron-sulfur cluster damage by the superoxide radical in neural tissues of the SOD1G93A ALS rat model. Free Radic. Biol. Med. 2016, 96, 313–322. [Google Scholar] [CrossRef] [PubMed]
- Repetto, M.; Semprine, J.; Boveris, A. Lipid peroxidation: Chemical mechanism, biological implications and analytical determination. In Lipid Peroxidation; Catala, A., Ed.; InTechOpen: London, UK, 2012; pp. 3–30. [Google Scholar]
- Rosenwasser, S.; Fluhr, R.; Joshi, J.R.; Leviatan, N.; Sela, N.; Hetzroni, A.; Friedman, H. ROSMETER: A bioinformatic tool for the identification of transcriptomic imprints related to reactive oxygen species type and origin provides new insights into stress responses. Plant Physiol. 2013, 163, 1071–1083. [Google Scholar] [CrossRef] [PubMed]
- Willems, P.; Mhamdi, A.; Stael, S.; Storme, V.; Kerchev, P.; Noctor, G.; Gevaert, K.; Van Breusegem, F. The ROS wheel: Refining ROS transcriptional footprints. Plant Physiol. 2016, 171, 1720–1733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Locato, V.; Cimini, S.; De Gara, L. ROS and redox balance as multifaceted players of cross-tolerance: Epigenetic and retrograde control of gene expression. J. Exp. Bot. 2018, 69, 3373–3391. [Google Scholar] [CrossRef] [PubMed]
- Farooq, M.A.; Niazi, A.K.; Akhtar, J.; Farooq, M.; Souri, Z.; Karimi, N.; Rengel, Z. Acquiring control: The evolution of ROS-Induced oxidative stress and redox signaling pathways in plant stress responses. Plant Physiol. Biochem. 2019, 141, 353–369. [Google Scholar] [CrossRef] [PubMed]
- Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 2010, 33, 453–467. [Google Scholar] [CrossRef] [PubMed]
- Munné-Bosch, S.; Queval, G.; Foyer, C.H. The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol. 2013, 161, 5–19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smykowski, A.; Zimmermann, P.; Zentgraf, U. G-Box binding factor1 reduces CATALASE2 expression and regulates the onset of leaf senescence in Arabidopsis. Plant Physiol. 2010, 153, 1321–1331. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Breeze, E.; Harrison, E.; McHattie, S.; Hughes, L.; Hickman, R.; Hill, C.; Kiddle, S.; Kim, Y.-S.; Penfold, C.A.; Jenkins, D. High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 2011, 23, 873–894. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Balazadeh, S.; Siddiqui, H.; Allu, A.D.; Matallana-Ramírez, L.P.; Caldana, C.; Mehrnia, M.; Zanor, M.I.; Köhler, B.; Mueller-Roeber, B. A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 2010, 62, 250–264. [Google Scholar] [CrossRef] [PubMed]
- Waters, M.T.; Wang, P.; Korkaric, M.; Capper, R.G.; Saunders, N.J.; Langdale, J.A. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 2009, 21, 1109–1128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sabater, B.; Martín, M. Hypothesis: Increase of the ratio singlet oxygen plus superoxide radical to hydrogen peroxide changes stress defense response to programmed leaf death. Front. Plant Sci. 2013, 4, 479. [Google Scholar] [CrossRef] [PubMed] [Green Version]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mayta, M.L.; Hajirezaei, M.-R.; Carrillo, N.; Lodeyro, A.F. Leaf Senescence: The Chloroplast Connection Comes of Age. Plants 2019, 8, 495. https://doi.org/10.3390/plants8110495
Mayta ML, Hajirezaei M-R, Carrillo N, Lodeyro AF. Leaf Senescence: The Chloroplast Connection Comes of Age. Plants. 2019; 8(11):495. https://doi.org/10.3390/plants8110495
Chicago/Turabian StyleMayta, Martín L., Mohammad-Reza Hajirezaei, Néstor Carrillo, and Anabella F. Lodeyro. 2019. "Leaf Senescence: The Chloroplast Connection Comes of Age" Plants 8, no. 11: 495. https://doi.org/10.3390/plants8110495