Photosynthetica 2020, 58(3):720-731 | DOI: 10.32615/ps.2020.028
Endogenous ascorbic acid delays ethylene-induced leaf senescence in Arabidopsis thaliana
- Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitoring, Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou 510631, China
Leaf senescence is an important event in the plant life cycle. Ethylene and ascorbic acid (AsA) both regulate the leaf senescence process. The role of endogenous AsA in ethylene-induced leaf senescence was explored in two independent endogenous AsA changing Arabidopsis thaliana mutants. The line vtc2-1 with a single base change in VTC was AsA-deficient mutant; the GLDH-overexpressing line (GLDHOE) driven by the CaMV 35S promoter was AsA-overaccumulating mutant. After spraying 600 μM ethephon for 6 d, vtc2-1 showed the most serious leaf chlorosis, reactive oxygen species (ROS) accumulation, chlorophyll breakdown, Rubisco degradation, and had the highest expression level of senescence-associated genes (SAGs), such as SAG12, SAG13, SAG20, and SAG21 among the three lines. In contrast, GLDHOE maintained the highest photosynthetic pigments contents, Rubisco content, antioxidant capacity, and the lowest expression of SAG2, SAG20, and SAG21 among the three lines. Taken together, we conclude that endogenous AsA can delay ethylene-induced senescence by scavenging ROS and inhibiting SAGs expression.
Additional key words: antioxidant; reduced ascorbic acid; senescent; vegetative organ.
Received: November 12, 2019; Revised: March 4, 2020; Accepted: March 19, 2020; Prepublished online: April 18, 2020; Published: June 11, 2020 Show citation
Supplementary files
| Download file | Zheng 2455 supplement.docx File size: 2.06 MB |
References
- Alscher R.G., Donahue J.L., Cramer C.L.: Reactive oxygen species and antioxidants: Relationships in green cells. - Physiol. Plantarum 100: 224-233, 1997.
Go to original source... - Barth C., De Tullio M., Conklin P.L.: The role of ascorbic acid in the control of flowering time and the onset of senescence. - J. Exp. Bot. 57: 1657-1665, 2006.
Go to original source... - 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. 134: 1784-1792, 2004.
Go to original source... - Bradford M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976.
Go to original source... - Caviglia M., Morales L.M.M., Concellón A. et al.: Ethylene signaling triggered by low concentrations of ascorbic acid regulates biomass accumulation in Arabidopsis thaliana. - Free Radical Bio. Med. 122: 130-136, 2018.
Go to original source... - Clough S.J., Bent A.F.: Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. - Plant J. 16: 735-743, 1998.
Go to original source... - Dowdle J., Ishikawa T., Gatzek S. et al.: Two genes in Arabido-psis thaliana encoding GDP-l-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. - Plant J. 52: 673-689, 2007.
Go to original source... - Draper H.H., Hadley M.: Malondialdehyde determination as index of lipid peroxidation. - Method. Enzymol. 186: 421-431, 1990.
Go to original source... - Farouk S.: Ascorbic acid and α-tocopherol minimize salt-induced wheat leaf senescence. - J. Stress Physiol. Biochem. 7: 58-79, 2011.
- Gallie D.R.: The role of L-ascorbic acid recycling in responding to environmental stress and in promoting plant growth. - J. Exp. Bot. 64: 433-443, 2012.
Go to original source... - Gillespie K.M., Ainsworth E.A.: Measurement of reduced, oxidized and total ascorbate content in plants. - Nat. Protoc. 2: 871-874, 2007.
Go to original source... - González-Agüero M., Troncoso S., Gudenschwager O. et al.: Differential expression levels of aroma-related genes during ripening of apricot (Prunus armeniaca L.). - Plant Physiol. Bioch. 47: 435-440, 2009.
Go to original source... - Grbiæ V.: SAG2 and SAG12 protein expression in senescing Arabidopsis plants. - Physiol. Plantarum 119: 263-269, 2003.
Go to original source... - Hensel L.L., Grbiæ V., Baumgarten D.A., Bleecker A.B.: Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. - Plant Cell 5: 553-564, 1993.
Go to original source... - Hundertmark M., Hincha D.K.: Lea (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. - BMC Genomics 9: 118, 2008.
Go to original source... - Ingram J., Bartels D.: The molecular basis of dehydration tolerance in plants. - Annu. Rev. Plant Biol. 47: 377-403, 1996.
Go to original source... - Jander G., Norris S.R., Rounsley S.D. et al.: Arabidopsis map-based cloning in the post-genome era. - Plant Physiol. 129: 440-450, 2002.
Go to original source... - John C.F., Morris K., Jordan B.R. et al.: Ultraviolet-B exposure leads to up-regulation of senescence-associated genes in Arabidopsis thaliana. - J. Exp. Bot. 52: 1367-1373, 2001.
Go to original source... - John I., Drake R., Farrell A. et al.: Delayed leaf senescence in ethylene-deficient ACC-oxidase antisense tomato plants: molecular and physiological analysis. - Plant J. 7: 483-490, 1995.
Go to original source... - Kan J., Wang H.M., Jin C.H. et al.: Changes of reactive oxygen species and related enzymes in mitochondria respiratory metabolism during the ripening of peach fruit. - Agr. Sci. China 10: 149-158, 2011.
Go to original source... - Khan M., Rozhon W., Poppenberger B.: The role of hormones in the aging of plants - a mini-review. - Gerontology 60: 49-55, 2014.
Go to original source... - Khanna-Chopra R., Srivalli B., Ahlawat Y.S.: Drought induces many forms of cysteine proteases not observed during natural senescence. - Biochem. Bioph. Res. Co. 255: 324-327, 1999.
Go to original source... - Khanna-Chopra R.: Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. - Protoplasma 249: 469-481, 2012.
Go to original source... - Kim J.H., Woo H.R., Kim J. et al.: Trifurcate feed-forward regulation of age-dependent cell death involving mir164 in Arabidopsis. - Science 323: 1053-1057, 2009.
Go to original source... - Kotchoni S.O., Larrimore K.E., Mukherjee M. et al.: Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis. - Plant Physiol. 149: 803-815, 2009.
Go to original source... - Leopold A.C.: Senescence in plant development: the death of plants or plant parts may be of positive ecological or physiological value. - Science 134: 1727-1732, 1961.
Go to original source... - Lichtenthaler H.K.: Chlorophyll and carotenoids: Pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987.
Go to original source... - Livak K.J., Schmittgen T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. -Methods 25: 402-408, 2001.
Go to original source... - Lohman K.N., Gan S., John M.C., Amasino R.M.: Molecular analysis of natural leaf senescence in Arabidopsis thaliana. - Physiol. Plantarum 92: 322-328, 1994.
Go to original source... - Luo P., Ning G., Wang Z. et al.: Disequilibrium of flavonol synthase and dihydroflavonol-4-reductase expression asso-ciated tightly to white vs. red color flower formation in plants. -Front. Plant Sci. 6: 1257, 2016.
Go to original source... - Manríquez D., El-Sharkawy I., Flores F.B. et al.: Two highly divergent alcohol dehydrogenases of melon exhibit fruit ripening-specific expression and distinct biochemical characteristics. - Plant Mol. Biol. 61: 675-685, 2006.
Go to original source... - Mencuccini M., Munné-Bosch S.: Physiological and biochemical processes related to ageing and senescence in plants. - In: Shefferson R.P., Jones O.R., Salguero-Gómez R. (ed.): The Evolution of Senescence in the Tree of Life. Pp. 257-283. Cambridge University Press, Cambridge 2017.
Go to original source... - Millar A.H., Mittova V., Kiddle G. et al.: Control of ascorbate synthesis by respiration and its implications for stress responses. - Plant Physiol. 133: 443-447, 2003.
Go to original source... - Navabpour S., Morris K., Allen R. et al.: Expression of senescence-enhanced genes in response to oxidative stress. - J. Exp. Bot. 54: 2285-2292, 2003.
Go to original source... - Naz H., Akram N.A., Ashraf M.: Impact of ascorbic acid on growth and some physiological attributes of cucumber (Cucumis sativus) plants under water-deficit conditions. - Pak. J. Bot. 48: 877-883, 2016.
- Noctor G., Foyer C.H.: Ascorbate and glutathione: keeping active oxygen under control. - Annu. Rev. Plant Biol. 49: 249-279, 1998.
Go to original source... - Ougham H., Hörtensteiner S., Armstead I. et al.: The control of chlorophyll catabolism and the status of yellowing as a biomarker of leaf senescence. - Plant Biol. 10: 4-14, 2008.
Go to original source... - Oxborough K., Baker N.R.: Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components - calculation of qP and Fv'/Fm'; without measuring FO'. - Photosynth. Res. 54: 135-142, 1997.
Go to original source... - Peng C.L., Chen S.W., Lin Z.F., Lin G.Z.: Detection of antioxidative capacity in plants by scavenging organic free radical DPPH. - Prog. Biochem. Biophys. 27: 658-661, 2000. [In Chinese with English abstract]
- Picton S., Barton S.L., Bouzayen M. et al.: Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. - Plant J. 3: 469-481, 1993.
Go to original source... - Pineau B., Layoune O., Danon A., De Paepe R.: L-galactono-1,4-lactone dehydrogenase is required for the accumulation of plant respiratory complex I. - J. Biol. Chem. 283: 32500-32505, 2008.
Go to original source... - Romero-Puertas M.C., Rodríguez-Serrano M., Corpas F.J. et al.: Cadmium-induced subcellular accumulation of O2.- and H2O2 in pea leaves. - Plant Cell Environ. 27: 1122-1134, 2004.
Go to original source... - Rudu¶ I., Sasiak M., Kêpczyñski J.: Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane- 1-carboxylate oxidase (ACO) gene. - Acta Physiol. Plant. 35: 295-307, 2013.
Go to original source... - Sade N., del Mar Rubio-Wilhelmi M., Umnajkitikorn K., Blumwald E.: Stress-induced senescence and plant tolerance to abiotic stress. - J. Exp. Bot. 69: 845-853, 2017.
Go to original source... - Sarwat M., Naqvi A.R., Ahmad P. et al.: Phytohormones and microRNAs as sensors and regulators of leaf senescence: assigning macro roles to small molecules. - Biotechnol. Adv. 31: 1153-1171, 2013.
Go to original source... - Schaller G.E., Bleecker A.B.: Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. - Science 270: 1809-1811, 1995.
Go to original source... - Shi H., Liu W., Yao Y. et al.: Alcohol dehydrogenase 1 (ADH1) confers both abiotic and biotic stress resistance in Arabido-psis. - Plant Sci. 262: 24-31, 2017.
Go to original source... - Singh R.K., Sane V.A., Misra A. et al.: Differential expression of the mango alcohol dehydrogenase gene family during ripening. - Phytochemistry 71: 1485-1494, 2010.
Go to original source... - Smart C.M.: Gene expression during leaf senescence. - New Phytol. 126: 419-448, 1994.
Go to original source... - Stanford A., Bevan M., Northcote D.: Differential expression within a family of novel wound-induced genes in potato. - Mol. Gen. Genet. 215: 200-208, 1989.
Go to original source... - Szarka A., Bánhegyi G., Asard H.: The inter-relationship of ascorbate transport, metabolism and mitochondrial, plastidic respiration. - Antioxid. Redox Sign. 19: 1036-1044, 2013.
Go to original source... - Tabata K., Ôba K., Suzuki K., Esaka M.: Generation and properties of ascorbic acid-deficient transgenic tobacco cells expressing antisense RNA for l-galactono-1,4-lactone dehydrogenase. - Plant J. 27: 139-148, 2001.
Go to original source... - Terzi R., Kalaycioglu E., Demiralay M. et al.: Exogenous ascorbic acid mitigates accumulation of abscisic acid, proline and polyamine under osmotic stress in maize leaves. - Acta Physiol. Plant. 37: 43, 2015.
Go to original source... - Tokunaga T., Miyahara K., Tabata K., Esaka M.: Generation and properties of ascorbic acid-overproducing transgenic tobacco cells expressing sense RNA for L-galactono-1,4-lactone dehydrogenase. - Planta 220: 854-863, 2005.
Go to original source... - van der Graaff E., Schwacke R., Schneider A. et al.: Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. -Plant Physiol. 141: 776-792, 2006.
Go to original source... - Weaver L.M., Gan S., Quirino B., Amasino R.M.: A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. - Plant Mol. Biol. 37: 455-469, 1998.
Go to original source... - Wheeler G.L., Jones M.A., Smirnoff N.: The biosynthetic pathway of vitamin C in higher plants. - Nature 393: 365-369, 1998.
Go to original source... - Wojciechowska N., Sobieszczuk-Nowicka E., Bagniewska-Zadworna A.: Plant organ senescence - regulation by manifold pathways. - Plant Biol. 20: 167-181, 2018.
Go to original source... - Woo H.R., Masclaux-Daubresse C., Lim P.O.: Plant senescence: how plants know when and how to die. - J. Exp. Bot. 69: 715-718, 2018.
Go to original source... - Xu Z., Mahmood K., Rothstein S.J.: ROS induces anthocyanin production via late biosynthetic genes and anthocyanin deficiency confers the hypersensitivity to ROS-generating stresses in Arabidopsis. - Plant Cell Physiol. 58: 1364-1377, 2017.
Go to original source... - Yoshida S.: Molecular regulation of leaf senescence. - Curr. Opin. Plant Biol. 6: 79-84, 2003.
Go to original source... - Yu Y.W., Wang J., Li S.H. et al.: Ascorbic acid integrates the antagonistic modulation of ethylene and abscisic acid in the accumulation of reactive oxygen species. - Plant Physiol. 179: 1861-1875, 2019.
Go to original source... - Zhang T.J., Chow W.S., Liu X.T. et al.: A magic red coat on the surface of young leaves: anthocyanins distributed in trichome layer protect Castanopsis fissa leaves from photoinhibition. - Tree Physiol. 36: 1296-1306, 2016.
Go to original source... - Zhang X.H., Zheng X.T., Sun B.Y. et al.: Over-expression of the CHS gene enhances resistance of Arabidopsis leaves to high light. - Environ. Exp. Bot. 154: 33-43, 2018.
Go to original source...




