Abstract
Senescence constitutes the final stage of a plant organ and tissue development and is a subject to gene control and strict regulation. By the late growing season, when Alhagi sparsifolia entered the natural senescence period, a girdling treatment was carried out on the phloem to increase the sugar content in leaves and to investigate carbohydrate-induced leaf senescence. After the semi-girdling and full-girdling treatment, organic matter could not leave leaves due to the destruction of sieve tubes. This led to constantly increasing sugar contents in leaves. Girdling was shown to greatly accelerate the senescence of plants. In girdled leaves, chlorophyll (Chl) a, Chl b, carotenoids (Car), and both ratios of Chl a/b and Chl/Car were significantly reduced. On the donor side of PSII, the oxygen-evolving complex was inhibited under high concentrations of carbohydrates, which was manifested as the emergence of the K phase in fluorescence kinetic curves. On the acceptor side of PSII, the high carbohydrate content also led to the disruption of electron transport and reduced light-use efficiency, which was manifested as a reduction in numerous fluorescence parameters. We believe that the emergence and development of plant senescence was not necessarily induced by the high content of carbohydrates, because even a decrease in the carbohydrate concentration could not stop the senescence process. Although the high content of carbohydrates in plants could induce plant senescence, this kind of senescence was likely a pathological process, including degradations of physiological functions.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Abbreviations
- Car:
-
carotenoids
- Chl:
-
chlorophyll
- CK:
-
control
- DM:
-
dry mass
- FG:
-
full-girdling
- FM:
-
fresh mass
- Fv/Fm :
-
maximal quantum yield of PSII photochemistry
- MDA:
-
malondialdehyde
- M0 :
-
approximated initial slope of the fluorescence transient
- OEC:
-
oxygen-evolving complex
- PIabs :
-
performance index on absorption basis
- P N :
-
net photosynthetic rate
- Pro:
-
proline
- PQ:
-
plastoquinone
- QA :
-
primary quinone acceptor of PSII
- QB :
-
secondary quinone acceptor of PSII
- SE:
-
standard error
- SG:
-
semigirdling
- Sm :
-
normalized total complementary area above the O-J-I-P transient
- Ψ0 :
-
probability that a trapped exciton moves an electron into the electron transport chain beyond QA − (at t = 0)
- φE0 :
-
quantum yield for electron transport (at t = 0)
References
Appenroth K.J., Stöckel J., Srivastava A., Strasser.R.J.: Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements. — Environ. Pollut. 115: 49–64, 2001.
Argyroudi-Akoyunoglou J., Akoyunoglou G.: Photoinduced changes in the chlorophyll a to chlorophyll b ratio in young bean plants. — Plant Physiol. 46: 247–249, 1970.
Biswal B.: Carotenoid catabolism during leaf senescence and its control by light. — J. Photochem. Photobiol. B 30: 3–13, 1995.
Björkman O., Demmig B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. — Planta 170: 489–504, 1987.
Bleecker A.B., Patterson S.E.: Last exit: senescence, abscission, and meristem arrest in Arabidopsis. — Plant Cell 9: 1169–1179, 1997.
Buchanan-Wollaston V., Earl S., Harrison E. et al.: The molecular analysis of leaf senescence — a genomics approach. — Plant Biotechnol. J. 1: 3–22, 2003.
Buchanan-Wollaston V.: The molecular biology of leaf senescence. — J. Exp. Bot. 48: 181–199, 1997.
Burton G.W., Ingold K.U.: Beta-carotene: an unusual type of lipid antioxidant. — Science 224: 569–573, 1984.
Dai J., Dong H.: Stem girdling influences concentrations of endogenous cytokinins and abscisic acid in relation to leaf senescence in cotton. — Acta Physiol. Plant. 33: 1697–1705, 2011.
Dai N., Schaffer A., Petreikov M. et al.: Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. — Plant Cell 11: 1253–1266, 1999.
Demiral T., Türkan I.: Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. — Environ. Exp. Bot. 53: 247–257, 2005.
Dong H., Niu Y., Li W. et al.: Effects of cotton rootstock on endogenous cytokinins and abscisic acid in xylem sap and leaves in relation to leaf senescence. — J. Exp. Bot. 59: 1295–1304, 2008.
Feller U., Fischer A.: Nitrogen metabolism in senescing leaves. — Crit. Rev. Plant Sci. 13: 241–273, 1994.
Gan S., Amasino R.M.: Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). — Plant Physiol. 113: 313–319, 1997.
Gregersen P., Holm P., Krupinska K.: Leaf senescence and nutrient remobilisation in barley and wheat. — Plant Biol. 10: 37–49, 2008.
Guissé B., Srivastava A., Strasser R.: The polyphasic rise of the chlorophyll a fluorescence (OKJIP) in heat stressed leaves. — Arch. Sci. 48: 147–160, 1995.
Harrell D.C., Williams L.E.: Net CO2 assimilation rate of grapevine leaves in response to trunk girdling and gibberellic acid application. — Plant Physiol. 83: 457–459, 1987.
Hendry G.: Where does all the green go? — New Scientist 1637: 38–42, 1988.
Himelblau E., Amasino R.M.: Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence. — J. Plant Physiol. 158: 1317–1323, 2001.
Hörtensteiner S.: Chlorophyll degradation during senescence. — Annu. Rev. Plant Biol. 57: 55–77, 2006.
Humbeck K., Quast S., Krupinska K.: Functional and molecular changes in the photosynthetic apparatus during senescence of flag leaves from field-grown barley plants. — Plant Cell Environ. 19: 337–344, 1996.
Jaleel C.A., Manivannan P., Sankar B. et al.: Calcium chloride effects on salinity-induced oxidative stress, proline metabolism and indole alkaloid accumulation in Catharanthus roseus. — C. R. Biol. 330: 674–683, 2007.
Jongebloed U., Szederkényi J., Hartig K. et al.: Sequence of morphological and physiological events during natural ageing and senescence of a castor bean leaf: sieve tube occlusion and carbohydrate back-up precede chlorophyll degradation. — Physiol. Plantarum 120: 338–346, 2004.
Koch K.: Carbohydrate-modulated gene expression in plants. — Annu. Rev. Plant Biol. 47: 509–540, 1996.
Kosugi H., Kikugawa K.: Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. — Lipids 20: 915–921, 1985.
Krapp A., Stitt M.: An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. — Planta 195: 313–323, 1995.
Li N., Zhang S., Zhao Y. et al.: Over-expression of AGPase genes enhances seed weight and starch content in transgenic maize. — Planta 233: 241–250, 2011.
Lichtenthaler H.K., Babani F.: Light adaptation and senescence of the photosynthetic apparatus. Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity. — In: Papageorgiou, G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 713–736. Springer, Dordrecht 2004.
Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. — Methods Enzymol. 148: 350–382, 1987.
Lim P.O., Kim H.J., Gil-Nam H.: Leaf senescence. — Annu. Rev. Plant Biol. 58: 115–136, 2007.
Lu P., Chacko E.: Evaluation of Granier’s sap flux sensor in young mango trees. — Agronomie 18: 461–471, 1998.
Lu Q., Lu C., Zhang J. et al.: Photosynthesis and chlorophyll a fluorescence during flag leaf senescence of field-grown wheat plants. — J. Plant Physiol. 159: 1173–1178, 2002.
Masclaux C., Valadier M.-H., Brugière N. et al.: Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. — Planta 211: 510–518, 2000.
Matile P.: Fluorescent idioblasts in autumn leaves of Ginkgo biloba. — Bot. Helv. 104: 87–92, 1994.
Matile P.: Chloroplast senescence. — Topics Photosynth. 12: 413–440, 1992.
Mickelson S., See D., Meyer F.D. et al.: Mapping of QTL associated with nitrogen storage and remobilization in barley (Hordeum vulgare L.) leaves. — J. Exp. Bot. 54: 801–812, 2003.
Miller A., Schlagnhaufer C., Spalding M., Rodermel, S.: Carbohydrate regulation of leaf development: prolongation of leaf senescence in Rubisco antisense mutants of tobacco. — Photosynth. Res. 63: 1–8, 2000.
Mittler R., Merquiol E., Hallak-Herr E. et al.: Living under a ‘dormant’ canopy: a molecular acclimation mechanism of the desert plant Retama raetam. — Plant J. 25: 407–416, 2001.
Moore B., Zhou L., Rolland F. et al.: Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. — Science 300: 332–336, 2003.
Ono K., Nishi Y., Watanabe A., Terashima, I.: Possible mechanisms of adaptive leaf senescence. — Plant Biol. 3: 234–243, 2001.
Parrott D., Yang L., Shama L., Fischer, A.M.: Senescence is accelerated, and several proteases are induced by carbon “feast” conditions in barley (Hordeum vulgare L.) leaves. — Planta 222: 989–1000, 2005.
Parrott D.L., Martin J.M., Fischer A.M.: Analysis of barley (Hordeum vulgare) leaf senescence and protease gene expression: a family C1A cysteine protease is specifically induced under conditions characterized by high carbohydrate, but low to moderate nitrogen levels. — New Phytol. 187: 313–331, 2010.
Parrott D.L., McInnerney K., Feller U., Fischer, A.M.: Steamgirdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. — New Phytol. 176: 56–69, 2007.
Pourtau N., Jennings R., Pelzer E. et al.: Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. — Planta 224: 556–568, 2006.
Pourtau N., Marès M., Purdy S. et al.: Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. — Planta 219: 765–772, 2004.
Rahman M.M., Chongling Y., Rahman M.M., Islam, K.S.: Effects of copper on growth, accumulation, antioxidant activity and malondialdehyde content in young seedlings of the mangrove species Kandelia candel (L.). — Plant Biosyst. 146: 47–57, 2012.
Rajcan I., Dwyer L.M., Tollenaar M.: Note on relationship between leaf soluble carbohydrate and chlorophyll concentrations in maize during leaf senescence. — Field Crops Res. 63: 13–17, 1999.
Rivas F., Erner Y., Alós E. et al.: Girdling increases carbohydrate availability and fruit-set in citrus cultivars irrespective of parthenocarpic ability. — J. Hortic. Sci. Biotechnol. 81: 289–295, 2006.
Rivas F., Fornes F., Rodrigo J.M. et al.: Changes in carotenoids and ABA content in Citrus leaves in response to girdling. — Sci. Hortic. 127: 482–487, 2011.
Roper T.R., Williams L.E.: Net CO2 assimilation and carbohydrate partitioning of grapevine leaves in response to trunk girdling and gibberellic acid application. — Plant Physiol. 89: 1136–1140, 1989.
Schaper H., Chacko E.: Effect of irradiance, leaf age, chlorophyll content and branch-girdling on gas exchange of cashew (Anacardium accidentale L.) leaves. — J. Hortic. Sci. 68: 541–550, 1993.
Smart C.M.: Gene expression during leaf senescence. — New Phytol. 126: 419–448, 1994.
Strasser B.J., Strasser R.J.: Measuring fast fluorescence transients to address environmental questions: the JIP test. — In: Mathis P. (ed.): Photosynthesis: From Light to Biosphere. Volume 5. Pp. 977–980. Kluwer Academic Publisher, Dordrecht 1995.
Strasser R.J., Govindjee: On the O-J-I-P fluorescence transient in leaves and D1 mutants of Chlamydomonas reinhardtii. — In: Murata, N. (ed.): Research in Photosynthesis. 2nd Ed., Vol. 2. Pp. 529–532. Kluwer Academic Publishers, Dordrecht 1992.
Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples. — In: Yunus M., Pathre U., Mohanty P. (eds.): Probing Photosynthesis: Mechanism, Regulation and Adaptation. Pp. 443–480. Taylor and Francis, London 2000.
Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the chlorophyll a fluorescence transient. — In: Papageorgiou, G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 321–362. Springer, Dordrecht 2004.
Thomas H., Smart C.M.: Crops that stay green. — Ann. Appl. Biol. 123: 193–219, 1993.
Urban L., Alphonsout L.: Girdling decreases photosynthetic electron fluxes and induces sustained photoprotection in mango leaves. — Tree Physiol. 27: 345–352, 2007.
Van Heerden P.D., Strasser R.J., Krüger G.H.: Reduction of dark chilling stress in N2-fixing soybean by nitrate as indicated by chlorophyll a fluorescence kinetics. — Physiol. Plantarum 121: 239–249, 2004.
Van Heerden P.D., Tsimilli-Michael M., Krüger G.H., Strasser, R.J.: Dark chilling effects on soybean genotypes during vegetative development: parallel studies of CO2 assimilation, chlorophyll a fluorescence kinetics O-J-I-P and nitrogen fixation. — Physiol. Plantarum 117: 476–491, 2003.
Van Rensburg L., Kruger G., Eggenberg P., Strasser, R.J.: Can screening criteria for drought resistance in Nicotiana tabacum L. be derived from the polyphasic rise of the chlorophyll a fluorescence transient (OJIP)? — S. Afr. J. Bot. 62: 337–341, 1996.
Willekens H., Van Camp W., Van Montagu M. et al.: Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. — Plant Physiol. 106: 1007–1014, 1994.
Wingler A., Purdy S., MacLean J.A., Pourtau, N.: The role of sugars in integrating environmental signals during the regulation of leaf senescence. — J. Exp. Bot. 57: 391–399, 2006.
Wingler A., Von Schaewen A., Leegood R.C. et al.: Regulation of leaf senescence by cytokinin, sugars, and light effects on NADH-dependent hydroxypyruvate reductase. — Plant Physiol. 116: 329–335, 1998.
Xue W., Li X., Lin L. et al.: Effects of elevated temperature on photosynthesis in desert plant Alhagi sparsifolia S. — Photosynthetica 49: 435–447, 2011.
Yang X.-Y., Wang F.-F., Teixeira da Silva J.A. et al.: Branch girdling at fruit green mature stage affects fruit ascorbic acid contents and expression of genes involved in L-galactose pathway in citrus. — New Zealand J. Crop Hortic. Sci. 41: 23–31, 2013.
Yoshida S.: Molecular regulation of leaf senescence. — Curr. Opin. Plant Biol. 6: 79–84, 2003.
Zeng J., Zeng F., Arndt S. et al.: Growth, physiological characteristics and ion distribution of NaCl stressed Alhagi sparsifolia seedlings. — Chin. Sci. Bull. 53: 169–176, 2008.
Author information
Authors and Affiliations
Corresponding author
Additional information
Acknowledgments: We thank the anonymous reviewers for their invaluable comments. We also express gratitude to Zhuyu Gu for assistance with experiment, and Jake Carpenter for polishing the English in this manuscript. This work was financially supported by the National Natural Sciences Foundation of China (41571057), Key Program of Joint Funds of the National Natural Sciences Foundation and the Government of Xinjiang Uygur Autonomous Region of China (U1203201), National Natural Sciences Foundation of China (41371516).
Rights and permissions
About this article
Cite this article
Tang, G.L., Li, X.Y., Lin, L.S. et al. Girdling-induced Alhagi sparsifolia senescence and chlorophyll fluorescence changes. Photosynthetica 53, 585–596 (2015). https://doi.org/10.1007/s11099-015-0148-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-015-0148-8