Plant Growth Regulation

, Volume 78, Issue 2, pp 205–216 | Cite as

Impact of girdling and leaf removal on Alhagi sparsifolia leaf senescence

  • Gang-Liang Tang
  • Xiang-Yi Li
  • Li-Sha Lin
  • Fan-Jiang Zeng
Original paper


Leaf senescence can be described as the dismantling of cellular components during the terminal stage in the development of plant organs and tissues. In order to determine the leaf senescence process when stem girdling and leaf removal both exist. An experiment was carried out in Alhagi sparsifolia, which grew in the Cele oasis-desert transitional zone with the treatment of control (CK), phloem girdling (PG), leaf removal (LR), and combined girdling and removal (GR). Some parameters related to leaf senescence were measured at the 1st and 30th day post-girdling. The results showed that after PG and GR, leaf soluble sugar content, starch content, abscisic acid content, proline content, and malondialdehyde content increased substantially and leaf photosynthetic rate, stomatal conductance, transpiration rate, photosynthetic pigment content, and water potential decreased substantially compared with CK. It also changed much more in PG leaves than in GR leaves. The change in LR leaves was opposite to that of PG and GR leaves, but the change was rather slight. The result of the present work implied that senescence of leaves treated with PG greatly accelerates, and the accumulation of carbohydrates and ABA in leaves is probably the main reason for this. Separate LR could play a role in delaying leaf senescence in plants; however, this delay effect was not obvious. Nevertheless, partial removal of leaves led to a significant compensation of girdling effects, i.e., senescence will be delayed significantly in girdled leaves when treated with partial LR.


Alhagi sparsifolia Carbohydrate Phloem girdling Phloem transport Leaf removal Senescence 


  1. Agüera E, Cabello P, de la Mata L, Molina E, de la Haba P (2012) Metabolic regulation of leaf senescence in sunflower (Helianthus annuus L.) plants. In: Nagata T (ed) senescence. Rijeka, InTech, pp 51–68Google Scholar
  2. An X, Liao Y, Zhang J, Dai L, Zhang N, Wang B, Liu L, Peng D (2015) Overexpression of rice NAC gene SNAC1 in ramie improves drought and salt tolerance. Plant Growth Regul 76:211–223CrossRefGoogle Scholar
  3. Brand MH (2011) Tissue proliferation condition in micropropagated ericaceous plants. Plant Growth Regul 63:131–136CrossRefGoogle Scholar
  4. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnol J 1:3–22CrossRefPubMedGoogle Scholar
  5. Crafts-Brandner SJ, Below FE, Harper JE, Hageman RH (1984) Effects of pod removal on metabolism and senescence of nodulating and nonnodulating soybean isolines II. Enzymes and Chlorophyll. Plant Physiol 75(2):318–322CrossRefPubMedGoogle Scholar
  6. Dai J, Dong H (2011) Stem girdling influences concentrations of endogenous cytokinins and abscisic acid in relation to leaf senescence in cotton. Acta Physiol Plant 33(5):1697–1705CrossRefGoogle Scholar
  7. Demiral T, Türkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257CrossRefGoogle Scholar
  8. Di Vaio C, Petito A, Buccheri M (2001) Effect of girdling on gas exchanges and leaf mineral content in the “Independence” nectarine. J Plant Nutr 24:1047–1060CrossRefGoogle Scholar
  9. Distelfeld A, Avni R, Fischer AM (2014) Senescence, nutrient remobilization, and yield in wheat and barley. J Exp Bot 65(14):3783–3798CrossRefPubMedGoogle Scholar
  10. García-Plazaola J, Hernández A, Becerril J (2003) Antioxidant and pigment composition during autumnal leaf senescence in woody deciduous species differing in their ecological traits. Plant Biol 5:557–566CrossRefGoogle Scholar
  11. Gaweł S, Wardas M, Niedworok E, Wardas P (2003) Malondialdehyde (MDA) as a lipid peroxidation marker. Wiadomosci lekarskie (Warsaw, Poland: 1960) 57:453–455Google Scholar
  12. Gregersen P, Holm P, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol 10:37–49CrossRefPubMedGoogle Scholar
  13. Hörtensteiner S (2006) Chlorophyll degradation during senescence*. Ann Rev Plant Biol 57:55–77CrossRefGoogle Scholar
  14. Kong L, von Aderkas P, Owen SJ, Jaquish B, Woods J, Abrams SR (2011) Effects of stem girdling on cone yield and endogenous phytohormones and metabolites in developing long shoots of Douglas-fir (Pseudotsuga menziesii). N For 43(4):491–503Google Scholar
  15. Kosugi H, Kikugawa K (1985) Thiobarbituric acid reaction of aldehydes and oxidized lipids in glacial acetic acid. Lipids 20:915–921CrossRefGoogle Scholar
  16. Krapp A, Stitt M (1995) 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 195:313–323CrossRefGoogle Scholar
  17. Kumar M, Singh V, Arora A, Singh N (2014) The role of abscisic acid (ABA) in ethylene insensitive Gladiolus (Gladiolus grandiflora Hort.) flower senescence. Acta Physiologiae Plantarum 36:151–159CrossRefGoogle Scholar
  18. Li CY, Weiss D, Goldschmidt EE (2003) Girdling affects carbohydrate-related gene expression in leaves, bark and roots of alternate-bearing citrus trees. Ann Bot 92:137–143PubMedCentralCrossRefPubMedGoogle Scholar
  19. Li N, Zhang S, Zhao Y, Li B, Zhang J (2011) Over-expression of AGPase genes enhances seed weight and starch content in transgenic maize. Planta 233:241–250CrossRefPubMedGoogle Scholar
  20. Li Y, Xu S, Gao J, Pan S, Wang G (2015) Bacillus subtilis-regulation of stomatal movement and instantaneous water use efficiency in Vicia faba. Plant Growth Regul. doi:10.1007/s10725-015-0073-7 Google Scholar
  21. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  22. Mae T, Ohira K (1981) The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol 22(6):1067–1074Google Scholar
  23. Mahouachi J, Iglesias DJ, Agustí M, Talon M (2009) Delay of early fruitlet abscission by branch girdling in citrus coincides with previous increases in carbohydrate and gibberellin concentrations. Plant Growth Regul 58:15–23CrossRefGoogle Scholar
  24. Masclaux C, Valadier M-H, Brugière N, Morot-Gaudry J-F, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211:510–518CrossRefPubMedGoogle Scholar
  25. Miller A, Schlagnhaufer C, Spalding M, Rodermel S (2000) Carbohydrate regulation of leaf development: prolongation of leaf senescence in Rubisco antisense mutants of tobacco. Photosynth Res 63:1–8CrossRefPubMedGoogle Scholar
  26. Mittler R, Merquiol E, Hallak-Herr E, Rachmilevitch S, Kaplan A, Cohen M (2001) Living under a ‘dormant’ canopy: a molecular acclimation mechanism of the desert plant Retama raetam. Plant J 25:407–416CrossRefPubMedGoogle Scholar
  27. Mondal MH, Brun WA, Brenner ML (1978) Effects of sink removal on photosynthesis and senescence in leaves of soybean (Glycine max L.) plants. Plant Physiol 61(3):394–397PubMedCentralCrossRefPubMedGoogle Scholar
  28. Nooden L, Rupp D, Derman B (1978) Separation of seed development from monocarpic senescence in soybeans. Nat (Lond) 271:354–357CrossRefGoogle Scholar
  29. Palmer LJ, Palmer LT, Rutzke MA, Graham RD, Stangoulis JC (2014) Nutrient variability in phloem: examining changes in K, Mg, Zn and Fe concentration during grain loading in common wheat (Triticum aestivum). Physiol Plantarum 152(4):729–737CrossRefGoogle Scholar
  30. Parrott D, Yang L, Shama L, Fischer A (2005) Senescence is accelerated, and several proteases are induced by carbon “feast” conditions in barley (Hordeum vulgare L.) leaves. Planta 222:989–1000CrossRefPubMedGoogle Scholar
  31. Parrott DL, McInnerney K, Feller U, Fischer AM (2007) Steam-girdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. New Phytol 176:56–69CrossRefPubMedGoogle Scholar
  32. Parrott DL, Martin JM, Fischer AM (2010) 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. N Phytol 187:313–331CrossRefGoogle Scholar
  33. Pérez P, Alonso A, Zita G, Morcuende R, Martínez-Carrasco R (2011) Down-regulation of Rubisco activity under combined increases of CO2 and temperature minimized by changes in Rubisco kcat in wheat. Plant Growth Regul 65:439–447CrossRefGoogle Scholar
  34. Petrie P, Trought M, Howell G (2000) Influence of leaf ageing, leaf area and crop load on photosynthesis, stomatal conductance and senescence of grapevine (Vitis vinifera L. cv. Pinot noir) leaves. Vitis-Geilweilerhof 39:31–36Google Scholar
  35. Polívka T, Frank HA (2010) Molecular factors controlling photosynthetic light harvesting by carotenoids. Acc Chem Res 43:1125–1134PubMedCentralCrossRefPubMedGoogle Scholar
  36. Pourtau N, Marès M, Purdy S, Quentin N, Ruël A, Wingler A (2004) Interactions of abscisic acid and sugar signalling in the regulation of leaf senescence. Planta 219:765–772CrossRefPubMedGoogle Scholar
  37. Pourtau N, Jennings R, Pelzer E, Pallas J, Wingler A (2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224:556–568CrossRefGoogle Scholar
  38. Rabiza-wider J, Łukaszewska A, Skutnik E, Leszko M (2004) Ammonium and proline accumulation in senescing cut leaves of Zantedeschia. Acta Physiologiae Plantarum 26:417–422CrossRefGoogle Scholar
  39. Rahman MM, Chongling Y, Rahman MM, Islam KS (2012) Effects of copper on growth, accumulation, antioxidant activity and malondialdehyde content in young seedlings of the mangrove species Kandelia candel (L.). Plant Biosyst 146:47–57CrossRefGoogle Scholar
  40. Regier N, Streb S, Zeeman SC, Frey B (2010) Seasonal changes in starch and sugar content of poplar (Populus deltoides × nigra cv. Dorskamp) and the impact of stem girdling on carbohydrate allocation to roots. Tree Physiol 30:979–987CrossRefGoogle Scholar
  41. Setter TL, Brun WA, Brenner ML (1980) Effect of obstructed translocation on leaf abscisic acid, and associated stomatal closure and photosynthesis decline. Plant Physiol 65:1111–1115PubMedCentralCrossRefPubMedGoogle Scholar
  42. Setter TL, Brun WA, Brenner ML (1981) Abscisic acid translocation and metabolism in soybeans following depodding and petiole girdling treatments. Plant Physiol 67:774–779PubMedCentralCrossRefPubMedGoogle Scholar
  43. Singh I, Shah K (2015) Evidences for suppression of cadmium induced oxidative stress in presence of sulphosalicylic acid in rice seedlings. Plant Growth Regul 76:99–110CrossRefGoogle Scholar
  44. Suzuki Y, Shioi Y (2004) Changes in chlorophyll and carotenoid contents in radish (Raphanus sativus) cotyledons show different time courses during senescence. Physiol Plant 122:291–296CrossRefGoogle Scholar
  45. Tang G, Li X, Lin L, Guo H, Li L (2015) Combined effects of girdling and leaf removal on fluorescence characteristic of Alhagi sparsifolia leaf senescence. Plant Biol. doi:10.1111/plb.12309 Google Scholar
  46. Urban L, Léchaudel M, Lu P (2004) Effect of fruit load and girdling on leaf photosynthesis in Mangifera indica L. J Exp Bot 55:2075–2085CrossRefPubMedGoogle Scholar
  47. Veselov D, Sharipova G, Veselov S, Kudoyarova G (2008) The effects of NaCl treatment on water relations, growth, and ABA content in barley cultivars differing in drought tolerance. J Plant Growth Regul 27:380–386CrossRefGoogle Scholar
  48. Vonlanthen B, Zhang X, Bruelheide H (2010) On the run for water–root growth of two phreatophytes in the Taklamakan Desert. J Arid Environ 74(12):1604–1615CrossRefGoogle Scholar
  49. Vysotskaya L, Kudoyarova G, Veselov S, Jones H (2004) Unusual stomatal behaviour on partial root excision in wheat seedlings. Plant, Cell Environ 27:69–77CrossRefGoogle Scholar
  50. Weaver LM, Amasino RM (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol 127:876–886PubMedCentralCrossRefGoogle Scholar
  51. Williams L, Araujo F (2002) Correlations among predawn leaf, midday leaf, and midday stem water potential and their correlations with other measures of soil and plant water status in Vitis vinifera. J Am Soc Hortic Sci 127:448–454Google Scholar
  52. Williams L, Baeza P, Vaughn P (2012) Midday measurements of leaf water potential and stomatal conductance are highly correlated with daily water use of Thompson Seedless grapevines. Irrig Sci 30:201–212CrossRefGoogle Scholar
  53. Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57:391–399CrossRefPubMedGoogle Scholar
  54. Wittenbach VA (1982) Effect of pod removal on leaf senescence in soybeans. Plant Physiol 70:1544–1548PubMedCentralCrossRefPubMedGoogle Scholar
  55. Wolfe D, Henderson D, Hsiao T, Alvino A (1988) Interactive water and nitrogen effects on senescence of maize. II. Photosynthetic decline and longevity of individual leaves. Agron J 80:865–870CrossRefGoogle Scholar
  56. Xue W, Li X, Lin L, Wang Y, Li L (2011) Effects of elevated temperature on photosynthesis in desert plant Alhagi sparsifolia S. Photosynthetica 49:435–447CrossRefGoogle Scholar
  57. Xue W, Li X, Zhu J, Lin L (2012) Effects of temperature and irradiance on photosystem activity during Alhagi sparsifolia leaf senescence. Biol Plant 56(4):785–788CrossRefGoogle Scholar
  58. Ying Y, Yue Y, Huang X, Wang H, Mei L, Yu W, Zheng B, Wu J (2013) Salicylic acid induces physiological and biochemical changes in three Red bayberry (Myric rubra) genotypes under water stress. Plant Growth Regul 71:181–189CrossRefGoogle Scholar
  59. Zeng J, Zeng F, Arndt S, Guo H, Yan H, Xing W, Liu B (2008) Growth, physiological characteristics and ion distribution of NaCl stressed Alhagi sparsifolia seedlings. Chin Sci Bull 53:169–176CrossRefGoogle Scholar
  60. Zeng F-J, Lu Y, H-F Guo, Liu B, Zeng J, Zhang L-G (2012) Ecological characteristics of Alhagi sparsifolia Shap. seedling roots under different irrigation treatments. Russ J Ecol 43(3):196–203CrossRefGoogle Scholar
  61. Zhang Z, Li G, Gao H, Zhang L, Yang C, Liu P, Meng Q (2012) Characterization of photosynthetic performance during senescence in stay-green and quick-leaf-senescence Zea mays L. inbred lines. PLoS ONE 7:e42936PubMedCentralCrossRefPubMedGoogle Scholar
  62. Zhang H, Liu K, Wang Z, Liu L, Yang J (2015) Abscisic acid, ethylene and antioxidative systems in rice grains in relation with grain filling subjected to postanthesis soil-drying. Plant Growth Regul 76:135–146CrossRefGoogle Scholar
  63. Zhou R, Quebedeaux B (2003) Changes in photosynthesis and carbohydrate metabolism in mature apple leaves in response to whole plant source-sink manipulation. J Am Soc Hortic Sci 128:113–119Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Gang-Liang Tang
    • 1
    • 2
    • 3
    • 4
  • Xiang-Yi Li
    • 1
    • 2
    • 3
  • Li-Sha Lin
    • 1
    • 2
    • 3
  • Fan-Jiang Zeng
    • 1
    • 2
    • 3
  1. 1.State Key Laboratory of Desert and Oasis Ecology, Xinjiang Institute of Ecology and GeographyChinese Academy of SciencesÜrümqiChina
  2. 2.Cele National Station of Observation and Research for Desert-Grassland Ecosystem in XinjiangCeleChina
  3. 3.Key Laboratory of Biogeography and Bioresource in Arid ZoneChinese Academy of SciencesÜrümqiChina
  4. 4.University of Chinese Academy of SciencesBeijingChina

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