Brazilian Journal of Botany

, Volume 39, Issue 2, pp 519–529 | Cite as

Different causes of photosynthetic decline and water status in different stages of girdling in Alhagi sparsifolia Shap. (Fabaceae)

  • Gang-liang Tang
  • Xiang-yi Li
  • Li-sha Lin
  • Fan-jiang Zeng


Phloem girdling can cause decline of photosynthetic rate (Pn), and the reason for Pn decline had been attributed to the reduction of stomatal conductance (Gs) and end-product feedback inhibition. In order to explore the reason for Pn decline, the different stages of girdling—control, semi-girdling (SG), and full-girdling (FG)—were performed on Alhagi sparsifolia Shap. (Fabaceae) on the southern rim of the Taklamakan Desert. Our results showed that on the 1st day, abscisic acid (ABA) content and water use efficiency (WUE) increased, and Gs, Pn, and transpiration rate (Tr) decreased in the full-girdled leaf. On the 30th day, leaf ABA content, leaf starch content, and leaf soluble sugar content increased in the full-girdled leaf, and Gs, Pn, Tr, WUE, root starch content, root soluble sugar content, chlorophyll (Chl) content, maximum photochemical efficiency (Fv/Fm), and leaf water potential (Ψleaf) all decreased in the full-girdled leaf. SG showed no physiological change on the 1st day, whereas on the 30th day, the change was similar to FG, although the degree was less. The result of the present work implied that the reason for Pn decline in girdling may depend on time. In the short term, girdling (FG)-induced Pn decline was due to ABA accumulation, which resulted in the reduction of Gs. In the long term, however, Pn decline caused by girdling was due to many factors, including Gs reduction, which resulted from ABA accumulation, carbohydrate feedback inhibition, degradation of Chl content, decreasing of Fv/Fm, and deterioration of Ψleaf. In addition, a portion (half) of the phloem cannot undertake the transport work conducted by the whole phloem, and thus the girdled half circle of the phloem would lead to a similar effect to FG in the long term, although the degree was less.


Chlorophyll Carbohydrate feedback Girdling Phloem transport Stomatal conductance Water potential 


  1. Ackerson R, Krieg D, Haring C, Chang N (1977) Effects of plant water status on stomatal activity, photosynthesis, and nitrate reductase activity of field grown cotton. Crop Sci 17:81–84CrossRefGoogle Scholar
  2. Adams WW III, Muller O, Cohu CM, Demmig-Adams B (2014) Photosystem II efficiency and non-photochemical fluorescence quenching in the context of source-sink balance. In: Demmig-Adams B et al (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Springer, Berlin, pp 503–529Google Scholar
  3. Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiol 155:64–69CrossRefPubMedGoogle Scholar
  4. Ben Mimoun M, Longuenesse J, Génard M (1996) Pmax as related to leaf: fruit ratio and fruit assimilate demand in peach. J Hortic Sci 71:767–775CrossRefGoogle Scholar
  5. Blum A (2005) Drought resistance, water-use efficiency, and yield potential-are they compatible, dissonant, or mutually exclusive? Crop Pasture Sci 56:1159–1168CrossRefGoogle Scholar
  6. Bouranis DL, Chorianopoulou SN, Dionias A, Liakopoulos G, Nikolopoulos D (2014a) Distribution profile of stomatal conductance and its interrelations to transpiration rate and water dynamics in young maize laminas under sulfate deprivation. Plant Biosyst. doi:10.1080/11263504.2014.984789 Google Scholar
  7. Bouranis DL, Dionias A, Chorianopoulou SN, Liakopoulos G, Nikolopoulos D (2014b) Distribution profiles and interrelations of stomatal conductance, transpiration rate and water dynamics in young maize laminas under nitrogen deprivation. Am J Plant Sci 5:659–670CrossRefGoogle Scholar
  8. Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644CrossRefGoogle Scholar
  9. Cheng Y-C, Fleming GR (2009) Dynamics of light harvesting in photosynthesis. Phys Chem 60:241–262CrossRefGoogle Scholar
  10. Collini E, Wong CY, Wilk KE, Curmi PM, Brumer P, Scholes GD (2010) Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463:644–647CrossRefPubMedGoogle Scholar
  11. DaMatta FM, Cunha RL, Antunes WC, Martins SC, Araujo WL, Fernie AR, Moraes GA (2008) In field-grown coffee trees source–sink manipulation alters photosynthetic rates, independently of carbon metabolism, via alterations in stomatal function. New Phytol 178:348–357CrossRefPubMedGoogle Scholar
  12. 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
  13. Fumuro M (1998) Effects of trunk girdling during early shoot elongation period on tree growth, mineral absorption, water stress, and root respiration in Japanese persimmon (Diospyros kaki L.) cv. Nishimurawase. J Jpn Soc Hortic Sci (Japan) 67:219–227CrossRefGoogle Scholar
  14. Génard M, Lescourret F, Ben Mimoun M, Besset J, Bussi C (1998) A simulation model of growth at the shoot-bearing fruit level. II. Test and effect of source and sink factors in the case of peach. Eur J Agron 9:189–202CrossRefGoogle Scholar
  15. Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol 99:1443–1448CrossRefPubMedPubMedCentralGoogle Scholar
  16. Grant OM, Davies MJ, James CM, Johnson AW, Leinonen I, Simpson DW (2012) Thermal imaging and carbon isotope composition indicate variation amongst strawberry (Fragaria × ananassa) cultivars in stomatal conductance and water use efficiency. Environ Exp Bot 76:7–15CrossRefGoogle Scholar
  17. Héroult A, Lin YS, Bourne A, Medlyn BE, Ellsworth DS (2013) Optimal stomatal conductance in relation to photosynthesis in climatically contrasting Eucalyptus species under drought. Plant Cell Environ 36:262–274CrossRefPubMedGoogle Scholar
  18. Hoad G (1995) Transport of hormones in the phloem of higher plants. Plant Growth Regul 16:173–182CrossRefGoogle Scholar
  19. Jarvis P (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos Trans R Soc Lond 273:593–610CrossRefGoogle Scholar
  20. Kaschuk G, Hungria M, Leffelaar P, Giller K, Kuyper T (2010) Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max [L.] Merrill) dependent on N2 fixation or nitrate supply. Plant Biol 12:60–69CrossRefPubMedGoogle Scholar
  21. Kaufmann MR (1970) Water potential components in growing citrus fruits. Plant Physiol 46:145–149CrossRefPubMedPubMedCentralGoogle Scholar
  22. Layne DR, Flore J (1995) End-product inhibition of photosynthesis in Prunus cerasus L. in response to whole-plant source-sink manipulation. J Am Soc Hortic Sci 120:583–599Google Scholar
  23. Leakey AD, Ainsworth EA, Bernacchi CJ, Zhu X, Long SP, Ort DR (2012) In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation, advances in photosynthesis and respiration. Springer, Berlin, pp 733–768CrossRefGoogle Scholar
  24. 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
  25. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382CrossRefGoogle Scholar
  26. López R, Brossa R, Gil L et al (2015) Stem girdling evidences a trade-off between cambial activity and sprouting and dramatically reduces plant transpiration due to feedback inhibition of photosynthesis and hormone signaling. Front Plant Sci 6:285CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lu P, Chacko E (1998) Evaluation of Granier’s sap flux sensor in young mango trees. Agronomie 18:461–471CrossRefGoogle Scholar
  28. Medlyn BE, Duursma RA, Eamus D, Ellsworth DS, Prentice IC, Barton CV, Crous KY, de Angelis P, Freeman M, Wingate L (2011) Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biol 17:2134–2144CrossRefGoogle Scholar
  29. Mencuccini M, Hölttä T, Sevanto S, Nikinmaa E (2012) Can plant phloem properties affect the link between ecosystem assimilation and respiration? In: EGU General Assembly 2012, vol. 14, Vienna, Austria, p 14419Google Scholar
  30. 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
  31. Nebauer SG, Renau-Morata B, Guardiola JL, Molina R-V (2011) Photosynthesis down-regulation precedes carbohydrate accumulation under sink limitation in Citrus. Tree Physiol 31:169–177CrossRefPubMedGoogle Scholar
  32. Nikinmaa E, Hölttä T, Hari P, Kolari P, Mäkelä A, Sevanto S, Vesala T (2013) Assimilate transport in phloem sets conditions for leaf gas exchange. Plant Cell Environ 36:655–669CrossRefPubMedGoogle Scholar
  33. Pallozzi E, Marino G, Fortunati A, Loreto F, Centritto M (2013) Effect of exposure to UVA radiation on photosynthesis and isoprene emission in Populus × Euroamericana. In: Kuang T et al (eds) Photosynthesis research for food, fuel and the future. Springer, Berlin, pp 763–767CrossRefGoogle Scholar
  34. Pammenter NW, Loreto F, Sharkey TD (1993) End product feedback effects on photosynthetic electron transport. Photosynth Res 35:5–14CrossRefPubMedGoogle Scholar
  35. 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
  36. 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
  37. Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. J Exp Bot 52:1383–1400CrossRefPubMedGoogle Scholar
  38. Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. J Exp Bot 54:539–547CrossRefPubMedGoogle Scholar
  39. Rebetzke GJ, Rattey AR, Farquhar GD, Richards RA, Condon ATG (2013) Genomic regions for canopy temperature and their genetic association with stomatal conductance and grain yield in wheat. Funct Plant Biol 40:14–33CrossRefGoogle Scholar
  40. Roper TR, Williams LE (1989) Net CO2 assimilation and carbohydrate partitioning of grapevine leaves in response to trunk girdling and gibberellic acid application. Plant Physiol 89:1136–1140CrossRefPubMedPubMedCentralGoogle Scholar
  41. Saxe H, Cannell MG, Johnsen Ø, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–399CrossRefGoogle Scholar
  42. Setter TL, Brun WA, Brenner ML (1980) Effect of obstructed translocation on leaf abscisic acid, and associated stomatal closure and photosynthesis decline. Plant Physiol 65:1111–1115CrossRefPubMedPubMedCentralGoogle Scholar
  43. Shi C, Sun G, Zhang H, Xiao B, Ze B, Zhang N, Wu N (2014) Effects of warming on chlorophyll degradation and carbohydrate accumulation of alpine herbaceous species during plant senescence on the Tibetan Plateau. PLoS One 9:e107874CrossRefPubMedPubMedCentralGoogle Scholar
  44. Speirs J, Binney A, Collins M, Edwards E, Loveys B (2013) Expression of ABA synthesis and metabolism genes under different irrigation strategies and atmospheric VPDs is associated with stomatal conductance in grapevine (Vitis vinifera L. cv Cabernet Sauvignon). J Exp Bot 64:1907–1916CrossRefPubMedPubMedCentralGoogle Scholar
  45. Tang GL, Li XY, Lin LS, Guo H, Li L (2015a) Combined effects of girdling and leaf removal on fluorescence characteristic of Alhagi Sparsifolia leaf senescence. Plant Biol 17:980–989CrossRefPubMedGoogle Scholar
  46. Tang GL, Li XY, Lin LS, Zeng FJ, Gu ZY (2015b) Girdling-induced Alhagi sparsifolia senescence and chlorophyll fluorescence changes. Photosynthetica 53:585–596CrossRefGoogle Scholar
  47. Tang G-L, Li X-Y, Lin L-S, Zeng F-J (2015c) Impact of girdling and leaf removal on Alhagi sparsifolia leaf senescence. Plant Growth Regul. doi:10.1007/s10725-015-0086-2 Google Scholar
  48. Ueda M, Shibata EI, Fukuda H, Sano A, Waguchi Y (2014) Girdling and tree death: lessons from Chamaecyparis pisifera. Can J For Res 44:1133–1137CrossRefGoogle Scholar
  49. 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
  50. 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
  51. 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
  52. 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 Hort Sci 127:448–454Google Scholar
  53. Williams LE, Retzlaff WA, Yang W, Biscay PJ, Ebisuda N (2000) Effect of girdling on leaf gas exchange, water status, and non-structural carbohydrates of field-grown Vitis vinifera L. (cv. Flame Seedless). Am J Enol Viticult 51:49–54Google Scholar
  54. 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
  55. Woodrow IE, Berry J (1988) Enzymatic regulation of photosynthetic CO2, fixation in C3 plants. Annu Rev Plant Physiol Plant Mol Biol 39:533–594CrossRefGoogle 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. Yan S, Li X, Li W, Fan P, Duan W, Li S (2011) Photosynthesis and chlorophyll fluorescence response to low sink demand of tubers and roots in Dahlia pinnata source leaves. Biol Plant 55:83–89CrossRefGoogle Scholar
  58. Yang X-Y, Wang F-F, Teixeira da Silva JA, Zhong J, Liu Y-Z, Peng S-A (2013) Branch girdling at fruit green mature stage affects fruit ascorbic acid contents and expression of genes involved in l-galactose pathway in citrus. N Z J Crop Hortic Sci 41:23–31CrossRefGoogle 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. Zhang Y, Guanter L, Berry JA, Joiner J, Tol C, Huete A, Gitelson A, Voigt M, Köhler P (2014) Estimation of vegetation photosynthetic capacity from space-based measurements of chlorophyll fluorescence for terrestrial biosphere models. Global Change Biol 20:3727–3742CrossRefGoogle Scholar
  61. 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 Hort Sci 128:113–119Google Scholar
  62. Zhou S, Medlyn B, Sabaté S, Sperlich D, Prentice IC (2014) Short-term water stress impacts on stomatal, mesophyll and biochemical limitations to photosynthesis differ consistently among tree species from contrasting climates. Tree Physiol 34:1035–1046CrossRefPubMedGoogle Scholar

Copyright information

© Botanical Society of Sao Paulo 2016

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 SciencesUrumqiChina
  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 SciencesUrumqiChina
  4. 4.University of the Chinese Academy of SciencesBeijingChina

Personalised recommendations