Photosynthetica 2019, 57(3):780-787 | DOI: 10.32615/ps.2019.097

Photoprotection in heteromorphic leaves of savin juniper (Juniperus sabina L.)

J.L. ZHANG1,2, X.H. XU1, X.G. LI1, Y.L. LI1, R.D. GUY2, H.P. CHEN1
1 College of Forestry, Agricultural University of Hebei, 071000 Baoding, China
2 Department of Forest and Conservation Sciences, Faculty of Forestry, University of British Columbia, V6T 1Z4 Vancouver, Canada

Savin juniper has green, photosynthetic branchlets with scale and/or needle leaves and these heteromorphic forms may contribute differentially to its success in open, arid environments. To test differences in photoprotection between fully sun-exposed scale-holding branchlets (SHB) and needle-holding branchlets (NHB), we measured gas exchange, chlorophyll (Chl) fluorescence, and pigment concentrations. NHB had higher net photosynthetic rate, stomatal conductance, and intrinsic water-use efficiency. In contrast, SHB had higher nonphotochemical quenching. Chl a, Chl b, and antheraxanthin concentrations were higher in NHB. SHB had higher zeaxanthin, lutein, and carotenoids (Car), and higher Chl a/b, Car/Chl, and α-carotene/β-carotene ratios. The results indicate greater engagement of xanthophyll-based thermal dissipation in SHB. Branchlet types acclimate to strong light using different strategies; SHB by investing in photoprotective mechanisms, and NHB by having a high photosynthetic capacity. Heterophylly may allow savin juniper to be more functionally flexible under variable environmental conditions.

Keywords: gas exchange; leaf morphology; photoinhibition; Sabina vulgaris Ant.; water-use efficiency.

Received: February 17, 2019; Accepted: May 20, 2019; Prepublished online: June 14, 2019; Published: July 23, 2019Show citation

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ZHANG, J.L., XU, X.H., LI, X.G., LI, Y.L., GUY, R.D., & CHEN, H.P. (2019). Photoprotection in heteromorphic leaves of savin juniper (Juniperus sabina L.). Photosynthetica57(3), 780-787. doi: 10.32615/ps.2019.097.
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References

  1. Björkman O., Demmig-Adams B.: Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. - In: Schulze E.D., Caldwell M.M. (ed.): Ecophysiology of Photosynthesis. Pp. 17-47. Springer, Berlin 1995. Go to original source...
  2. Cao H., Zhang J., Xu J. et al.: Comprehending crystalline β-carotene accumulation by comparing engineered cell models and the natural carotenoid-rich system of citrus. - J. Exp. Bot. 63: 4403-4417, 2012. Go to original source...
  3. Cazzaniga S., Bressan M., Carbonera D. et al.: Differential roles of carotenes and xanthophylls in photosystem I photoprotection. -Biochemistry-US 55: 3636-3649, 2016. Go to original source...
  4. de Laubenfels D.J.: The external morphology of coniferous leaves. - Phytomorphology 3: 1-20, 1953.
  5. Demmig-Adams B., Adams III W.W., Barker D.H. et al.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. - Physiol. Plantarum 98: 253-264, 1996. Go to original source...
  6. Demmig-Adams B., Adams III W.W.: The role of xanthophyll cycle carotenoids in the protection of photosynthesis. - Trends Plant Sci. 1: 21-26, 1996. Go to original source...
  7. Deschamp P.A., Cooke T.J.: Leaf dimorphism in the aquatic angiosperm Callitriche heterophylla. - Am. J. Bot. 72: 1377-1387, 1985. Go to original source...
  8. Dong G., Chen Y., Li G. et al.: [Xanthophyll cycle and non-radiative energy dissipation in sun and shade plants.] - J. Wuhan Bot. Res. 19: 128-134, 2001. [In Chinese]
  9. Dörken V. M., Lepetit B.: Morpho-anatomical and physiological differences between sun and shade leaves in Abies alba Mill. (Pinaceae, Coniferales): a combined approach. - Plant Cell Environ. 41: 1683-1697, 2018. Go to original source...
  10. Esteban R., Barrutia O., Artetxe U. et al.: Internal and external factors affecting photosynthetic pigment composition in plants: a meta-analytical approach. - New Phytol. 206: 268-280, 2015. Go to original source...
  11. Gilmore A.M.: Mechanistic aspects of xanthophyll cycle-dependent photoprotection in higher plant chloroplasts and leaves. - Physiol. Plantarum 99: 197-209, 1997. Go to original source...
  12. Gruszecki W.I., Grudzinski W., Gospodarek M. et al.: Xantho-phyll-induced aggregation of LHCII as a switch between light-harvesting and energy dissipation systems. - BBA-Bioenergetics 1757: 1504-1511, 2006. Go to original source...
  13. Hao J., Yue N., Zheng C.: Analysis of changes in anatomical characteristics and physiologic features of heteromorphic leaves in a desert tree, Populus euphratica. - Acta Physiol. Plant. 39: 160, 2017. Go to original source...
  14. He W., Zhang X., Dong M.: Gas exchange, leaf structure, and hydraulic features in relation to sex, shoot form, and leaf form in an evergreen shrub Sabina vulgaris in the semi-arid Mu Us Sandland in China. - Photosynthetica 41: 105-109, 2003. Go to original source...
  15. He W., Zhang X.: [Ecological significance of change of leaf form in Sabina vulgaris.] - Acta Bot. Yunnan. 23: 433-438, 2001. [In Chinese]
  16. He W., Zhang X.: Responses of an evergreen shrub Sabina vulgaris to soil water and nutrient shortages in the semi-arid Mu Us Sandland in China. - J. Arid Environ. 53: 307-316, 2003. Go to original source...
  17. Jahns P., Holzwarth A.R.: The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. - BBA-Bioenergetics 1817: 182-193, 2012.
  18. Kane M.E., Albert L.S.: Environmental and growth regulator effects on heterophylly and growth of Proserpinaca inter-media (Haloragaceae). - Aquat. Bot. 13: 73-85, 1982. Go to original source...
  19. Kang M.Y., Dong S., Huang X. et al.: Ecological regionalization of suitable trees, shrubs and herbages for vegetation restoration in the farming-pastoral zone of northern China. - Acta Bot. Sin. 45: 1157-1165, 2003.
  20. Ke B.: Role of carotenoids in photosynthesis. - In: Photosynthesis. Photobiochemistry and Photobiophysics. Pp. 229-250. Springer, Dordrecht 2003.
  21. Kitao M., Lei T.T., Koike T. et al.: Temperature response and photoinhibition investigated by chlorophyll fluorescence measurements for four distinct species of dipterocarp trees. - Physiol. Plantarum 109: 284-290, 2000. Go to original source...
  22. Kopsell D.A., Sams C.E., Morrow R.C.: Interaction of light quality and fertility on biomass, shoot pigmentation and xanthophyll cycle flux in Chinese kale. - J. Sci. Food Agr. 97: 911-917, 2017. Go to original source...
  23. Krause G.H., Jahns P.: Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characteri-zation and function. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence. Pp. 463-495. Springer, Dordrecht 2004. Go to original source...
  24. Lee D.W., Richards J.H.: Heteroblastic development in vines. -In: Putz F.E., Mooney H.A. (ed.): The Biology of Vines. Pp. 205-243. Cambridge University Press, Cambridge 1991. Go to original source...
  25. Lee P.C., Schmidt-Dannert C.: Metabolic engineering towards biotechnological production of carotenoids in micro-organisms. - Appl. Microbiol. Biot. 60: 1-11, 2002.
  26. Lichtenthaler H.K.: Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. - Method. Enzymol. 148: 350-382, 1987. Go to original source...
  27. Liu Q., Xu J., Liu Y. et al.: A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck). - J. Exp. Bot. 58: 4161-4171, 2007. Go to original source...
  28. Ma X., Song L., Yu W. et al.: Growth, physiological, and biochemical responses of Camptotheca acuminata seedlings to different light environments. - Front. Plant Sci. 6: 321, 2015. Go to original source...
  29. Miller P.M., Eddleman L.E., Miller J.M.: Juniperus occidentalis juvenile foliage: advantages and disadvantages for a stress-tolerant, invasive conifer. - Can. J. Forest Res. 25: 470-479, 1995. Go to original source...
  30. Mouget J.L., Tremblin G.: Suitability of the fluorescence moni- toring system (FMS, Hansatech) for measurement of photo-synthetic characteristics in algae. - Aquat. Bot. 74: 219-231, 2002. Go to original source...
  31. Murchie E.H., Horton P.: Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference. - Plant Cell Environ. 20: 438-448, 1997. Go to original source...
  32. Nakayama H., Sinha N.R., Kimura S.: How do plants and phyto-hormones accomplish heterophylly, leaf phenotypic plasticity, in response to environmental cues. - Front. Plant Sci. 8: 1717, 2017. Go to original source...
  33. Nicotra A.B., Leigh A., Boyce C.K. et al.: The evolution and functional significance of leaf shape in the angiosperms. - Funct. Plant Biol. 38: 535-552, 2011. Go to original source...
  34. Niyogi K.K., Björkman O., Grossman A.R.: The roles of specific xanthophylls in photoprotection. - P. Natl. Acad. Sci. USA 94: 14162-14167, 1997. Go to original source...
  35. Paine J.A., Shipton C.A., Chaggar S. et al.: Improving the nutritional value of Golden Rice through increased pro-vitamin A content. - Nat. Biotechnol. 23: 482-487, 2005. Go to original source...
  36. Palacio-López K., Beckage B., Scheiner S., Molofsky J.: The ubiquity of phenotypic plasticity in plants: a synthesis. - Ecol. Evol. 5: 3389-3400, 2015. Go to original source...
  37. Pastenes C., Pimentel P., Lillo J.: Leaf movements and photo-inhibition in relation to water stress in field-grown beans. - J. Exp. Bot. 56: 425-433, 2005.
  38. Porra R.J.: The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. - Photosynth. Res. 73: 149-156, 2002. Go to original source...
  39. Quevedo-Rojas A., García-Núñez C., Jerez-Rico M. et al.: Leaf acclimation strategies to contrasting light conditions in saplings of different shade tolerance in a tropical cloud forest. -Funct. Plant Biol. 45: 968-982, 2018. Go to original source...
  40. Ray T.S.: Cyclic heterophylly in Syngonium (Araceae). - Am. J. Bot. 74: 16-26, 1987. Go to original source...
  41. Ray T.S.: Metamorphosis in the Araceae. - Am. J. Bot. 77: 1599-1609, 1990. Go to original source...
  42. Ribeiro R.V., Machado E.C., Santos M.G., Oliveira R.F.: Seasonal and diurnal changes in photosynthetic limitation of young sweet orange trees. - Environ. Exp. Bot. 66: 203-211, 2009. Go to original source...
  43. Steinbauer M.J.: Oviposition preference and neonate performance of Mnesampela privata in relation to heterophylly in Euca-lyptus dunnii and E. globulus. - Agr. Forest Entomol. 4: 245-253, 2002. Go to original source...
  44. Tanaka-Oda A., Kenzo T., Kashimura S. et al.: Physiological and morphological differences in the heterophylly of Sabina vulgaris Ant. in the semi-arid environment of Mu Us Desert, Inner Mongolia, China. - J. Arid Environ. 74: 43-48, 2010. Go to original source...
  45. Thayer S.S., Björkman O.: Leaf xanthophyll content and composition in sun and shade determined by HPLC. - J. Photosynth. Res. 23: 331-343, 1990. Go to original source...
  46. Ueno M., Sae-Tang P., Kusama Y. et al.: Moderate heat stress stimulates repair of photosystem II during photoinhibition in Synechocystis sp. PCC 6803. - Plant Cell Physiol. 57: 2417-2426, 2016. Go to original source...
  47. Wang L., Dang H., Zhang G. et al.: [Distribution and biomass of natural Juniperus sabina community in China.] - Inner Mongolia Agric. Univ. 1: 37-45, 2014. [In Chinese]
  48. Wang T.L., Wang G.G., Innes J.L. et al.: ClimateAP: an application for dynamic local downscaling of historical and future climate data in Asia Pacific. - Front. Agr. Sci. Eng. 4: 448-458, 2017. Go to original source...
  49. Weger H.G., Silim S.N., Guy R.D.: Photosynthetic acclimation to low temperature by western red cedar seedlings. - Plant Cell Environ. 16: 711-717, 1993. Go to original source...
  50. Winn A.A.: The functional significance and fitness consequences of heterophylly. - Int. J. Plant Sci. 160: S113-S121, 1999. Go to original source...
  51. Xu D.: [Several problems in the research of plant light stress.] -Plant Physiol. Commun. 39: 493-495, 2003. [In Chinese]
  52. Yuan L., Wang C., Huang X. et al.: [The regulation of 24-epibrassinolide on AsA-GSH cycle and xanthophylls homeostasis in chloroplast of cucumber under Ca(NO3)2 stress.] - Acta Hortic. Sin. 44: 881-890, 2017. [In Chinese]
  53. Zakar T., Herman E., Vajravel S. et al.: Lipid and carotenoid cooperation-driven adaptation to light and temperature stress in Synechocystis sp. PCC6803. - BBA-Bioenergetics 1858: 337-350, 2017.
  54. Zhang J.L., Chen H.P., Li Y.L. et al.: [Comparison of water characteristics in the heterophylly of Sabina vulgaris.] - J. Arid Land Res. Environ. 32: 154-159, 2018. [In Chinese]
  55. Zhang J.L., Cheng D., Li Y.L. et al.: [Effect of light and water stress on photochemical efficiency and pigment composition of Sabina vulgaris seedlings.] - Chin. Bull. Bot. 3: 278-289, 2017. [In Chinese]
  56. Zhang J.L., Li Y.L., Pang M.L. et al.: [Comparison of drought resistance of anatomical structure in the heterophylly mecha-nism of Sabina vulgaris.] - Acta Bot. Boreal.-Occident. Sin. 37: 1756-1763, 2017. [In Chinese]
  57. Zhang S., Li Q., Ma K., Chen L.: Temperature-dependent gas exchange and stomatal/non-stomatal limitation to CO2 assimilation of Quercus liaotungensis under midday high irradiance. - Photosynthetica 39: 383-388, 2001. Go to original source...
  58. Zhang W., Xu A., Zhang R. et al.: [Review of soil classification and revision of China soil classification system.] - Sci. Agr. Sin. 47: 3214-3230, 2014. [In Chinese]