Abstract
Key message
In savin juniper, age and season can affect photosynthesis, chlorophyll fluorescence and photoprotective pigments. In spring, 2-year-old plants had more lutein than 5-year-olds, but the reverse occurred during summer and autumn.
Abstract
Savin juniper is an endemic evergreen shrub in the Mu Us Desert, where it establishes only with the protection of larger plants. Ultimately, established plants emerge into full sunlight as they grow. To explore how photoprotection responses change during this transition, a pot study was established under field conditions with three sunlight regimes (10%, 50% and 100% light transmittance) and two age cohorts (1- and 4-year-old rooted scions). To avoid potentially confounding effects of differences in leaf form, after one year we measured photosynthesis, chlorophyll fluorescence and foliar pigments of 2- and 5-year-old savin juniper on a monthly basis from April to October. For gas exchange and fluorescence variables, there were no interactions between cohort and sunlight except for intrinsic water-use efficiency in June; however, there were many interactions regarding pigment concentrations and ratios. Generally, 5-year-old plants had higher mean chlorophyll, total carotenoids, and chlorophyll a/b ratios than 2-year-old plants, but lower mean β-carotene/α-carotene ratio, zeaxanthin and lutein. Plants under brighter light had lower mean lutein. There were obvious changes in β-carotene/α-carotene, zeaxanthin and lutein in June, July and August, respectively. Under 100% sunlight, lutein concentration was higher in 2-year-old than 5-year-old plants from April to June, but this pattern reversed from July to October. The effects of age and season, in addition to the prevailing light regime, need to be considered when investigating the role of carotenoids in photoprotection.
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References
Anderson JM (1986) Photoregulation of the composition, function, and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136. https://doi.org/10.1146/annurev.pp.37.060186.000521
Athanasiou K, Dyson BC, Webster RE, Johnson GN (2010) Dynamic acclimation of photosynthesis increases plant fitness in changing environments. Plant Physiol 152:366–373. https://doi.org/10.1104/pp.109.149351
Avramov S, Miljković D, Klisarić NB, Živković U, Tarasjev A (2017) Ontogenetic plasticity of anatomical and ecophysiological traits and their correlations in Iris pumila plants grown in contrasting light conditions. Plant Spec Biol 32:392–402. https://doi.org/10.1111/1442-1984.12171
Bielczynski LW, Łącki MK, Hoefnagels I, Gambin A, Croce R (2017) Leaf and plant age affects photosynthetic performance and photoprotective capacity. Plant Physiol 175:1634–1648. https://doi.org/10.1104/pp.17.00904
Bond BJ (2000) Age-related changes in photosynthesis of woody plants. Trends Plant Sci 5:349–353. https://doi.org/10.1016/S1360-1385(00)01691-5
Chondrogiannis C, Grammatikopoulos G (2016) Photosynthesis in developing leaf of juveniles and adults of three Mediterranean species with different growth forms. Photosynth Res 130:427–444. https://doi.org/10.1007/s11120-016-0276-4
Choudhury NK, Behera RK (2001) Photoinhibition of photosynthesis: role of carotenoids in photoprotection of chloroplast constituents. Photosynthetica 39:481–488. https://doi.org/10.1023/A:1015647708360
Dall’Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. BMC Plant Biol 6:32. https://doi.org/10.1186/1471-2229-6-32
Demmig-Adams B (1998) Survey of thermal energy dissipation and pigment composition in sun and shade leaves. Plant Cell Physiol 39:474–482. https://doi.org/10.1093/oxfordjournals.pcp.a029394
Dörken VM, Lepetit B (2018) 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. https://doi.org/10.1111/pce.13213
Esteban R, Barrutia O, Artetxe U, Fernández-Marín B, Hernández A, García-Plazaola JI (2015) Internal and external factors affecting photosynthetic pigment composition in plants: a meta-analytical approach. New Phytol 206:268–280. https://doi.org/10.1111/nph.13186
Griffin JJ, Ranney TG, Pharr DM (2004) Photosynthesis, chlorophyll fluorescence, and carbohydrate content of Illicium taxa grown under varied irradiance. J Am Soc Hortic Sci 129:46–53. https://doi.org/10.21273/JASHS.129.1.0046
Grubb PJ (1998) A reassessment of the strategies of plants which cope with shortages of resources. Perspect Plant Ecol 1:3–31. https://doi.org/10.1078/1433-8319-00049
Hanba YT, Kogami H, Terashima I (2002) The effect of growth irradiance on leaf anatomy and photosynthesis in Acer species differing in light demand. Plant Cell Environ 25:1021–1030. https://doi.org/10.1046/j.1365-3040.2002.00881.x
Hansen U, Fiedler B, Rank B (2002) Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees Struct Funct 16:354–364. https://doi.org/10.1007/s00468-002-0163-9
He WM, Zhang XS (2003) 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. https://doi.org/10.1006/jare.2002.1051
He WM, Zhang XS, Dong M (2003) 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. https://doi.org/10.1023/A:1025872815480
Herbinger K, Then C, Löw M, Haberer K, Alexou M, Koch N, Remele K, Heerdt C, Grill D, Rennenberg H, Häberle KH (2005) Tree age dependence and within-canopy variation of leaf gas exchange and antioxidative defence in Fagus sylvatica under experimental free-air ozone exposure. Environ Pollut 137:476–482. https://doi.org/10.1016/j.envpol.2005.01.034
Ishida A, Yazaki K, Hoe AL (2005) Ontogenetic transition of leaf physiology and anatomy from seedlings to mature trees of a rain forest pioneer tree, Macaranga gigantea. Tree Physiol 25:513–522. https://doi.org/10.1093/treephys/25.5.513
Ishii Y, Sakamoto K, Yamanaka N, Wang L, Yoshikawa K (2006) Light acclimation of needle pigment composition in Sabina vulgaris seedlings under nurse plant canopy. J Arid Environ 67:403–415. https://doi.org/10.1016/j.jaridenv.2006.03.004
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. BBA Bioenerg 1817:182–193. https://doi.org/10.1016/j.bbabio.2011.04.012
Juárez-López FJ, Escudero A, Mediavilla S (2008) Ontogenetic changes in stomatal and biochemical limitations to photosynthesis of two co-occurring Mediterranean oaks differing in leaf life span. Tree Physiol 28:367–374. https://doi.org/10.1093/treephys/28.3.367
Kang MY, Dong SK, Huang XX, Xiong M, Chen H, Zhang XS (2003) 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. https://doi.org/researchgate.net/publication/286979024
Kenzo T, Ichie T, Watanabe Y, Yoneda R, Ninomiya I, Koike T (2006) Changes in photosynthesis and leaf characteristics with tree height in five dipterocarp species in a tropical rain forest. Tree Physiol 26:865–873. https://doi.org/10.1093/treephys/26.7.865
Lee HS (2001) Characterization of carotenoids in juice of red navel orange (cara cara). J Agr Food Chem 49:2563–2568. https://doi.org/10.1021/jf001313g
Levizou E, Petropoulou Y, Manetas Y (2004) Carotenoid composition of peridermal twigs does not fully conform to a shade acclimation hypothesis. Photosynthetica 42:591–596. https://doi.org/10.1007/S11099-005-0018-x
Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R et al (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21:1798–1812. https://doi.org/10.1105/tpc.109.066571
Li QS, Deng M, Xiong YS, Coombes A, Zhao W (2014) Morphological and photosynthetic response to high and low irradiance of Aeschynanthus longicaulis. Sci World J 2014:347461. https://doi.org/10.1155/2014/347461
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In: Methods in enzymology. Academic Press, pp 350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Mathur S, Jain L, Jajoo A (2018) Photosynthetic efficiency in sun and shade plants. Photosynthetica 56:354–365. https://doi.org/10.1007/s11099-018-0767-y
Matsubara S, Krause GH, Aranda J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Funct Plant Biol 36:20–36. https://doi.org/10.1071/FP08214
Mencuccini M, Martínez-Vilalta J, Hamid HA, Korakaki E, Vanderklein D (2007) Evidence for age- and size-mediated controls of tree growth from grafting studies. Tree Physiol 27:463–473. https://doi.org/10.1093/treephys/27.3.463
Morosinotto T, Caffarri S, Dall’Osto L, Bassi R (2003) Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol Plant 119:347–354. https://doi.org/10.1034/j.1399-3054.2003.00213.x
Munné-Bosch S, Alegre L (2002) Plant aging increases oxidative stress in chloroplasts. Planta 214:608–615. https://doi.org/10.1007/s004250100646
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998. https://doi.org/10.1093/jxb/ert208
Nan WG, Liu SQ, Yang SJ, Dong ZB, Yang JH, Shi WK (2020) Changes of Sabina vulgaris growth and of soil moisture in natural stands and plantations in semi-arid northern China. Glob Ecol Conserv 21:e00859. https://doi.org/10.1016/j.gecco.2019.e00859
Nichelmann L, Schulze M, Herppich WB, Bilger W (2016) A simple indicator for nondestructive estimation of the violaxanthin cycle pigment content in leaves. Photosynth Res 128:183–193. https://doi.org/10.1007/s11120-016-0218-1
Niinemets Ü (1997) Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species. Funct Ecol 11:518–531. https://doi.org/10.1046/j.1365-2435.1997.00109.x
Pinnola A, Bassi R (2018) Molecular mechanisms involved in plant photoprotection. Biochem Soc Trans 46:467–482. https://doi.org/10.1042/BST20170307
Porra RJ (2002) 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. https://doi.org/10.1023/A:1020470224740
Quevedo-Rojas A, García-Núñez C, Jerez-Rico M, Jaimez R, Schwarzkopf T (2018) Leaf acclimation strategies to contrasting light conditions in saplings of different shade tolerance in a tropical cloud forest. Funct Plant Biol 45:968–982. https://doi.org/10.1071/FP17308
Steppe K, Niinemets Ü, Teskey RO (2011). Tree size-and age-related changes in leaf physiology and their influence on carbon gain. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size-and age-related changes in tree structure and function. Springer, Dordrecht, pp 235–253. https://doi.org/10.1007/978-94-007-1242-3_9
Tanaka-Oda A, Kenzo T, Fukuda K (2009) Optimal germination condition by sulfuric acid pretreatment to improve seed germination of Sabina vulgaris Ant. J Forest Res 14:251–256. https://doi.org/10.1007/s10310-009-0129-5
Tefler A (2005) Too much light? How beta-carotene protects the photosystem II reaction centre. Photochem Photobiol Sci 4:950–956. https://doi.org/10.1039/b507888c
Tegischer K, Tausz M, Wieser G, Grill D (2002) Tree-and needle-age-dependent variations in antioxidants and photoprotective pigments in Norway spruce needles at the alpine timberline. Tree Physiol 22:591–596. https://doi.org/10.1093/treephys/22.8.591
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol S 39:237–257. https://doi.org/10.1146/annurev.ecolsys.39.110707.173506
Vanderklein D, Martínez-Vilalta J, Lee S, Mencuccini M (2007) Plant size, not age, regulates growth and gas exchange in grafted Scots pine trees. Tree Physiol 27:71–79. https://doi.org/10.1093/treephys/27.1.71
Wang LH, Dang HZ, Zhang GS, Dang GF, Feng W, Gaodabuxilatu, Wan JH (2014) Distribution and biomass of natural Juniperus sabina community in China. Inner Mongolia Agric Univ (Nat Sci Edn) 1:37–45. https://doi.org/10.16853/j.cnki.1009-3575.2014.01.008
Wang TL, Wang GG, Innes JL, Seely B, Chen BZ (2017) Climate AP: an application for dynamic local downscaling of historical and future climate data in Asia Pacific. Front Agr Sci Eng 4:448–458. https://doi.org/10.15302/J-FASE-2017172
Wieser G, Hecke K, Tausz M, Häberle KH, Grams TE, Matyssek R (2003) The influence of microclimate and tree age on the defense capacity of European beech (Fagus sylvatica L.) against oxidative stress. Ann Forest Sci 60:131–135. https://doi.org/10.1051/forest:2003005
Young AJ, Phillip D, Frank HA, Horton P, Frank HA (1997) The xanthophyll cycle and carotenoid mediated dissipation of excess excitation energy in photosynthesis. Pure Appl Chem 69:2125–2130. https://doi.org/10.1351/pac199769102125
Zhang WL, Xu AG, Zhang RL, Ji HJ (2014) Review of soil classification and revision of China soil classification system. Sci Agr Sin 47:3214–3230. https://doi.org/10.3864/j.issn.0578-1752.2014.16.009
Zhang W, Zhao J, Pan FJ, Li DJ, Chen HS, Wang KL (2015) Changes in nitrogen and phosphorus limitation during secondary succession in a karst region in southwest China. Plant Soil 391:77–91. https://doi.org/10.1007/s11104-015-2406-8
Zhang JL, Cheng D, Li YL, Chen HP (2017) Effect of light and water stress on photochemical efficiency and pigment composition of Sabina vulgaris seedlings. Chinese Bull Bot 52:278–289
Zhang JL, Xu XH, Li XG, Li YL, Guy RD, Chen HP (2019) Photoprotection in heteromorphic leaves of savin Juniper (Juniperus sabina L.). Photosynthetica 57:780–787. https://doi.org/10.32615/ps.2019.097
Zhang JL, Li XG, Xu XH, Chen HP, Li YL, Guy RD (2021). Leaf morphology, photosynthesis and pigments change with age and sunlight in savin juniper. Plant Biol https://doi.org/10.1111/plb.13256
Acknowledgements
We thank Ai-Hua Yan, Bing-Xiang Liu, Ke-Jiu Du, Hong-Bo Cao and Min-Sheng Yang for laboratory and technical assistance; and Feng Mu, Xin Lin, An-Ning Wang, Da Cheng, Ge-Chang Liu and Zi-Min Cheng for experiment assistance.
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This research was supported by the Natural Science Foundation of Hebei Province (C2011204096), the Doctoral Student Innovation Capability Promotion Project of Hebei Agricultural University, China Scholarship Council and the Key Laboratory of Forest Tree Germplasm Resources and Forest Conservation of Hebei Province.
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JLZ and YLL designed the study. JLZ, XGL, XHX and HPC conducted the field and laboratory research. JLZ and HPC organized and analyzed the data. JLZ, YLL and RDG interpreted the data and wrote the manuscript. All authors provided intellectual input and edited/approved the manuscript.
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Zhang, JL., Li, XG., Xu, XH. et al. Seasonal progression of photoprotection responses in different aged savin juniper plants under shade and sun. Trees 35, 1601–1612 (2021). https://doi.org/10.1007/s00468-021-02139-2
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DOI: https://doi.org/10.1007/s00468-021-02139-2