Abstract
Liquidambar formosana Hance is an attractive landscape tree species because its leaves gradually change from green to red, purple or orange in autumn. In this study, the red variety of L. formosana was used to establish a quantitative model of leaf color. Physiological changes in leaf color, pigment levels, enzyme activity, photosynthetic fluorescence characteristics and chloroplast ultrastructure were monitored. The relationship between leaf color and physiological structure indices was quantitatively analyzed to systematically explore the mechanisms behind leaf color. Our data showed that with a decrease in external temperatures, chloroplast numbers and sizes gradually decreased, thylakoid membranes became distorted, and chlorophyll synthesis was blocked and gradually decreased. As a result, chloroplast membranes could not be biosynthesized normally; net photosynthesis, maximum and actual photochemical efficiency, and rate of electron transfer decreased rapidly. Excess light energy caused leaf photoinhibition. With intensification of photoinhibition, leaves protected themselves using two mechanisms. In the first, anthocyanin synthesis was promoted by increasing chalcone isomerase and flavonoid glycosyltransferase activities and soluble sugar content so as to increase anthocyanin to filter light and eliminate reactive oxygen species to reduce photoinhibition. In the second, excessive light energy was consumed in the form of heat energy by increasing the non-photochemical quenching coefficient. These processes tuned the leaves red.
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References
Archetti M (2000) The origin of autumn colours by coevolution. J Theor Biol 205:625–630
Becker C, Klaering HP, Kroh LW, Krumbein A (2014) Cool-cultivated red leaf lettuce accumulates cyanidin-3-O-(6-O-malonyl)-glucoside and caffeoylmalic acid. Food Chem 146:404–411
Bertamini M, Nedunchezhian N (2003) Photoinhibition of photosynthesis in mature and young leaves of grapevine (Vitis vinifera L.). Plant Sci 164(4):635–644
Boo HO, Heo BG, Gorinstein S, Chon SU (2011) Positive effects of temperature and growth conditions on enzymatic and antioxidant status in lettuce plants. Plant Sci 181(4):479–484
Cooney LJ, Klink JW, Hughes NM, Perry NB, Schaefer HM, Menzies IJ, Gould KS (2012) Red leaf margins indicate increased polygodial content and function as visual signals to reduce herbivory in Pseudowintera colorata. New Phytol 194:488–497
Eris A, Gulen H, Barut E, Cansev A (2007) Annual patterns of total soluble sugars and proteins related to cold hardiness in olive (Olea europaea L. ’Gemlik’). J Hortic Sci Biotech 82(4):597–604
Esteban R, Fernández-Marín B, Becerril JM, García-Plazaola JI (2008) Photoprotective implications of leaf variegation in E. dens-canis L. and P. officinalis L. J Plant Physiol 165(12):1255–1263
Feild TS, Lee DW, Holbrook NM (2001) Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol 127(2):566–574
Feng S, Chen X, Zhang Y, Wang Y, Song Y, Chen XL, Li X, Li M (2011) Differential expression of proteins in red pear following fruit bagging treatment. Protein J 30:194–200
Gu C, Liao L, Zhou H, Wang L, Deng XB, Han YP (2015) Constitutive activation of an anthocyanin regulatory gene pcMYB10.6 is related to red coloration in purple-foliage plum. PLoS ONE 10(8):81–88
Hanke G, Mulo P (2013) Plant type ferredoxins and ferredoxin-dependent metabolism. Plant Cell Environ 36(6):1071–1084
Hiiner NPA, Oquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230
Hoch WA, Zeldin EL, McCown BH (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21(1):1–8
Hughes NM (2011) Winter leaf reddening in ‘Evergreen’ species. New Phytol 190:573–581
Hughes NM, Morley CB, Smith WK (2007) Seasonal photosynthesis and anthocyanin production in 10 broadleaf evergreen species. Funct Plant Biol 34:1072–1079
Jiang X, Peng J, Jia M, Liu Y, Guo L, Gao R (2016) Relationship between leaf reddening, ROS and antioxidants in Buxus microphylla during overwintering. Acta Physiol Plant 38(8):199
Ju ZG, Yuan YB, Liu CL, Xin SH (1995) Relationship among phenylalanine ammonia-lyase activity, simple phenol concentrations and anthocyanin accumulation in apple. Sci Hortic 61:215–226
Ju ZG, Liu CL, Yuan YB, Wang YZ, Liu GS (1999) Coloration potential, anthocyanin accumulation, and enzyme activity in fruit of commercial apple cultivars and their F1 progeny. Sci Hortic 79:39–50
Junker LV, Ensminger I (2016) Relationship between leaf optical properties, chlorophyll fluorescence and pigment changes in senescing Acer saccharum leaves. Tree Physiol 36(6):694–711
Keskitalo J, Bergquist G, Gardeström P, Jansson S (2005) A cellular timetable of autumn senescence. Plant Physiol 139(4):1635–1648
Kobayashi S, Ishimaru M, Ding CK, Yakushiji H, Goto N (2001) Comparison of UDP-glucose: flavonoid 3-O-glucosyltransferase (UFGT) gene sequences between white grapes (Vitis vinifera) and their sports with red skin. Plant Sci 160(3):543–550
Kovinich N, Kayanja G, Chanoca A, Riedl K, Otegui MS, Grotewold E (2014) Not all anthocyanins are born equal: distinct patterns induced by stress in Arabidopsis. Planta 240:931–940
Kumar P, Sharma SD, Sharma NC, Devi M (2015) The path coefficient analysis of yield components for leaf nutrient concentrations in Mango (Mangifera indica L.) under rainfed agroclimatic conditions of north-west Himalaya. Sci Hortic Amsterdam 190:31–35
Kytridis VP, Manetas Y (2006) Mesophyll versus epidermal anthocyanins as potential in vivo antioxidants: evidence linking the putative antioxidant role to the proximity of oxy-radical source. J Exp Bot 57:2203–2210
Lee DW, Keefe J, Holbrook NM, Field TS (2003) Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecol Res 18(6):677–694
Li CF, Xu YX, Ma JQ, Jin JQ, Huang DJ, Yao MZ, Ma CL, Chen L (2016) Biochemical and transcriptomic analyses reveal different metabolite biosynthesis profiles among three color and developmental stages in ‘Anji Baicha’ (Camellia sinensis). BMC Plant Biol 16(1):195–212
Li Y, Sun Y, Jiang J, Liu J (2019) Spectroscopic determination of leaf chlorophyll content and color for genetic selection on Sassafras tzumu. Plant Methods 15:73
Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf in different solvents. Biochem Soc T 11(5):591–592
Lister CE, Lancaster JE (1996) Developmental changes in enzymes of flavonoid biosynthesis in the skins of red and green apple cultivars. J Sci Food Agric 71:313–320
Lister CE, Lancaster JE, Walker JRL (1996) Phenylalanine ammonia-lyase (PAL) activity and its relationship to anthocyanin and flavonoid levels in New Zealand-grown apple cultivars. J Am Soc Hortic Sci 121(2):281–285
Liu R, Yuan QQ, Yuan XP, Zhou XH (2017) The relationship with change of pigment content in leaves of different Liquidambar formosana families and change of leaf color. South China for Sci 45(4):46–49
Liu Z, Gao J, Gao F, Liu P, Zhao B, Zhang J (2018) Photosynthetic characteristics and chloroplast ultrastructure of summer maize response to different nitrogen supplies. Front Plant Sci 9:576
Luo Z, Guan H, Zhang X, Liu N (2017) Photosynthetic capacity of senescent leaves for a subtropical broadleaf deciduous tree species Liquidambar formosana Hance. Sci Rep 7:6323
Ma D, Reichelt M, Yoshida K, Gershenzon J, Constabel CP (2018) Two R2R3-MYB proteins are broad repressors of flavonoid and phenylpropanoid metabolism in poplar. Plant J 96:949–965
Menzies IJ, Youard LW, Lord JM, Perry NB, Schaefer HM, Gould KS (2016) Leaf colour polymorphisms: a balance between plant defence and photosynthesis. J Ecol 104(1):104–113
Moustaka J, Panteris E, Adamakis IDS, Tanou G, Giannakoula A, Eleftheriou EP, Moustakas M (2018) High anthocyanin accumulation in poinsettia leaves is accompanied by thylakoid membrane unstacking, acting as a photoprotective mechanism, to prevent ROS formation. Environ Exp Bot 154:44–55
Moustaka J, Tanou G, Giannakoula A, Adamakis IDS, Panteris E, Eleftheriou EP, Moustakas M (2020) Anthocyanin accumulation in poinsettia leaves and its functional role in photo-oxidative stress. Environ Exp Bot 175:104065
Muller P (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125(4):1558–1566
Murakami PF, Schaberg PG, Shane JB (2008) Stem girdling manipulates leaf sugar concentrations and anthocyanin expression in sugar maple trees during autumn. Tree Physiol 28(10):1467–1473
Nishihara M, Nakatsuka T, Yamamura S (2005) Flavonoid components and flower color change in transgenic tobacco plants by suppression of chalcone isomerase gene. Febs Lett 579(27):6074–6087
Noda N, Yoshioka S, Kishimoto S, Nakayama M, Douzono M, Tanaka Y, Aida R (2017) Generation of blue chrysanthemums by anthocyanin B-ring hydroxylation and glucosylation and its coloration mechanism. Sci Adv 3(7):e1602785
Novak AB, Short FT (2011) UV-B induces leaf reddening and supports photosynthesis in the seagrass Thalassia testudinum. J Exp Mar Biol Ecol 409:136–142
Osamu A (1988) Photoregulation of anthocyanin synthesis in apple fruit under UV-B and red light. Plant Cell Physiol 8:1385–1389
Paul M, Pellny T, Goddijn O (2001) Enhancing photosynthesis with sugar signals. Trends Plant Sci 6(5):197–200
Sarker U, Oba S (2018) Augmentation of leaf color parameters, pigments, vitamins, phenolic acids, flavonoids and antioxidant activity in selected Amaranthus tricolor under salinity stress. Sci Rep 8:12349
Shaked-Sachray L, Weiss D, Reuveni M, Nissim-Levi A, Oren-Shamir M (2002) Increased anthocyanin accumulation in aster flowers at elevated temperatures due to magnesium treatment. Physiol Plantarum 114(4):559–565
Sherwin HW, Farrant JM (1998) Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regul 24:203–210
Shi J, Zhang X, Zhang Y, Lin X, Li B, Chen Z (2020) Integrated metabolomic and transcriptomic strategies to understand the effects of dark stress on tea callus flavonoid biosynthesis. Plant Physiol Bioch 155:549–559
Sinkkonen A, Somerkoski E, Paaso U, Holopainen JK, Rousi M, Mikola J (2012) Genotypic variation in yellow autumn leaf colours explains aphid load in silver birch. New Phytol 195(2):461–469
Snider JL, Chastain DR, Meeks CD, Collins GD, Sorensen RB, Byrd SA, Perry CD (2015) Predawn respiration rates during flowering are highly predictive of yield response in Gossypium hirsutum when yield variability is water-induced. J Plant Physiol 183:114–120
Sperdouli I, Moustakas M (2012) Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. J Plant Physiol 169(6):577–585
Stiles EA, Cech NB, Dee SM, Lacey EP (2007) Temperature-sensitive anthocyanin production in flowers of Plantago lanceolata. Physiol Plantarum 129(4):756–765
Sun R, Lin F, Huang P, Zheng Y (2016) Moderate genetic diversity and genetic differentiation in the relict tree Liquidambar formosana Hance revealed by genic simple sequence repeat markers. Front Plant Sci 7:1411
Wang HC, Huang XM, Hu GB, Huang HB (2004) Studies on the relationship between anthocyanin biosynthesis and related enzymes in Litchi Pericarp. Sci Agr Sin 37(12):2028–2032
Wang DX, Sun HJ, De YJ, Shi JX (2019) Change of leaf color of Liquidambar formosana seedlings under different light quality treatments. For Res 32(4):158–164
Xu ZS, Yang QQ, Feng K, Xiong AS (2019) Changing carrot color: insertions in DcMYB7 alter the regulation of anthocyanin biosynthesis and modification. Plant Physiol 181:195–207
Zeliou K, Manetas Y, Petropoulou Y (2009) Transient winter leaf reddening in Cistus creticus characterizes weak (stress-sensitive) individuals, yet anthocyanins cannot alleviate the adverse effects on photosynthesis. J Exp Bot 60(11):3031–3042
Zhang H, Li J, Yoo JH (2006) Rice Chlorina-1 and Chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Mol Biol 62(3):325–337
Zhang KM, Wang XM, Cui JX, Ogweno JO, Shi K, Zhou YH, Yu JQ (2011) Characteristics of gas exchange and chlorophyll fluorescence in red and green leaves of Begonia semperflorens. Biol Plantarum 55(2):361–364
Zhang YJ, Yang QY, Lee DW, Goldstein G, Cao KF (2013) Extended leaf senescence promotes carbon gain and nutrient resorption: importance of maintaining winter photosynthesis in subtropical forests. Oecologia 173(3):721–730
Zhao MH, Li X, Zhang XX, Zhang H, Zhao XY (2020) Mutation mechanism of leaf color in plants: a review. Forests 11(8):851
Zhu HF, Xf Li, Zhai W, Liu Y, Gao QQ, Liu JP, Li R, Chen HY, Zhu Y (2017) Effects of low light on photosynthetic properties, antioxidant enzyme activity, and anthocyanin accumulation in purple pak-choi (Brassica campestris ssp. Chinensis Makino). PLoS ONE 12(6):e0179305
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Project funding: This work was supported by the Fundamental Research Funds for Guangxi Zhuang Autonomous Region Forestry Research Institute (No. Linke 201809) and Guangxi Forestry Science and Technology Promotion Demonstration Project (No. 26 Guilin Research 2021).
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Corresponding editor: Yanbo Hu.
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Yin, G., Wang, Y., Xiao, Y. et al. Relationships between leaf color changes, pigment levels, enzyme activity, photosynthetic fluorescence characteristics and chloroplast ultrastructure of Liquidambar formosana Hance. J. For. Res. 33, 1559–1572 (2022). https://doi.org/10.1007/s11676-021-01441-6
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DOI: https://doi.org/10.1007/s11676-021-01441-6