The temporal changes of pigments content and key enzyme activities during autumnal turning period of Pistacia chinensis bunge

yichen wang

College of Forestry, Shanxi Agricultural University, Taigu 030801, China
https://orcid.org/0009-0007-3486-7963

Xiuyun Yang

College of Forestry, Shanxi Agricultural University, Taigu 030801, China
https://orcid.org/0000-0003-2799-0094

Xiaogang Wu

College of urban and rural construction, Shanxi Agricultural University, Taigu 030801, China
https://orcid.org/0000-0003-2898-9423

Shuhui Du

College of Forestry, Shanxi Agricultural University, Taigu 030801, China
https://orcid.org/0000-0002-5067-3591

Meiling Han

College of urban and rural construction, Shanxi Agricultural University, Taigu 030801, China
https://orcid.org/0000-0003-2746-3438


Abstract

In this study, the temporal regularity of pigments and key enzyme intermediates of Pistacia chinensis Bunge in the color-changing period was investigated to provide a theoretical basis for exploring the mechanism of leaf discoloration. The pigment content and activities of key enzymes of P. chinensis during leaf discoloration were investigated. The correlation between leaf discoloration and environmental factors (temperature, relative humidity, light) was also analyzed. During the color change, the chlorophyll content decreased, while no significant change in the carotenoid content was observed. The anthocyanin content significantly increased in the middle of the period of color change. The ratios of carotenoids/chlorophyll and anthocyanins/chlorophyll showed an upward trend during the period of color change. The lightness parameter (L) and hue parameter (B) of P. chinensis Bunge leaves showed a fluctuating tendency, reaching the highest value at the beginning of color conversion. The hue parameter (A) showed an upward trend at the color conversion stage. The 5-aminolevulinic acid (ALA) and porphobilinogen (PBG) values showed an upward-downward-upward trend. The contents of ALA and PBG at the end of the color transformation were 2.01 times and 2.88 times higher than those at the beginning. The activity of phenylalaninammo-nialyase increased during the color change period. Chalcone isomerase and chalcone synthase first increased, then declined, reaching their highest level in the middle of color conversion, 261.0 u/g and 157.3 u/g, respectively. Although the activities of both enzymes declined at the end of the color conversion, they were higher than at the beginning of the color change. Anthocyanin content was negatively correlated with temperature, relative humidity, day length, and chalcone isomerase, whereas it was positively correlated with phenylalaninammo-nialyase. The results revealed the reasons for the discoloration of P. chinensis leaves in autumn and thus should be considered when exploring the mechanism of color-changing plants and performing color-changing plant applications.

Keywords:

color change period, essential enzymes, leaf color parameters, pigment, Pistacia chinensis Bung

Bwcker, C., Klaering, H.P., Kroh, L.W., Krumbein, A. (2014). Cool-cultivated red leaf lettuce accumulates cyaniding-3-o-(6″-o-malonyl)-glucoside and caffeoylmalic acid. Food Chem., 146, 404–411. https://doi.org/10.1016/j.foodchem.2013.09.061 DOI: https://doi.org/10.1016/j.foodchem.2013.09.061

Cai, Y.P. (2017). Experimental guidance of plant physiology. China Agric. University Press, Beijing, China [in Chinese].

Chalker-Scott, L. (1999). Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 70, 1–9. https://doi.org/10.1111/j.1751-1097.1999.tb01944.x DOI: https://doi.org/10.1111/j.1751-1097.1999.tb01944.x

Chen, J.R. (2008). The physiological mechanism of leaf color change and nitrogen regulation on rice. College of Agricultural, Henan Agricultural University [in Chinese].

Chen, J.W., Shen, C.D., Jia, Y.F, Chen, S., Chai, M.L. (2010). Physiological changes of Japanese maple (Acer Palmatum Thunb) leaves during color-changing period. J. Nuclear Agric. Sci. 24, 171–175 [in Chinese]. https://doi.org/10.15889/j.issn.1002-1302.2018.22.026

Cui, H.R., Xia, Y.W., Gao, M.W. (2001). Effects of temperature on leaf color and chlorophyll biosynthesis of rice mutantw1. Acta Agric. Nucleatae Sinica, 15, 269–273 [in Chinese]. https://doi.org/10.3969/j.issn.1000-8551.2001.05.003

Dai, X.H., Zhou, L.Y., Hou, L.Q. (2015). Relationship between color variation and pigments in Loropetalum chinense var. rubrum leaves under different. J. Northeast For. Univ., 43, 62–65 [in Chinese]. https://doi.org/10.13759/j.cnki.dlxb.20150120.012.

Davies, K.M., Albert, N.W., Schwinn, K.E. (2012). From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Funct. Plant Biol., 39, 619–638. https://doi.org/10.1071/FP12195 DOI: https://doi.org/10.1071/FP12195

Fei, F., Wang, H.Y., Tang, Q.R. (2008). [Study on the impact of temperature on loropetalum Chinese var. rubrum leaves color]. Journal of Hunan Institute of Science and Technology (Natural Sciences) 21, 88-90 [in Chenese]. https://doi.org/10.3969/j.issn.1672-5298.2008.02.028

Feng, L.J., Yuan, Z.H., Yi, Y.L., Zhao, X.Q., Xu, X.K., Xu, R., Li, Z.F. (2009). Anthocyanin content and the relevant enzymes activities during leaf color changing of two Acer species. Scientia Silvae Sinicae, 45, 56–60 [in Chinese], https://doi.org/10.3321/j.issn:1001-7488.2009.08.010

Ge, C.L., Huang, C.H., Xu, X.B. (2012). Research on anthocyanins biosynthesis in fruit. Acta Horticulturae Sinica, 39, 1655–1664 [in Chinese]. https://doi.org/10.16420/j.issn.0513-353x.2012.09.002

Gu, C., Liao, L., Zhou, H., Wang, L., Deng, X.B., Han, Y.P. (2015). Constitutive activation of an anthocyanin regulatory gene PcMYB10.6 is related to red coloration in purple-foliage plum. PLOS One 10:e0135159. DOI: https://doi.org/10.1371/journal.pone.0135159

Guo, H.H., Liu, Y., Yao, F., Li, S.A., Song, X.H. (2017). Relationship between pigment contents and leaf color parameters of Pistacia chinensis Bunge of different provenances in autumn. Acta Botanica Boreali-Occidentalia Sinica, 37, 2003–2009 [in Chinese]. https://doi.org/10.7606/j.issn.1000-4025.2017.10.2003

Guo, Y.L. (2013). Preliminary study on the chromogenic mechanism of leaf in red-leaf poplars. Forestry Institute, Sichuan Agricultural University [in Chinese].

He, B., Liu, L.L., Zhang, W.W., Wan, J.M. (2006). Plant leaf color mutants. Plant Physiol. Commun., 42, 1–9.

Hong, L., Pang, S.L., Zhu, C.F., Zhang, L. (2012). [Analysis of pigment content in leaves of Acer negundo at different color stages. J. Heilongjiang Vocat. Inst. Ecol. Eng., 25, 42–44 [in Chinese].

Hong, L., Wang, J.G., Gong, S.F. (2010). Progress in color changes and its influencing factors of color leaf plant. J. Northeast Agric. Univ., 41, 152–156 [in Chinese]. https://doi.org/10.3969/j.issn.1005-9369.2010.06.030

Hu, J.J., Shen, X., Li, X.F., Zhao, J., Li, X., Zhang, X.X. (2010). Relationships of leaf color changes and soluble sugars and mineral elements in leaves of Pistacia chinensis in autumn. Scientia Silvae Sinicae, 46, 80–86 [in Chinese]. https://doi.org/10.11707/j.1001-7488.20100214

Huang, X.Q., Zhao, H.X., Dong, C.L., Sun, Y.Y., Wang, P.R., Deng, X.J. (2005). Chlorophyll-deficit rice mutants and their research advances in biology. Acta Bot. Boreali-Occidentalia Sinica, 25, l685–1691 [in Chinese]. https://doi.org/10.3321/j.issn:1000-4025.2005.08.037

Jiang, J.B., Liang, L., Zhang, T.J., Li, Y.J., Chen, X.H. (2019). Seasonal dynamic of physiological characteristics of pink Davidia involucrate. Acta Bot. Boreali-Occidentalia Sinica 39, 2019–2027 [in Chinese]. https://doi.org/10.7606/j.issn.1000-4025.2019.11.2019

Jiang, M., Cao, J.S. (2007). Chalcone Synthase Gene. Chinese J. Cell Biol., 29, 525–529 [in Chinese]. https://doi.org/10.3969/j.issn.1674-7666.2007.04.014

Jiang, W.B., Zhuang, M., Han, H.Z., Dai, M.S., Hua, G.P. (2005). Progress on color emerging mechanism and photosynthetic characteristics of colored-leaf plants. Acta Hortic. Sinica, 32, 352–358 [in Chinese]. https://doi.org/10.3321/j.issn:0513-353X.2005.02.042

Lev-yadun, S., Yamazaki, K., Holopainen, J.K., Sinkkonen, A. (2012). Spring versus autumn leaf colours: evidence for different selective agents and evolution in various species and floras. Flora, 207, 80–85, https://doi.org/10.1016/j.flora.2011.10.007 DOI: https://doi.org/10.1016/j.flora.2011.10.007

Li, C.F., Xu, Y.X., Ma, J.Q., Jin, J.Q., Huang, D.J., Yao, M.Z., Ma, C.L., Chen, L. (2016). Biochemical and transcriptomic analyses reveal different metabolite biosynthesisprofiles among three color and developmental stages in‘Anji Baicha’ (Camellia sinensis). Bmc Plant Biol., 16, 195–196. https://doi.org/10.1186/s12870-016-0885-2 DOI: https://doi.org/10.1186/s12870-016-0885-2

Li, W.X., Yang, S.B., He, Z.C., Jin B. (2017a). Research advances in the regulatory mechanisms of leaf coloration]. Acta Hortic. Sinica, 44, 1811–1824 [in Chinese]. https://doi.org/10.16420/j.issn.0513-353x.2017-0167Li, L., Zhang, S.N., Liu, Y.M., Liu, Y.M. (2017b). Lab model based analysis on physiological factors affecting color of Acer rubrum L. J. Northwest A & F Univ., 45, 87–94 [in Chinese]. https://doi.org/10.13207/j.cnki.jnwafu.2017.09.012

Li, X.F., Zhang, Z.L. (2016). Experimental guidance of plant physiology]. Higher Education Press, Beijing, China [in Chinese].

Li, Y.Y. (2012). Anthurium flowers PAL gene cloning and anthocyanin content. College of Horticulture and Landscape Architecture, University of Hainan.

Liu, X.D., Yu, J. (2011). Extraction of anthocyanin from Physocarpus pulifolius ‘Diabolo’ and its stability. J. Northeast For. Univ., 39 [in Chinese]. https://doi.org/10.3969/j.issn.1000-5382.2011.02.012

Luo, L. (2020). Preliminary study on the mechanism of leaf color variation in anthurium andraeanum mutant based on transcriptome analysis. Golden Mantis Institute of Architecture, Soochow University [in Chinese].

Luo, Y.L., Zhang, G.B., Zhang, A.M. (2013). Comparison of leaf structures in the green and yellow parts of Liriodendron tulipifera ‘Aureo marginatum’. Bull. Bot. Res., 33, 282–286 [in Chinese]. https://doi.org/10.7525/j.issn.1673-5102.2013.03.006

Nie, Q.J., Shi, B.S., Meng, Z., Liu, D.Y., Lou, L.N. (2008). The enzyme activities, pigment and inclusion contents in different leaves color of Cotinus coggygria ‘Royal Purple’ in autumn. Bull. Bot. Res., 28, 599–602 [in Chinese]. https://doi.org/10.7525/j.issn.1673-5102.2008.05.020

Ougham, H.J., Morris, P., Thomas, H. (2005). The colors of autumn leaves as symptoms of cellular recycling and defenses against environmental stresses. Curr. Top. Dev. Biol., 66, 135–160. https://doi.org/10.1016/S0070-2153(05)66004-8 DOI: https://doi.org/10.1016/S0070-2153(05)66004-8

Schaberg, P.G., Murakami, P.F., Butnor, J.R., Hawley, G.J. (2017). Experimental branch cooling increases foliar sugar and anthocyanin concentrations in sugar maple at the end of the growing season. Can. J. For. Res., 47, 696–701. https://doi.org/10.1139/cjfr-2016-0534 DOI: https://doi.org/10.1139/cjfr-2016-0534

Shi, S.C., Gao, Y.K., Zhang, X.H., Sun, J.Q., Zhao, L.L., Wang, Y. (2011). Progress on plant genes involved in biosynthetic pathway of anthocyanins. Bull. Bot. Res., 31, 633–640 [in Chinese]. https://doi.org/10.7525/j.issn.1673-5102.2011.05.020

Sun, Y., Li, P. (2015). Studied on contents of pigments in the leaves of several excellent color-leaved plants in autumn. Shandong For. Sci. Technol., 45, 1–5 [in Chinese]. https://doi.org/10.3969/j.issn.1002-2724.2015.05.001 DOI: https://doi.org/10.1016/j.fop.2015.10.033

Tai, D., Tian, J., Zhang, J., Song, T.T., Yao, Y.C. (2014). A malus crabapple chalcone synthase gene, McCHS, regulates red petal color and flavonoid biosynthesis. Plos One 9:e110570 [in Chinese]. https://doi.org/10.1371/journal.pone.0110570 DOI: https://doi.org/10.1371/journal.pone.0110570

Tang, Q.R., Chen, D.F., Chen, Y.Y., Zhang, H.Z., Zhou, P.H. (2006). Changes of physiology and biochemistry during leaf color transformation in loropetalum chinense var. rubrum. Sci. Silvae Sinicae, 42, 111–115 [in Chinese]. https://doi.org/10.3321/j.issn:1001-7488.2006.02.019

Wang, B.L., Guo, G.L., Wang, P.H. (1996). Changes of chlorophyll metabolism during the albinic stage of a wheatmutant Acta Bot. Sinica, 38, 557–562.

Wang, F., Wang, X.J., Zhao, S.N., Yan, J.R., Bu, X., Zhang, Y., Liu, Y.F., Xu, T., Qi, M.F., Qi, H.Y., Li, T.L. (2020). Light regulation of anthocyanin biosynthesis in horticultural crops. Sci. Agric. Sinica, 53, 4904–4917 [in Chinese]. https://doi.org/10.3864/j.issn.0578-1752.2020.23.015

Wang, L.J., Ni, D.A., Ye, X.F., Xia, Z.A., Liu, J.R. (1997). Determination of δ-aminolevulinic acid in plant leaves. Plant Physiol. Commun., 35, 439–441 [in Chinese].

Wang, Q.J., Li, X.L., Wang, L., Sun, F.Y., Shen, X. (2008). Dynamic changes of anthocyanin and the relevant biosynthesis enzymes in Padus virginiana ‘Schubert’ leaves. Sci. Silvae Sinicae, 44, 45–49 [in Chinese]. https://doi.org/10.3321/j.issn:1001-7488.2008.03.011

Wu, Y.F., Yu, P., Zhu, Z.L. (2016). Physiological and biochemical characteristics of Carpinus turczaninowii leaves with different colors in spring. J. Northwest A&F Univ., 44, 120-126+132, https://doi.org/10.13207/j.cnki.jnwafu.2016.05.016

Xu, P.Z., Li, Y., Yuan, P., Zhang, H.Y., Peng, H., Lin, H.H., Wang, X.D., Wu, X.J. (2006). Studies of photosystem complexes and chlorophyll synthesis in chlorophyll-deficient rice mutant W1. Scientia Agricultura Sinica, 39, 1299–1305 [in Chinese]. https://doi.org/10.3321/j.issn:0578-1752.2006.07.001

Yuan, M., Xu, M.Y., Yuan, S., Chen, Y.E., Du, J.B., Xu, F., Zhang, Z.W., Guo, Z.C., Zhao, Z.Y., Lin, H.H. (2010). Light regulation to chlorophyll synthesis and plastid development of the chlorophyll-less golden-leaf privet. J. Integr. Plant Biol., 52, 809–816. https://doi.org/10.1111/j.1744-7909.2010.00979.x DOI: https://doi.org/10.1111/j.1744-7909.2010.00979.x

Zhang, M., Huang, L.B., Zhou, P., Qian, M., Dou, Q.Q. (2015). Physiological and biochemical changes in Zelkova serrata leaves during leaf color transformation in autumn. Sci. Silvae Sinicae, 51, 44–51 [in Chinese]. https://doi.org/10.11707/j.1001-7488.20150806

Zhang, Y.P., Jin, X.L., Zeng, Y., Wang, X.L. (2017). Chemicals on plant leaf color regulations and research progress of leaf color. Northern Hortic., 14, 180–184 [in Chinese]. https://doi.org/10.11937/bfyy.20164595

Zhou, F.J., Wang, Y.Q., Chen, Y.Q. (2008). Progress of plant chalcone isomerase (summary). J. Hebei Normal Univ. Sci. Technol., 22, 73–77 [in Chinese]. https://doi.org/10.3969/j.issn.1672-7983.2008.01.015 DOI: https://doi.org/10.1007/s11596-008-0118-5

Zhu, Z.X., Lu, Y.Q. (2016). Plant color mutants and the anthocyanin pathway. Chinese Bull. Bot., 51, 107–119 [in Chinese]. https://doi.org/10.11983/CBB15059

Zhuo, Q.M., Ding, Y.F., Yu, H., Zhu, G.Q. (2018). Physiological characters of Euonymus europaea leaves during the color-Changing period in autumn and winter. Acta Bot. Boreali-Occidentalia Sinica, 38, 1072–1079 [in Chinese]. https://doi.org/10.7606/j.issn.1000-4025.2018.06.1072

Download

Published
2023-06-30



yichen wang 
College of Forestry, Shanxi Agricultural University, Taigu 030801, China https://orcid.org/0009-0007-3486-7963
Xiuyun Yang 
College of Forestry, Shanxi Agricultural University, Taigu 030801, China https://orcid.org/0000-0003-2799-0094
Xiaogang Wu 
College of urban and rural construction, Shanxi Agricultural University, Taigu 030801, China https://orcid.org/0000-0003-2898-9423
Shuhui Du 
College of Forestry, Shanxi Agricultural University, Taigu 030801, China https://orcid.org/0000-0002-5067-3591
Meiling Han 
College of urban and rural construction, Shanxi Agricultural University, Taigu 030801, China https://orcid.org/0000-0003-2746-3438



License

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

 

Articles are made available under the conditions CC BY 4.0 (until 2020 under the conditions CC BY-NC-ND 4.0).
Submission of the paper implies that it has not been published previously, that it is not under consideration for publication elsewhere.

The author signs a statement of the originality of the work, the contribution of individuals, and source of funding.