Abstract
Herbaceous peony (Paeonia lactiflora Pall.) is one of the color-leaved ornamental spring plants, with graceful appearance and splendid color. However, the underlying mechanism of this coloration variation from purple to green has not been studied in P. lactiflora. In th study, the leaves in purple, purple–green, and green stages were compared in terms of anatomical, physiological, and molecular. We found that the variation of leaf color from purple to green was mainly determined by the change in pigments distributed in the leaf surface. Physiological experiments showed a significant increase in chlorophyll contents and a notable reduction in anthocyanin contents in leaves from the purple to green stages. We further found that the anthocyanin biosynthesis-related dihydroflavonol 4-reductase (DFR) gene and anthocyanin synthase (ANS) gene as well as chlorophyll biosynthesis-related glutamyl-tRNA reductase (HEMA) gene showed a decreased trend in leaves from purple to green stages, whereas the chlorophyll degradation-related chlorophyll b reductase (NYC) gene showed a rising trend. Alteration of DFR and ANS gene expression might reduce anthocyanin accumulation, whereas increased HEMA gene expression would enhance chlorophyll biosynthesis and reduced NYC gene expression would inhibit chlorophyll degradation. Consequently, reduction in anthocyanins and enhanced deposition of chlorophylls resulted in leaf coloration variation from purple to green in P. lactiflora, which could improve our understanding of its mechanism for further studies.
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References
Beale SI (2005) Green genes gleaned. Trends Plant Sci 10(7):309–312. https://doi.org/10.1016/j.tplants.2005.05.005
Carlson JE, Holsinger KE (2010) Natural selection on inflorescence color polymorphisms in wild Protea populations: the role of pollinators, seed predators, and intertrait correlations. Am J Bot 97:934–944. https://doi.org/10.3732/ajb.0900348
Deng XJ, Zhang HQ, Wang Y, He F, Liu JL, Xiao X, Shu ZF, Li W, Wang GH, Wang GL (2014) Mapped clone and functional analysis of leaf-color gene Ygl7 in a rice hybrid (Oryza sativa L. ssp. indica). PLoS ONE 9:e99564. https://doi.org/10.1371/journal.pone.0099564
Ewa M (2009) Survey of plant pigments molecular and environmental determinants of plant colors. Acta Biol Crac Ser Bot 51(1):7–16. https://doi.org/10.1186/1471-2229-9-1
Field 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 127:566–574. https://doi.org/10.1104/pp.127.2.566
Gong SJ, Hao ZJ, Meng JS, Liu D, Wei MR, Tao J (2015) Digital gene expression analysis to screen disease resistance-relevant genes from leaves of herbaceous peony (Paeonia lactiflora Pall.) infected by Botrytis cinerea. Plos One 10(7):e0133305. https://doi.org/10.1371/journal.pone.0133305
Hao ZJ, Wei MR, Gong SJ, Zhao DQ, Tao J (2016) Transcriptome and digital gene expression analysis of herbaceous peony (Paeonia lactiflora Pall.) to screen thermo-tolerant related differently expressed genes. Genes Genom 38(12):1201–1215. https://doi.org/10.1007/s13258-016-0465-8
Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends Plant Sci 18(9):477–483. https://doi.org/10.1016/j.tplants.2013.06.003
Jia T, Ito H, Tanaka A (2015) The Chlorophyll b, reductase NOL participates in regulating the antenna size of photosystem II in Arabidopsis thaliana. Proc Chem 14:422–427. https://doi.org/10.1016/j.proche.2015.03.057
Kanemakia A, Otania M, Takanoa M, Fujimotoa T, Okuharab H, Nomizub T, Kondob M, Kobayashib H, Tatsuzawac F, Nakano M (2018) Ectopic expression of the R2R3-MYB gene from Tricyrtis sp. results in leaf color alteration in transgenic Pelargonium crispum. Sci Hortic 240:411–416. https://doi.org/10.1016/j.scienta.2018.06.029
Koch M, Breithaupt C, Kiefersauer R, Freigang J, Huber R, Messerschmidt A (2004) Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J 23(8):1720–1728. https://doi.org/10.1038/sj.emboj.7600189
Kumar AM, Söll D (2000) Antisense HEMA1 RNA expression inhibits heme and chlorophyll biosynthesis in Arabidopsis. Plant Physiol 122:49–56. https://doi.org/10.1104/pp.122.1.49
Lai B, Hu B, Qin YH, Zhao JT, Wang HC, Hu GB (2015) Transcriptomic analysis of Litchi chinensis pericarp during maturation with a focus on chlorophyll degradation and flavonoid biosynthesis. BMC Genom 16:225. https://doi.org/10.1186/s12864-015-1433-4
Leahu A, Ghinea C, Oroian MA, Damian C (2018) Determination of essential and toxic elements, ascorbic acid content and color of different leaves in two cabbage varieties. Ovidius Uni Ann Chem 29(2):110–116. https://doi.org/10.2478/auoc-2018-0016
Lewis DH, Arathoon HS, Swinny EE, Huang SC, Funnell KA (2003) Anthocyanin and carotenoid pigments in spathe tissue from selected Zantedeschia hybrids. Acta Hortic 624:147–154. https://doi.org/10.17660/actahortic.2003.624.19
Li Y, Zhang ZY, Wang P, Wang SA, Ma LL, Li LF, Yang RT, Ma YZ, Wang Q (2015) Comprehensive transcriptome analysis discovers novel candidate genes related to leaf color in a Lagerstroemia indica yellow leaf mutant. Genes Genom 37:851–863. https://doi.org/10.1007/s13258-015-0317-y
Li WX, Yang SB, Lu ZG, He ZC, Ye YL, Zhao BB, Wang L (2018) Jin B (2018) Cytological, physiological, and transcriptomic analyses of golden leaf coloration in Ginkgo biloba L. Hortic Res 5:12. https://doi.org/10.1038/s41438-018-0015-4
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Liu RY, Dong XC, Gu WT, Yu LX, Jin WJ, Qu Y, Zhang F, Li WJ (2016) Variation in the phenotypic features and transcripts of thermo-sensitive leaf-color mutant induced by carbon ion beam in green wandering jew (Tradescantia fluminensis). Sci Hortic 213:303–313. https://doi.org/10.1016/j.scienta.2016.11.001
Liu C, Shi NR, Wu HY, An XY, Zheng JJ, Duan Sun DJ, Feng Y, Zhang LL (2018a) Cytogenetic analyses of PSL1 mutant, a novel low-temperature-sensitive purple-striped leaf color mutant in wheat. Crop Sci 58:1919–1931. https://doi.org/10.2135/cropsci2018.01.0057
Liu MY, Lu Y, Wang S, Wu F, Li JR, Wang YH, Zhao JJ, Shen SX (2018b) Characterization of the leaf color mutant hy and identification of the mutated gene in Chinese cabbage. J Am Soc Hortic Sci 143(5):363–369. https://doi.org/10.21273/JASHS04403-18
Nguyen P, Cin VD (2009) The role of light on foliage colour development in coleus (Solenostemon scutellarioides (L.) Codd). Plant Physiol Biochem 47(10):934–945. https://doi.org/10.1016/j.plaphy.2009.06.006
Sato Y, Morita R, Katsuma S, Nishimura M, Tanaka A, Kusaba M (2009) Two short-chain dehydrogenase/reductases, Non-Yellow coloring 1 and Nyc1-Like, are required for chlorophyll band light-harvesting complex II degradation during senescence in rice. Plant J 57(1):120–131. https://doi.org/10.1111/j.1365-313x.2008.03670.x
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108. https://doi.org/10.1038/nprot.2008.73
Shen JZ, Zou ZW, Zhang XZ, Zhou L, Wang YH, Fang WP, Zhu XJ (2018) Metabolic analyses reveal different mechanisms of leaf color change in two purple-leaf tea plant (Camellia sinensis L.) cultivars. Hortic Res 5:7. https://doi.org/10.1038/s41438-017-0010-1
Su TB, Yu SC, Zhang JWF, Yu YJ, Zhang DS, Zhao XY, Wang WH (2014) Loss of function of the carotenoid isomerase gene BrCRTISO confers orange color to the inner leaves of Chinese cabbage (Brassica rapa L ssp pekinensis). Plant Mol Biol Rep 33(3):648–659. https://doi.org/10.1007/s11105-014-0779-0
Szankowski I, Flachowsky H, Li HH, Halbwirth H, Treutter D, Regos I, Hanke MV, Stich K, Fischer TC (2009) Shift in polyphenol profile and sublethal phenotype caused by silencing of anthocyanidin synthase in apple (Malus sp.). Planta 229(3):681–692. https://doi.org/10.1007/s00425-008-0864-4
Tang YH, Zhao DQ, Meng JS, Tao J (2019) EGTA reduces the inflorescence stem mechanical strength of herbaceous peony by modifying secondary wall biosynthesis. Hortic Res 6:36. https://doi.org/10.1038/s41438-019-0117-7
Tian J, Han ZY, Zhang J, Hu YJ, Song TT, Yao YC (2015) The balance of expression of dihydroflavonol 4-reductase and flavonol synthase regulates flavonoid biosynthesis and red foliage coloration in crabapples. Sci Rep 5:12228. https://doi.org/10.1038/srep12228
Wei K, Zhang YZ, Wu LY, Li HL, Ruan L, Bai PX, Zhang CC, Zhang F, Xu LY, Wang LY, Cheng H (2016) Gene expression analysis of bud and leaf color in tea. Plant Physiol Biochem 107:310–318. https://doi.org/10.1016/j.plaphy.2016.06.022
Winkel-Shirley B (2001) Flavonoid Biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126(2):485–493. https://doi.org/10.1104/pp.126.2.485
Wu ZM, Zhang X, He B, Diao LP, Sheng SL, Wang JL, Guo XP, Su N, Wang LF, Jiang L, Wang CM, Zhai HQ, Wan JM (2007) A chlorophyll-deficient rice mutant with impaired chlorophyllide esterification in chlorophyll biosynthesis. Plant Physiol 145:29–40. https://doi.org/10.1104/pp.107.100321
Wu YQ, Tang YH, Jiang Y, Zhao DQ, Shang JL, Tao J (2018) Combination of transcriptome sequencing and iTRAQ proteome reveal the molecular mechanisms determining petal shape in herbaceous peony (Paeonia lactiflora Pall.). Biosci Rep. https://doi.org/10.1042/BSR20181485
Yang YX, Chen XX, Xu B, Li YX, Ma YH, Wang GD (2015) Phenotype and transcriptome analysis reveals chloroplast development and pigment biosynthesis together influenced the leaf color formation in mutants of Anthurium andraeanum ‘Sonate’. Front Plant Sci 6:139. https://doi.org/10.3389/fpls.2015.00139
Yang T, Li KT, Hao SX, Zhang J, Song TT, Tian J, Yao YC (2018) The use of RNA sequencing and correlation network analysis to study potential regulators of leaf color transformation. Plant Cell Physiol 59(5):1027–1042. https://doi.org/10.1093/pcp/pcy044
Yu JJ, Zhang JZ, Zhao Q, Liu YL, Chen SX, Guo HL, Shi Dai SJ (2016) Proteomic analysis reveals the leaf color regulation mechanism in chimera Hosta ‘Gold Standard’ leaves. Int J Mol Sci 17:346. https://doi.org/10.3390/ijms17030346
Zhang H, Liu LL, Cai MH, Zhu SS, Zhao JY, Zheng TH, Xu XY, Zeng ZQ, Niu J, Jiang L, Chen SH, Wan JM (2015) A point mutation of magnesium chelatase OsCHLI gene dampens the interaction between CHLI and CHLD subunits in rice. Plant Mol Biol Rep 33(6):1975–1987. https://doi.org/10.1007/s11105-015-0889-3
Zhang T, Feng P, Li YF, Yu P, Yu GL, Sang XC, Ling YH, Zeng XQ, Li YD, Huang JY, Zhang TQ, Zhao FM, Wang N, Zhang CW, Yang ZL, Wu RH, He GH (2018) Virescent-albino leaf 1 regulates leaf colour development and cell division in rice. J Exp Bot. https://doi.org/10.1093/jxb/ery250
Zhao DQ, Tao J, Han CX, Ge JT (2012a) Actin as an alternative internal control gene for gene expression analysis in herbaceous peony (Paeonia lactifora Pall.). Afr J Agric Res 7:2153–2159. https://doi.org/10.5897/AJAR11.1613
Zhao DQ, Tao J, Han CX, Ge JT (2012b) Flower color diversity revealed by differential expression of flavonoid biosynthetic genes and favonoid accumulation in herbaceous peony (Paeonia lactifora Pall.). Mol Biol Rep 39:11263–11275. https://doi.org/10.1007/s11033-012-2036-7
Zhao DQ, Tang WH, Hao ZJ, Tao (2015) Identification of flavonoids and expression of flavonoid biosynthetic genes in two coloured tree peony flowers. Biochem Biophys Res Commun 459(3):450–456. https://doi.org/10.1016/j.bbrc.2015.02.126
Zhao DQ, Wei MR, Liu D, Tao J (2016) Anatomical and biochemical analysis reveal the role of anthocyanins in flower coloration of herbaceous peony. Plant Physiol Biochem 102:97–106. https://doi.org/10.1016/j.plaphy.2016.02.023
Zhao DQ, Tang YH, Xia X, Sun J, Meng JS, Shang JL, Tao J (2019) Integration of transcriptome, proteome, and metabolome provides insights into how calcium enhances the mechanical strength of herbaceous peony inflorescence stems. Cells 8(2):102. https://doi.org/10.3390/cells8020102
Zhu GF, Yang FX, Shi SS, Li DM, Wang Z, Liu HL, Huang D, Wang CY (2015) Transcriptome characterization of Cymbidium sinense ‘Dharma’ using 454 pyrosequencing and its application in the identification of genes associated with leaf color variation. PLoS ONE 10(6):e0128592. https://doi.org/10.1371/journal.pone.0128592
Acknowledgements
This work was supported by the Natural Science Foundation of China (31400592), the National Key Research and Development Program (2018YFD1000405), the Graduate Innovation Program of Jiangsu Province (XKYCX19_119), the Program of Key Members of Yangzhou University Outstanding Young Teacher and the Priority Academic Program Development from Jiangsu Government.
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JT and DZ planned and designed the experiments. YT, ZF and ML performed the experiments. YT analyzed the data and wrote the manuscript. All authors carefully read and approved the final manuscript.
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Tang, Y., Fang, Z., Liu, M. et al. Color characteristics, pigment accumulation and biosynthetic analyses of leaf color variation in herbaceous peony (Paeonia lactiflora Pall.). 3 Biotech 10, 76 (2020). https://doi.org/10.1007/s13205-020-2063-3
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DOI: https://doi.org/10.1007/s13205-020-2063-3