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De novo transcriptomic analysis of light-induced flavonoid pathway, transcription factors in the flower buds of Lonicera japonica

  • Hailing Fang
  • Xiwu Qi
  • Yiming Li
  • Xu Yu
  • Dongbei Xu
  • Chengyuan LiangEmail author
  • Weilin Li
  • Xin Liu
Original Article
Part of the following topical collections:
  1. Functional Genomics


Key message

Transcriptomic analysis of the relationship between gene expression patterns and flavonoid contents in the flower buds of Lonicera japonica under light-induced conditions, especially the flavonoid pathway genes and transcription factors.


Flos Lonicerae Japonicae (FLJ), the flower buds of Lonicera japonica Thunb., has been used to treat some human diseases including severe respiratory syndromes and hand-foot-and-mouth diseases owing to its putative antibacterial, and antiviral effects. Luteoloside is a flavonoid that is used by the Chinese Pharmacopoeia to evaluate the quality of FLJ. Light is an important environmental factor that affects flavonoid biosynthesis in the flower buds of L. japonica. However, how light triggers increases in flavonoid production remains unclear. To enhance our understanding of the mechanism involved in light-regulated flavonoid biosynthesis, we sequenced the transcriptomes of L. japonica exposed to three different light conditions: 100% light intensity (CK), 50% light intensity (LI50), and 25% light intensity (LI25) using an Illumina HiSeq 4000 System. A total of 77,297 unigenes with an average length of 809 bp were obtained. Among them, 43,334 unigenes (56.06%) could be matched to at least one biomolecular database. Additionally, 4188, 1545 and 1023 differentially expressed genes (DEGs) were identified by comparative transcriptomics LI25-vs-CK, LI50-vs-CK, and LI25-vs-LI50, respectively. Of note, genes known to be involved in flavonoid biosynthesis, such as 4-coumarate coenzyme A ligase (4CL), and chalcone synthase (CHS) were up-regulated. In addition, a total of 1649 transcription factors (TFs) were identified and divided into 58 TF families; 98 TFs exhibited highly dynamic changes in response to light intensity. Quantitative real-time PCR (qRT-PCR) was used to test the expression profiles of the RNA sequencing (RNA-Seq) data. This study offers insight into how transcriptional expression pattern is influenced by light in the flower buds of L. japonica, and will enhance the understanding of molecular mechanisms of flavonoid biosynthesis in response to light in L. japonica.


Lonicera japonica Thunb. Transcription Factor Light intensity Flavonoid Transcriptome sequencing 



Flos Lonicerae Japonicae


Differentially expressed genes


4-coumarate coenzyme A ligase


Chalcone synthase


Transcription factor


Quantitative real-time PCR


RNA sequencing


Phenylalanine ammonia-lyase


Flavanone 3-hydroxylase


Flavonol synthase


Chalcone isomerase


Flavonoid 3′-hydroxylase


Dihydroflavonol 4-reductase


Anthocyanidin synthase


Cinnamic acid 4-hydroxylase


Non-redundant protein sequence database


Clusters of eukaryotic orthologous Group


Gene ontology


Kyoto encyclopedia of genes and genomes


Flavonol synthase


UDP-glucose: flavone 7-O-beta-glucosyltransferase



This work was supported by the National Natural Science Foundation of China (31500249), the Natural Science Foundation of the Jiangsu Province (BK20160603, BK20161381).

Compliance with ethical standards

Conflict of interest

No potential conflict of interest was reported by the authors.

Availability of supporting data

We have deposit our data in Sequence Read Archive (SRA) database (, the accession for our submission is: SRP132670.

Supplementary material

468_2019_1916_MOESM1_ESM.png (19 kb)
Supplementary material 1 (PNG 19 kb). Fig S1 Length distribution of the assembled unigenes with a distribution larger than 200 bp in L. japonica
468_2019_1916_MOESM2_ESM.png (101 kb)
Supplementary material 2 (PNG 101 kb). Fig S2 Gene ontology (GO) classifications of DEGs in pairwise comparisons (LI25-vs-CK, LI50-vs-CK, and LI25-vs-LI50). The DEGs were classified into three main categories: (A) cellular component, (B) molecular function, and (C) biological process. Each bar indicates the number of unigenes classified under each specific category
468_2019_1916_MOESM3_ESM.docx (18 kb)
Supplementary material 3 (DOCX 17 kb)
468_2019_1916_MOESM4_ESM.docx (17 kb)
Supplementary material 4 (DOCX 16 kb)
468_2019_1916_MOESM5_ESM.docx (18 kb)
Supplementary material 5 (DOCX 18 kb)
468_2019_1916_MOESM6_ESM.docx (33 kb)
Supplementary material 6 (DOCX 32 kb)
468_2019_1916_MOESM7_ESM.docx (23 kb)
Supplementary material 7 (DOCX 23 kb)


  1. Amato A, Cavallini E, Zenoni S, Finezzo L, Begheldo M, Ruperti B, Tornielli GB (2016) A grapevine ttg2-like wrky transcription factor is involved in regulating vacuolar transport and flavonoid biosynthesis. Front Plant Sci 7:1979. PubMedCrossRefGoogle Scholar
  2. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106. PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bai SL, Sun YW, Qian MJ, Yang FX, Ni JB, Tao RY, Li L, Shu Q, Zhang D, Teng YW (2017) Transcriptome analysis of bagging-treated red Chinese sand pear peels reveals light-responsive pathway functions in anthocyanin accumulation. Sci Rep 7(1):63. PubMedPubMedCentralCrossRefGoogle Scholar
  4. Chinese Pharmacopoeia Commission (2015) The Pharmacopoeia of the People’s Republic of China. China Medical Science Press, Beijing, p 221Google Scholar
  5. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. PubMedCrossRefGoogle Scholar
  6. Cullum R, Alder O, Hoodless PA (2011) The next generation: using new sequencing technologies to analyse gene regulation. Respirology 16(2):210–222. PubMedCrossRefGoogle Scholar
  7. Dalman K, Wind JJ, Nemesio-Gorriz M, Hammerbacher A, Lundén K, Ezcurra I, Elfstrand M (2017) Overexpression of PaNAC03, a stress induced NAC gene family transcription factor in Norway spruce leads to reduced flavonol biosynthesis and aberrant embryo development. BMC Plant Biol 17(1):6. PubMedPubMedCentralCrossRefGoogle Scholar
  8. Deng B, Shang XL, Fang SZ, Li QQ, Fu XX, Su J (2012) Integrated effects of light intensity and fertilization on growth and flavonoid accumulation in Cyclocarya paliurus. J Agr Food Chem 60(25):6286–6292. CrossRefGoogle Scholar
  9. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15(10):573–581. PubMedCrossRefGoogle Scholar
  10. Duthie GG, Duthie SJ, Kyle JAM (2000) Plant polyphenols in cancer and heart disease: implications as nutritional antioxidants. Nutr Res Rev 13(1):79–106. PubMedCrossRefGoogle Scholar
  11. Ferdinando MD, Brunetti C, Fini A, Tattini M (2012) Flavonoids as antioxidants in plants under abiotic stresses. In: Ahmad P and Prasad MNV (eds) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York, USA, pp 159–179CrossRefGoogle Scholar
  12. Fu FF, Xue HW (2010) Coexpression analysis identifies Rice Starch Regulator 1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154(2):927–938. PubMedPubMedCentralCrossRefGoogle Scholar
  13. Gesell A, Yoshida K, Lan TT, Constabel CP (2014) Characterization of an apple TT2-type R2R3 MYB transcription factor functionally similar to the poplar proanthocyanidin regulator PtMYB134. Planta 240(3):497–511. PubMedCrossRefGoogle Scholar
  14. Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLHh/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53(5):814–827. PubMedCrossRefGoogle Scholar
  15. Hao XL, Zhong YJ, Fu XQ, Lv ZY, Shen Q, Yan TX, Shi P, Ma YA, Chen MH, Lv XY, Wu ZKY, Zhao JY, Sun XF, Li L, Tang KX (2017) Transcriptome analysis of genes associated with the artemisinin biosynthesis by jasmonic acid treatment under the light in Artemisia annua. Front Plant Sci 8:971. PubMedPubMedCentralCrossRefGoogle Scholar
  16. He SQ, Hu QF, Yang GY (2010) Research of honeysuckle. Yunnan Chem Technol 37:72–75. CrossRefGoogle Scholar
  17. He L, Xu XL, Li Y, Li CF, Zhu YJ, Yan HX, Sun ZY, Sun C, Song JY, Bi YA, Shen J, Cheng RY, Wang ZZ, Xiao W, Chen SL (2013) Transcriptome analysis of buds and leaves using 454 pyrosequencing to discover genes associated with the biosynthesis of active ingredients in Lonicera japonica Thunb. PLoS One 8(4): e62922. PubMedPubMedCentralCrossRefGoogle Scholar
  18. Hichri I, Heppel SC, Pillet J, Léon C, Czemmel S, Delrot S, Virginie L, Jochen B (2010) The basic helix-loop-helix transcription factor MYC1 is involved in the regulation of the flavonoid biosynthesis pathway in Grapevine. Mol Plant 3(3):509–523. PubMedCrossRefGoogle Scholar
  19. Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J Exp Bot 62(8):2465–2483. PubMedCrossRefGoogle Scholar
  20. Hong Y, Tang XJ, Huang H, Zhang Y, Dai SL (2015) Transcriptomic analyses reveal species-specific light-induced anthocyanin biosynthesis in chrysanthemum. BMC Genomics 16(1):202. PubMedPubMedCentralCrossRefGoogle Scholar
  21. Hsu HF, Hsiao PC, Kuo TC, Chiang ST, Chen SL, Chiou SJ, Ling XH, Liang MT, Cheng WY, Houng JY (2016) Antioxidant and anti-inflammatory activities of Lonicera japonica Thunb. var. sempervillosa Hayata flower bud extracts prepared by ater, ethanol and supercritical fluid extraction techniques. Ind Crop Prod 89:543–549. CrossRefGoogle Scholar
  22. Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, Okada K, Wada T (2007) Arabidopsis transparent testa glabra2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19(8):2531–2543. PubMedPubMedCentralCrossRefGoogle Scholar
  23. Jiao XZ, Yip WK, Yang SF (1987) The effect of light and phytochrome on 1-aminocyclopropane-1-carboxylic acid metabolism in etiolated wheat seedling leaves. Plant Physiol 85(3):643–647. PubMedPubMedCentralCrossRefGoogle Scholar
  24. Koyama K, Ikeda H, Poudel PR, Gotoyamamoto N (2012) Light quality affects flavonoid biosynthesis in young berries of cabernet sauvignon grape. Phytochemistry 78(6):54–64. PubMedCrossRefGoogle Scholar
  25. Ku SK, Seo BI, Park JH, Park GY, Seo YB, Kim JS, Lee HS, Roh SS (2009) Effect of Lonicerae Flos extracts on reflux esophagitis with antioxidant activity. World J Gastroenterol 15(38):4799–4805. PubMedPubMedCentralCrossRefGoogle Scholar
  26. Lai Y, Li HX, Yamagishi M (2013) A review of target gene specificity of flavonoid R2R3-MYB transcription factors and a discussion of factors contributing to the target gene selectivity. Front Biol 8:577–598. CrossRefGoogle Scholar
  27. Lai B, Li XJ, Hu B, Qin YH, Huang XM, Wang HC, Hu GB (2014) LcMYB1 is a key determinant of differential anthocyanin accumulation among genotypes, tissues, developmental phases and ABA and light stimuli in Litchi chinensis. PLoS One 9:e86293. PubMedPubMedCentralCrossRefGoogle Scholar
  28. Licausi F, Ohme-Takagi M, Perata P (2013) Apetala2/ethylene responsive factor (ap2/erf) transcription factors: mediators of stress responses and developmental programs. New Phytol 199(3):639–649. PubMedCrossRefGoogle Scholar
  29. Liu ZX, Cheng ZY, He QJ, Lin B, Gao PY, Li LZ, Liu QB, Song SJ (2016) Secondary metabolites from the flower buds of Lonicera japonica and their in vitro anti-diabetic activities. Fitoterapia 110:44–51. PubMedCrossRefGoogle Scholar
  30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408. CrossRefGoogle Scholar
  31. Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21(19):3787–3793. PubMedCrossRefGoogle Scholar
  32. Mehrtens F, Kranz H, Bednarek P, Weisshaar B (2005) The arabidopsis transcription factor myb12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiol 138(2):1083–1096. PubMedPubMedCentralCrossRefGoogle Scholar
  33. Morishita T, Kojima Y, Maruta T, Nishizawa-Yokoi A, Yabuta Y, Shigeoka S (2009) Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiol 50:2210–2222. PubMedCrossRefGoogle Scholar
  34. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628. PubMedCrossRefGoogle Scholar
  35. Nakano T, Nishiuchi T, Suzuki K, Fujimura T, Shinshi H (2006) Studies on transcriptional regulation of endogenous genes by erf2 transcription factor in tobacco cells. Plant Cell Physiol 47(4):554–558. PubMedCrossRefGoogle Scholar
  36. Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) Nac transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819(2):97–103. PubMedCrossRefGoogle Scholar
  37. Pan JQ, Chen HM, Guo BL, Liu C (2017) Understanding the molecular mechanisms underlying the effects of light intensity on flavonoid production by RNA-seq analysis in Epimedium pseudowushanense B.L.Guo. PLoS One 12(8):e0182348. PubMedPubMedCentralCrossRefGoogle Scholar
  38. Pandey A, Misra P, Bhambhani S, Bhatia C, Trivedi PK (2014) Expression of Arabidopsis MYB transcription factor, AtMYB111, in tobacco requires light to modulate flavonol content. Sci Rep 4(5):5018. PubMedPubMedCentralCrossRefGoogle Scholar
  39. Rai A, Kamochi H, Suzuki H, Nakamura M, Takahashi H, Hatada T, Saito K, Yamazaki M (2017) De novo transcriptome assembly and characterization of nine tissues of Lonicera japonica to identify potential candidate genes involved in chlorogenic acid, luteolosides, and secoiridoid biosynthesis pathways. J Nat Med 71(1):1–15. PubMedCrossRefGoogle Scholar
  40. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140. CrossRefGoogle Scholar
  41. Roy NC, Altermann E, Park ZA, McNabb WC (2011) A comparison of analog and Next-Generation transcriptomic tools for mammalian studies. Brief Funct Genomics 10(3):135–150. PubMedCrossRefGoogle Scholar
  42. Schluttenhofer C, Yuan L (2015) Regulation of specialized metabolism by WRKY transcription factors. Plant Physiol 167:295–306. PubMedCrossRefGoogle Scholar
  43. Seo ON, Kim GS, Park S, Lee JH, Kim YH, Lee WS, Lee SJ, Kim CY, Jin JS, Choi SK, Shin SC (2012) Determination of polyphenol components of Lonicera japonica Thunb. using liquid chromatography-tandem mass spectrometry: contribution to the overall antioxidant activity. Food Chem 134(1):572–577. CrossRefGoogle Scholar
  44. Shang XF, Pan H, Li MX, Miao XL, Ding H (2011) Lonicera japonica Thunb.: ethnopharmacology, phytochemistry and pharmacology of an important traditional Chinese medicine. J Ethnopharmacol 138(1):1–21. PubMedCrossRefGoogle Scholar
  45. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. PubMedPubMedCentralCrossRefGoogle Scholar
  46. Shao QS, Wang HZ, Guo HP, Zhou AC, Huang YQ, Sun YL, Li MY (2014) Effects of shade treatments on photosynthetic characteristics, chloroplast ultrastructure, and physiology of Anoectochilus roxburghii. PLoS One 9(2):e85996. PubMedPubMedCentralCrossRefGoogle Scholar
  47. Sun RZ, Cheng G, Li Q, He YN, Wang Y, Lan YB, Li SY, Zhu YR, Song WF, Zhang X, Cui XD, Chen W, Wang J (2017) Light-induced variation in phenolic compounds in cabernet sauvignon grapes (vitis vinifera L.) involves extensive transcriptome reprogramming of biosynthetic enzymes, transcription factors, and phytohormonal regulators. Front Plant Sci 8:547. PubMedPubMedCentralCrossRefGoogle Scholar
  48. Tattini M, Galardi C, Pinelli P, Massai R, Remorini D, Agati G (2004) Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytol 163(3):547–561. CrossRefGoogle Scholar
  49. Wang DY, Zhao XM, Liu YL (2017a) Hypoglycemic and hypolipidemic effects of a polysaccharide from flower buds of Lonicera japonica in streptozotocin-induced diabetic rats. Int J Biol Macromol 102:396–404. PubMedCrossRefGoogle Scholar
  50. Wang R, Xu S, Wang N, Xia B, Jiang Y, Wang R (2017b) Transcriptome analysis of secondary metabolism pathway, transcription factors, and transporters in response to methyl jasmonate in Lycoris aurea. Front Plant Sci 7:1971. PubMedPubMedCentralCrossRefGoogle Scholar
  51. Ward JA, Ponnala L, Weber CA (2012) Strategies for transcriptome analysis in nonmodel plants. Am J Bot 99(2):267–276. PubMedCrossRefGoogle Scholar
  52. Winkel SB (2001) Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126(2):485–493. CrossRefGoogle Scholar
  53. Xiong YQ, Liu TY, Tian CG, Sun SH, Li JY, Chen MS (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59(1):191–203. PubMedCrossRefGoogle Scholar
  54. Xu Y, Wang GB, Cao FL, Zhu CC, Wang GY, El-Kassaby YA (2014) Light intensity affects the growth and flavonol biosynthesis of ginkgo (ginkgo biloba, L.). New Forests 45(6):765–776. CrossRefGoogle Scholar
  55. Xu W, Dubos C, Lepiniec L (2015) Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20:176–185. PubMedCrossRefGoogle Scholar
  56. Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ, Wang J, Li ST, Li RQ, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:293–297. CrossRefGoogle Scholar
  57. Ye SY, Shao QS, Xu MJ, Li SL, Wu M, Tan X, Su LY (2017) Effects of light quality on morphology, enzyme activities, and bioactive compound contents in Anoectochilus roxburghii. Front Plant Sci 8:857. PubMedPubMedCentralCrossRefGoogle Scholar
  58. Yoneda Y, Shimizu H, Nakashima H, Miyasaka J, Ohdoi K (2017) Effects of light intensity and photoperiod on improving steviol glycosides content in stevia rebaudiana (bertoni) bertoni while conserving light energy consumption. J Appl Res Med Aro Plants 7:64–73. CrossRefGoogle Scholar
  59. Yonekura-Sakakibara K, Saito K (2013) Transcriptome coexpression analysis using ATTED-II for integrated transcriptomic/metabolomic analysis. Methods Mol Biol 1011:317–326. PubMedCrossRefGoogle Scholar
  60. Yuan Y, Song LP, Li MH, Liu GM, Chu YN, Ma LY, Zhou YY, Wang X, Gao W, Qin SS, Yu J, Wang XM, Huang LQ (2012) Genetic variation and metabolic pathway intricacy govern the active compound content and quality of the Chinese medicinal plant Lonicera japonica thunb. BMC Genomics 13:195. PubMedPubMedCentralCrossRefGoogle Scholar
  61. Yuk HJ, Song YH, Long MJC, Kim DW, Woo SG, Lee YB, Uddin Z, Kim CY, Park KH (2016) Ethylene induced a high accumulation of dietary isoflavones and expression of isoflavonoid biosynthetic genes in soybean (glycine max) leaves. J Agric Food Chem 64(43):8272. PubMedCrossRefGoogle Scholar
  62. Zhang W, Zou A, Miao J, Yin Y, Tian R, Pang YJ, Yang R, Qi JL, Yang YH (2011) LeERF-1, a novel AP2/ERF family gene within the B3 subcluster, is down-regulated by light signals in Lithospermum erythrorhizon. Plant Biol 13(2):343–348. PubMedCrossRefGoogle Scholar
  63. Zhang HN, Li WC, Wang HC, Shi SY, Shu B, Liu LQ, Wei YZ, Xie JH (2016a) Transcriptome profiling of light-regulated anthocyanin biosynthesis in the pericarp of Litchi. Front Plant Sci 7:963. PubMedPubMedCentralCrossRefGoogle Scholar
  64. Zhang L, Yan L, Fu C, Xiang J, Gan J, Gang W, Jia HB, Yu LJ, Li MT (2016b) Different gene expression patterns between leaves and flowers in Lonicera japonica revealed by transcriptome analysis. Front Plant Sci 7:637. PubMedPubMedCentralCrossRefGoogle Scholar
  65. Zhang RT, Kong ZY, Chen SH, Ran ZS, Ye MW, Xu JL, Zhou CX, Liao K, Cao JY, Yan XJ (2017) The comparative study for physiological and biochemical mechanisms of Thalassiosira pseudonana and Chaetoceros calcitrans in response to different light intensities. Algal Res 27:89–98. CrossRefGoogle Scholar
  66. Zoratti L, Karppinen K, Escobar AL, Häggman H, Jaakola L (2014) Light-controlled flavonoid biosynthesis in fruits. Front Plant Sci 5(5):534. PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Hailing Fang
    • 1
  • Xiwu Qi
    • 1
  • Yiming Li
    • 2
  • Xu Yu
    • 1
    • 3
  • Dongbei Xu
    • 1
  • Chengyuan Liang
    • 1
    Email author
  • Weilin Li
    • 2
  • Xin Liu
    • 2
  1. 1.Institute of BotanyJiangsu Province and Chinese Academy of SciencesNanjingPeople’s Republic of China
  2. 2.Nanjing Forestry UniversityNanjingChina
  3. 3.Missouri State UniversitySpringfieldUSA

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