Skip to main content
Log in

From green to red: large-scale transcriptome comparison of a bud sport in poplar (Populus deltoides)

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

An Erratum to this article was published on 31 March 2017

Abstract

The red-leaf coloration of Quanhong poplar (QHP) (Populus deltoides), resulting from a bud sport, is a distinctive trait conferring high ornamental value. However, the underlying molecular coloration mechanism of the red-leaf poplar remains unknown. In this study, tissue buds and leaves from mutant QHP(red)and its wild-type progenitor L2025 (green) were used to study the coloration mechanism by high-throughput RNA sequencing and comparative analysis of the transcriptomes. A total of 12,000 differentially expressed genes (DEGs) were obtained. Functional enrichment using Gene Ontology (GO) and, Genes and Genomes (KEGG) annotations showed that 4951 bud DEGs and 1927 leaf DEGs participate in many important biological and metabolic pathways, including anthocyanin biosynthesis. Importantly, some structural genes that contribute to photosynthesis were down-regulated, and some candidate genes involved in the biosynthesis of abscisic acid (ABA), ethylene and anthocyanin were up-regulated in the QHP mutant. The DEGs identified provided insight into the novel traits of the mutant. The unigene dataset that was used to discover candidate genes provides a comprehensive resource for molecular research in red-leaf poplar and may provide insight into coloration of other woody plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15(1):63–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7(10):986–995

    CAS  PubMed  Google Scholar 

  • Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 6(1):43–73

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57(1):289–300

    Google Scholar 

  • Castellarin SD, di Gaspero G (2007) Transcriptional control of anthocyanin biosynthetic genes in extreme phenotypes for berry pigmentation of naturally occurring grapevines. BMC Plant Biol 7:46–56

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen T, Zhang YD, Zhao L, Zhu Z, Lin J, Zhang SB, Wang CL (2007) Physiological character and gene mapping in a new green-revertible albino mutant in rice. J Genet Genom 34(4):331–338

    Article  CAS  Google Scholar 

  • Coe EH (1994) Anthocyanin genetics. In: Freeling M, Waibot V (eds) The maize handbook. Springer-Verlag, New York, pp 279–282

    Chapter  Google Scholar 

  • Dai Y, Fu ZM, Li JY (2003) Isolation and characterization of an Arabidopsis bushy and dwarf mutant. Acta Botanica Sinica 45(5):621–625

    CAS  Google Scholar 

  • Dong QL, Yan ZY, Liu Z, Yao YX (2011) Early ripening events caused by bud mutation in Beni Shogun apple. Russ J Plant Physio 58(3):439–447

    Article  CAS  Google Scholar 

  • Dykes L, Seitz LM, Rooney WL, Rooney LW (2009) Flavonoid composition of red sorghum genotypes. Food Chem 116:313–317

    Article  CAS  Google Scholar 

  • Eckhardt U, Grimm B, Hortensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56(1):1–14

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gould KS, Kuhn DN, Lee DW, Oberbauer SF (1995) Why leaves are sometimes red. Nature 378(6554):241–242

    CAS  Google Scholar 

  • Gould KS, McKelvie J, Markham KR (2002) Do anthocyanins function as antioxidants in leaves? Imaging of H2O2 in red and green leaves after mechanical injury. Plant, Cell Environ 25:1261–1269

    Article  CAS  Google Scholar 

  • He F, Liang NN, Mu L, Pan QH, Wang J, Reeves MJ, Duan CQ (2012) Anthocyanins and their variation in red wines I. Monomeric anthocyanins and their color expression. Molecules 17(2):1571–1601

    Article  CAS  PubMed  Google Scholar 

  • Hooley R (1994) Gibberellins: perception, transduction and responses. Plant Mol Biol 26:1529–1555

    Article  CAS  PubMed  Google Scholar 

  • Hortensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77

    Article  CAS  PubMed  Google Scholar 

  • Huang XQ, Zhao HX, Dong CL, Sun YY, Wang PR, Deng XJ (2005) Chlorophyll-deficit rice mutants and their research advances in Biology. Acta Botanica Boreali-Occidentalia Sinica 25(8):1685–1691 (in Chinese with an English abstract)

    CAS  Google Scholar 

  • Huang WJ, Zhang SL, Xiao CC, Zhang QJ, Qin GH, Wu J (2011) Relationship between Anthocyanin biosynthesis and related enzyme activities in pyrus communis L. CV. ‘Early Red Comice’ and its green bud mutant. Acta Botanica Boreali-Occidentalia Sinica 31(7):1428–1433 (In Chinese)

    CAS  Google Scholar 

  • Jara-Palacios MJ, Gordillo B, González-Miret ML, Hernanz D, Escudero-Gilete ML, Heredia FJ (2014) Comparative study of the enological potential of different winemaking byproducts: implications in the antioxidant activity and color expression of red wine anthocyanins in a model solution. J Agric Food Chem 62(29):6975–6983

    Article  CAS  PubMed  Google Scholar 

  • Jeong ST, Goto-Yamamoto N, Hashizume K, Esaka M (2006) Expression of the flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase genes and flavonoid composition in grape (Vitis vinifera). Plant Sci 170:61–69

    Article  CAS  Google Scholar 

  • Jeong ST, Goto-Yamamoto N, Hashizume K, Esaka M (2008) Expression of muti-copy flavonoid pathway genes coincides with anthocyanin, flavonol and flavan-3-ol accumulation of grapevine. Vitis 47:135–140

    CAS  Google Scholar 

  • Jiang Y, Wu K, Lin F, Qu Y, Liu X, Zhang Q (2014) Phosphatidic acid integrates calcium signaling and microtubule dynamics into regulating ABA-induced stomatal closure in Arabidopsis. Planta 239(3):565–575

    Article  CAS  PubMed  Google Scholar 

  • Jornet-Somoza J, Alberdi-Rodriguez J, Milne BF, Andrade X, Marques MA, Nogueira F, Oliveira MJ, Stewart JJ, Rubio A (2015) Insights into colour-tuning of chlorophyll optical response in green plants. Phys Chem Chem Phys 17(40):26599–26606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung KH, Hur J, Ryu CH, Choi Y, Chung YY, Miyao A, Hirochika H, An G (2003) Characterization of a Rice Chlorophyll-Deficient Mutant Using the T-DNA Gene-Trap System. Plant Cell Physiol 44(5):463–472

    Article  CAS  PubMed  Google Scholar 

  • Karageordou P, Manetas Y (2006) The importance of being red when young: anthocyanins and the protection of young leaves of Quercus coccifera from insect herbivory and excess light. Tree Physiol 26(5):613–621

    Article  Google Scholar 

  • Khan MR, Hu JY, He CY (2012) Plant hormones including ethylene are recruited in calyx inflation in Solanaceous plants. J Plant Physiol 169:940–948

    Article  CAS  PubMed  Google Scholar 

  • Koyanagi M, Terakita A (2014) Diversity of animal opsin-based pigments and their optogenetic potential. Biochimica et Biophysica Acta (BBA) –. Bioenergetics 1837(5):710–716

    Article  CAS  Google Scholar 

  • Landi M, Tattini M, Gould KS (2015) Multiple functional roles of anthocyanins in plant-environment interactions. Environ Exp Bot 119:4–17

    Article  CAS  Google Scholar 

  • Lee S, Kim JH, Yoo ES, Lee CH, Hirochika H, An GH (2005) Differential regulation of chlorophyll a oxygenase genes in rice. Plant Mol Biol 57(6):805–818

    Article  CAS  PubMed  Google Scholar 

  • Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967

    Article  CAS  PubMed  Google Scholar 

  • Li YL, Xiong XY, Yu XY, He CZ, Lü CP, Yuan FR, Zhu JH (2010) Biological characteristics of variegated bud sports of Loropetalum chinense var. rubrum. Scientia Silvae Sinicae 46(8):56–61 (In Chinese with English abstract)

    Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Method. Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu Q, Xu J, Liu YZ, Zhao XL, Deng XX, Guo LL, Gu JQ (2007) A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck). J Exp Bot 58(15/16):4161–4171

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Zhu A, Chai LJ, Zhou WJ, Yu KQ, Ding J, Xu J, Deng XX (2009) Transcriptome analysis of a spontaneous mutant in sweet orange [Citrus sinensis (L.) Osbeck] during fruit development. J Exp Bot 60(3):801–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△CT method. Method 25:402–408

    Article  CAS  Google Scholar 

  • Ma G, Zhang LC, Kato M, Yamawaki K, Kiriiwa Y, Yahata M, Ikoma Y, Matsumoto H (2015a) Effect of the combination of ethylene and red LED light irradiation on carotenoid accumulation and carotenogenic gene expression in the flavedo of citrus fruit. Postharvest Biol Technol 99:99–104

    Article  CAS  Google Scholar 

  • Ma PY, Bian XF, Jia ZD, Guo XD, Xie YZ (2015b) De novo sequencing and comprehensive analysis of the mutant transcriptome from purple sweet potato (Ipomoea batatas L.). Gene 575(2):641–649

    Article  PubMed  Google Scholar 

  • Macrobbie EAC (1992) Calcium and ABA-induced stomatal closure. Phil Transact R Soc Lond B 338(1283):5–18

    Article  CAS  Google Scholar 

  • Matile P (2000) Biochemistry of Indian summer: physiology of autumnal leaf coloration. Exp Gerontol 35:145–158

    Article  CAS  PubMed  Google Scholar 

  • Mishra A, Khare S, Trivedi PK, Nath P (2008) Ethylene induced cotton leaf abscission is associated with higher expression of cellulose (GhCell) and increased activities of ethylene biosynthesis enzymes in abscission zone. Plant Physiol Biochem 46:54–63

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Bio l56:165–185

  • Ono M, Iwashina T (2015) Quantitative flavonoid variation accompanied by change of flower colors in EDEGworthia chrysantha, Pittosporum tobira and Wisteria floribunda. Natural Product Communications 10(3):413–416

    PubMed  Google Scholar 

  • Pietrini F, Iannelli MA, Massacci A (2002) Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photo-inhibitory risks at low temperature, without further limitation to photosynthesis. Plant, Cell Environ 25:1251–1259

    Article  CAS  Google Scholar 

  • Pirie A, Mullins MG (1976) Changes in anthocyanin and phenolics content of grapevine leaf and fruit tissues treated with sucrosenitrate abscisic acid. Plant Physiol 58:468–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravaglia D, Espley RV, Henry-Kirk RA, Andreotti C, Ziosi V, Hellens RP, Costa G, Allan AC (2013) Transcriptional regulation of flavonoid biosynthesis in nectarine (Prunus persica) by a set of R2R3 MYB transcription factors. BMC Plant Biol 13:68–82

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta 1807:375–383

    Article  CAS  PubMed  Google Scholar 

  • Rodrigo MJ, Zacarias L (2007) Effect of postharvest ethylene treatment on carotenoid accumulation and the expression of carotenoid biosynthetic genes in the flavedo of orange (Citrus sinensis L. Osbeck) fruit. Postharvest Biol Technol 43(1):14–22

    Article  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Rudoi AB, Shcherbakov RA (1998) Analysis of the chlorophyll biosynthetic system in a chlorophyll b-less barley mutant. Photosynth Res 58:71-80

  • Santner A, Calderon-Villaobos LIA, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Schaberg PG, van den Berg AK, Murakami PF, Shane JB, Donnelly JR (2003) Factors influencing red expression in autumn foliage of sugar maple trees. Tree Physiol 23(5):325–333

    Article  CAS  PubMed  Google Scholar 

  • Shi T, GaO Z, Wang L, Zhang Z, Zhuang W, Sun H, Zhong W (2012) Identification of differentially-expressed genes associated with pistil abortion in Japanese apricot by genome-wide transcriptional analysis. PLoS One 7:e47810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Springob K, Nakajima J, Yamazaki M, Saito K (2003) Recent advances in the biosynthesis and accumulation of anthocyanins. Nat Prod Rep 20(3):288–303

    Article  CAS  PubMed  Google Scholar 

  • Tan H, Liu XH, Ma N, Xue JQ, Lu WJ, Bai JH, Gao JP (2006) Ethylene-influenced flower opening and expression of genes encoding Etrs, Ctrs, and Ein3 s in two cut rose cultivars. Postharvest Biol Technol 40:97–105

    Article  CAS  Google Scholar 

  • Taylor LP, Briggs WR (1990) Genetic regulation and photocontrol of anthocyanin accumulation in maize seedlings. Plant cell 2(2):115–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuerck JA, Fromm ME (1994) Elements of the maize A1 promoter required for transactivation by the anthocyanin B/CI or phlobaphene P regulatory genes. Plant Cell 6(11):1655–1663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ubi BE, Honda C, Bessho H, Kondo S, Wada M, Kobayashi S, Moriguchi T (2006) Expression analysis of anthocyanin biosynthetic genes in apple skin: effect of UV-B and temperature. Plant Sci 170:571–578

    Article  CAS  Google Scholar 

  • Van Doorn WG (2002) Effect of ethylene on flower abscission: a survey. Ann Bot 89(6):689–693

    Article  PubMed  Google Scholar 

  • Walker AR, Lee E, Robinson SP (2006) Two new grape cultivars, bud sports of Cabernet Sauvignon bearing pale-coloured berries, are the result of deletion of two regulatory genes of the berry colour locus. Plant Mol Biol 62:623–635

    Article  CAS  PubMed  Google Scholar 

  • Wei YZ, Hu FC, Hu GB, Li XJ, Huang XM, Wang HC (2011) Differential expression of anthocyanin biosynthetic genes in relation to anthocyanin accumulation in the pericarp of Litchi chinensis Sonn. PLoS ONE 6(4):e19455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wettstein DV, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7(7):1039–1057

    Article  Google Scholar 

  • Xu XM, Zhang RX, Tang YL (2004) Effects of low content of chlorophyll distribution of absorbed light energy in leaves of mutant rice. Scientia Agricultural Sinica 37:339–343 (in Chinese, with English abstract)

  • Xu P, Liu ZW, Fan XQ, Gao J, Zhang XG, Shen XL (2013) De novo transcriptome sequencing and comparative analysis of differentially expressed genes in Gossypium aridum under salt stress. Gene 525:26–34

    Article  CAS  PubMed  Google Scholar 

  • Zhang F, Wan XQ, Zhong Y (2014) Nitrogen as an important detoxification factor to cadmium stress in poplar plants. J Plant Interact 9(1):249–258

    Article  CAS  Google Scholar 

  • Zhao ZC, Hu GB, Hu FC, Wang HC, Yang ZY, Lai B (2012) The UDP glucose: flavonoid-3-O-glucosyltransferase (UFGT) gene regulates anthocyanin biosynthesis in litchi (Litchi chinesis Sonn.) during fruit coloration. Mol Biol Rep 39(6):6409–6415

    Article  CAS  PubMed  Google Scholar 

  • Zhao CL, Chen ZJ, Bai XS, Ding C, Long TJ, Wei FG, Miao KR (2014) Structure-activity relationships of anthocyanidin glycosylation. Mol Divers 18(3):687–700

    Article  CAS  PubMed  Google Scholar 

  • Zheng QF, Song J, Campbell-Palmer L, Thompson K, Li L, Walker B, Cui YS, Li XH (2013) A proteomic investigation of apple fruit during ripening and in response to ethylene treatment. J Proteom 93:276–294

    Article  CAS  Google Scholar 

  • Zivcak M, Brestic M, Balatova Z (2013) Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth Res 117:529–546

    Article  CAS  PubMed  Google Scholar 

  • Zykov KI (2000) Variations of flower coloration in garden rose sports. Biol Bull 27:462–470

    Google Scholar 

Download references

Acknowledgments

The authors thank Professor Cheng XJ and Zhou CS for providing the materials used in this study. This work was supported by the National Natural Science Fund of China (No. 31300514) and by the 12th Five Year Key Programs for forest breeding in Sichuan Province (No. 2011YZGG).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xueqin Wan.

Additional information

Communicated by J.-H. Liu.

An erratum to this article is available at http://dx.doi.org/10.1007/s11738-017-2406-9.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, F., Zhao, J., Wan, X. et al. From green to red: large-scale transcriptome comparison of a bud sport in poplar (Populus deltoides). Acta Physiol Plant 38, 244 (2016). https://doi.org/10.1007/s11738-016-2259-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-016-2259-7

Keywords

Navigation