Skip to main content
SpringerLink
Log in

Transcriptome analysis provides new insights into leaf shape variation in birch

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

The present study revealed many functional molecules for leaf splitting during the apical bud development and the switch development from the apical buds to leaf marginal tissues.

Abstract

The lobe, an important character of leaf architecture, is present in Betula pendula ‘Dalecarlica’. The presence of split lobes is of great significance in plant growth and development. The molecular mechanisms underlying leaf shape variation remains poorly understood in birch. Herein, the plants of B. pendula and B. pendula ‘Dalecarlica’ were designated as O (original variety) and V (variety), respectively. We performed transcriptome sequencing on the plant materials of apical buds from O (OSAM), apical buds from V (VSAM), leaf sinus from O (OS), leaf margin from O (OM), leaf sinus from V (VS) and lobe from V (VL) to uncover the candidate genes for sculpturing leaf margin. Analysis of the differential transcripts revealed 37 genes between OSAM and VSAM, 3702 genes between VSAM and VS, 3624 genes between VSAM and VL, 1731 genes between OSAM and OS, 1678 genes between OSAM and OM, 9 genes between VS and VL, 67 genes between OS and VS, and 45 genes between OM and VL. Functional analysis of genes showed that many genes related to auxin synthesis, cell division and antioxidant defense were detected at the apical bud stage. Some genes involved in transcription factors, cell proliferation, and auxin synthesis and signaling response were recorded during the switch development from the apical buds to leaf marginal tissues. Moreover, one to three genes coding for glycine-rich proteins (GRPs) were observed in each comparative combination. Particularly, GRP homology was weakly expressed in VS and strongly expressed in VL. Overall, these discovered genes, especially GRPs, might contribute to the development of lobed leaves. Our study provides useful information for leaf shape modification of woody plants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Akashi T, Aoki T, Ayabe S (2005) Molecular and biochemical characterization of 2-hydroxyisoflavanone dehydratase. Involvement of carboxylesterase-like proteins in leguminous isoflavone biosynthesis. Plant Physiol 137:882–891

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bai L, Zhang G, Zhou Y, Zhang Z, Wang W, Du Y, Wu Z, Song C (2009) Plasma membrane-associated proline-rich extension-like receptor kinase 4, a novel regulator of Ca2+ signaling, is required for abscisic acid responses in Arabidopsis thaliana. Plant J 60:314–327

    CAS  PubMed  Google Scholar 

  • Barkoulas M, Galinha C, Grigg SP, Tsiantis M (2007) From genes to shape: regulatory interactions in leaf development. Curr Opin Plant Biol 10(6):660–666

    CAS  PubMed  Google Scholar 

  • Ben-Gera H, Dafna A, Alvarez JP, Bar M, Mauerer M, Ori N (2016) Auxin-mediated lamina growth in tomato leaves is restricted by two parallel mechanisms. Plant J 86(6):443–457

    CAS  PubMed  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Google Scholar 

  • Bian X, Qu C, Zhang M, Li Y, Han R, Jiang J, Liu G (2019) Transcriptome sequencing to reveal the genetic regulation of leaf margin variation at early stage in birch. Tree Genet Genomes 15:4

    Google Scholar 

  • Bilsborough G, Runions A, Barkoulas M, Jenkins H, Hasson A, Galinha C, Laufs P, Hay A, Prusinkiewicz P, Tsiantis M (2011) Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci USA 108:3424–3429

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biswal AK, Atmodjo MA, Li M, Baxter HL, Yoo CG, Pu Y, Lee YC, Mazarei M, Black IM, Zhang JY, Ramanna H, Bray AL, King ZR, LaFayette PR, Pattathil S, Donohoe BS, Mohanty SS, Ryno D, Yee K, Thompson OA, Rodriguez M Jr, Dumitrache A, Natzke J, Winkeler K, Collins C, Yang X, Tan L, Sykes RW, Gjersing EL, Ziebell A, Turner GB, Decker SR, Hahn MG, Davison BH, Udvardi MK, Mielenz JR, Davis MF, Nelson RS, Parrott WA, Ragauskas AJ, Neal Stewart C, Mohnen D Jr (2018) Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. Nat Biotechnol 36:249–257

    CAS  PubMed  Google Scholar 

  • Burnham R, Pitman N, Johnson K, Wilf P (2001) Habitat-related error in estimating temperatures from leaf margins in a humid tropical forest. Am J Bot 88:1096–1102

    CAS  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Report 11:113–116

    CAS  Google Scholar 

  • Chen X, Kim J (2009) Callose synthesis in higher plants. Plant Signal Behav 4(6):489–492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coon M, Vaz A, Bestervelt L (1996) Cytochrome P4502: peroxidative reactions of diversozymes. FASEB J 10:428–434

    CAS  PubMed  Google Scholar 

  • Dai X, Mashiguchi K, Chen Q, Kasahara H, Kamiya Y, Ojha S (2013) The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin-containing monooxygenase. J Biol Chem 288:1448–1457

    CAS  PubMed  Google Scholar 

  • Debernardi JM, Mecchia MA, Vercruyssen L, Smaczniak C, Kaufmann K, Inze D, Rodriguez RE, Palatnik JF (2014) Post-transcriptional control of GRF transcription factors by microRNA miR396 and GIF co-activator affects leaf size and longevity. Plant J 79:413–426

    CAS  PubMed  Google Scholar 

  • Demeulenaere MJ, Beeckman T (2014) The interplay between auxin and cell cycle during plant development. In: Zažímalová E, Petrášek J, Benková E (eds) Auxin and its role in plant development. Springer, Vienna, pp 119–141

    Google Scholar 

  • Dolph G (1979) Variation in leaf margin with respect to climate in Costa Rica. Bull Torrey Bot Club 106:104–109

    Google Scholar 

  • Doong RL, Mohnen D (1998) Solubilization and characterization of a galacturonyltransferase that synthesizes the pectic polysaccharide homogalacturonan. Plant J 13(3):363–374

    CAS  Google Scholar 

  • Endo M, Shimizu H, Araki T (2016) Rapid and simple isolation of vascular, epidermal and mesophyll cells from plant leaf tissue. Nat Protoc 11(8):1388–1395

    CAS  PubMed  Google Scholar 

  • Exner V, Taranto P, Schönrock N, Gruissem W, Hennig L (2006) Chromatin assembly factor CAF-1 is required for cellular differentiation during plant development. Development 133(21):4163–4172

    CAS  PubMed  Google Scholar 

  • Eyüboglu B, Pfister K, Haberer G, Chevalier D, Fuchs A, Mayer KF, Schneitz K (2007) Molecular characterization of the STRUBBELIG-RECEPTOR FAMILY of genes encoding putative leucine-rich repeat receptor-like kinases in Arabidopsis thaliana. BMC Plant Biol 7:16

    PubMed  PubMed Central  Google Scholar 

  • Fang L, Zhao F, Cong Y, Sang X, Du Q, Wang D, Li Y, Ling Y, Yang Z, He G (2012) Rolling-leaf 14 is a 2OG-Fe(II) oxygenase family protein that modulates rice leaf rolling by affecting secondary cell wall formation in leaves. Plant Biotechnol J 10:524–532

    CAS  PubMed  Google Scholar 

  • Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31(6):713–727

    CAS  PubMed  Google Scholar 

  • Fleishon S, Shani E, Ori N, Weiss D (2011) Negative reciprocal interactions between gibberellin and cytokinin in tomato. New Phytol 190:609–617

    CAS  PubMed  Google Scholar 

  • Fujimori N, Suzuki N, Nakajima Y, Suzuki S (2014) DNA-damage-repair/toleration protein repairs UV-B-induced DNA damage. DNA Repair 21:171–176

    CAS  PubMed  Google Scholar 

  • Gao X, Zhang Y, Liu C, Dou B, Gai S (2018) Cloning of somatic embryogenesis receptor-like kinase gene PsSERK2 and cell division rate analysis during dormancy release in tree Peony (Paeonia suffruticosa). Acta Hortic Sinica 45(3):511–518

    Google Scholar 

  • Gassmann W (2005) Natural variation in the Arabidopsis response to the avirulence gene hopPsyA uncouples the hypersensitive response from disease resistance. MPMI 18(10):1054–1060

    CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma FD, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guerrucci MA, Soldano H, Bellé R (1990) Sequence analysis of cell cycle control (cdc2) protein kinases among protein serine/threonine kinases. Biol Cell 70(1–2):1–8

    CAS  PubMed  Google Scholar 

  • Harder PA, Silverstein RA, Meier I (2000) Conservation of matrix attachment region-binding filament-like protein 1 among higher plants. Plant Physiol 122(1):225–234

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hardie DG (1999) Plant protein serine/threonine kinases: classification and functions. Annu Rev Plant Physiol Plant Mol Biol 50:97–131

    CAS  PubMed  Google Scholar 

  • Horiguchi G, Kim G, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordial of Arabidopsis thaliana. Plant J 43:68–78

    CAS  PubMed  Google Scholar 

  • Huang H, Chen S, Li H, Jiang J (2015) Next-generation transcriptome analysis in transgenic birch overexpressing and suppressing APETALA1 sheds lights in reproduction development and diterpenoid biosynthesis. Plant Cell Rep 34:1663–1680

    CAS  PubMed  Google Scholar 

  • Kang J, Dengler N (2002) Cell cycling frequency and expression of the homeobox gene ATHB-8 during leaf vein development in Arabidopsis. Planta 216:212–219

    CAS  PubMed  Google Scholar 

  • Kang J, Mizukami Y, Wang H, Fowke L, Dengler NG (2007) Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana. Planta 226:1207–1218

    CAS  PubMed  Google Scholar 

  • Karpov PA, Nadezhdina ES, Emets AI, Matusov VG, Nyporko AIu, Shashina NIu, I Blium (2009) Bioinformatic search of plant protein kinases, participating in microtubule protein phosphorylation and cell division regulation. Tsitol Genet 43(3):63–79

    CAS  PubMed  Google Scholar 

  • Kasprzewska A, Carter R, Swarup R, Bennett M, Monk N, Hobbs JK, Fleming A (2015) Auxin influx importers modulate serration along the leaf margin. Plant J 83:705–718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keating RC (2009) Manual of leaf architecture. Syst Bot 34(4):825

    Google Scholar 

  • Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. PNAS 101(36):13374–13379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Klumb EK, Arge LWP, do Amaral MN, Rickes LN, Benitez LC, Braga EJB, Bianchi VJ (2017) Transcriptome profiling of Prunus persica plants under flooding. Trees 31(4):1127–1135

    CAS  Google Scholar 

  • Koenig D, Bayer E, Kang J, Kuhlemeier C, Sinha N (2009) Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136:2997–3006

    CAS  PubMed  Google Scholar 

  • Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohme-Takagib M (2010) TCP transcription factors regulate the activities of asymmetric leaves1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22:3574–3588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B (2010) Aligning short sequencing reads with Bowtie. Curr Protoc Bioinform 32:11–17

    Google Scholar 

  • Larsen PB, Cancel J, Rounds M, Ochoa V (2007) Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta 225:1447–1458

    CAS  PubMed  Google Scholar 

  • Lee S, Lee BH, Jung J, Park SK, Song JT, Kim JH (2018) Growth-regulating factor and GRF-interacting factor specify meristematic cells of gynoecia and anthers. Plant Physiol 176:717–729

    CAS  PubMed  Google Scholar 

  • Li SF, Santini JM, Nicolaou O, Parish RW (1996) A novel myb-related gene from Arabidopsis thaliana. FEBS Lett 379:117–121

    CAS  PubMed  Google Scholar 

  • Li H, Zhou S, Zhao W, Su S, Peng Y (2009) A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol 69:337–346

    CAS  PubMed  Google Scholar 

  • Li Y, Shen A, Xiong W, Sun Q, Luo Q, Song T, Li Z, Luan W (2016a) Overexpression of OsHox32 results in pleiotropic effects on plant type architecture and leaf development in rice. Rice 9:46

    PubMed  PubMed Central  Google Scholar 

  • Li H, Wu D, Wang Z, Liu F, Liu G, Jiang J (2016b) BpMADS12 mediates endogenous hormone signaling: effect on plant development Betula platyphylla. Plant Cell Tissue Organ Cult 124(1):169–180

    CAS  Google Scholar 

  • Li R, Chen S, Liu G, Han R, Jiang J (2017) Characterization and identification of a woody lesion mimic mutant lmd, showing defence response and resistance to Alternaria alternate in birch. Sci Rep 7(1):11308

    PubMed  PubMed Central  Google Scholar 

  • Liscum E, Reed J (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    CAS  PubMed  Google Scholar 

  • Liu P, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN response factor10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146

    CAS  PubMed  Google Scholar 

  • Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136(2):223–236

    CAS  PubMed  Google Scholar 

  • Liu C, Xu H, Jiang J, Wang S, Liu G (2017) Analysis of the promoter features of BpCUC2 in Betula platyphylla × Betula pendula. Plant Cell Tissue Organ Cult 132(1):191–199

    Google Scholar 

  • Lu Y, Li C, Wang H, Chen H, Berg H, Xia Y (2011) AtPPR2, an Arabidopsis pentatricopeptide repeat protein, binds to plastid 23S rRNA and plays an important role in the first mitotic division during gametogenesis and in cell proliferation during embryogenesis. Plant J 67:13–25

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moon J, Hake S (2011) How a leaf gets its shape. Curr Opin Plant Biol 14:24–30

    CAS  PubMed  Google Scholar 

  • Mu H, Lin L, Liu G, Jiang J (2013) Transcriptomic analysis of incised leaf-shape determination in birch. Gene 531(2):263–269

    CAS  PubMed  Google Scholar 

  • Naz AA, Raman S, Martinez CC, Sinha NR, Schmitz G, Theres K (2013) Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato. PNAS 110(6):2401–2406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson D, Werck-Reichhart D (2011) A P450-centric view of plant evolution. Plant J 66:194–211

    CAS  PubMed  Google Scholar 

  • Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–2945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nogueira FTS, Sarkar AK, Chitwood DH, Timmermans MCP (2006) Organ polarity in plants is specified through the opposing activity of two distinct small regulatory RNAs. Cold Spring Harb Symp Quant Biol 71:157–164

    CAS  PubMed  Google Scholar 

  • Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I, Alvarez J, Blum E, Zamir D, Eshed Y (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39(6):787–791

    CAS  PubMed  Google Scholar 

  • Qu C, Bian X, Jiang J, Chen S, Liu G (2017) Leaf morphological characteristics and related gene expression characteristic analysis in Betula pendula ‘Dalecarlica’ and Betula pendula. J Beijing For Univ 39(8):9–16

    Google Scholar 

  • Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375

    CAS  PubMed  Google Scholar 

  • Ringli C, Keller B, Ryser U (2001) Glycine-rich proteins as structural components of plant cell walls. Cell Mol Life Sci 58(10):1430–1441

    CAS  PubMed  Google Scholar 

  • Ryser U, Schorderet M, Zhao GF, Studer D, Ruel K, Hauf G, Keller B (1997) Structural cell-wall proteins in protoxylem development: evidence for a repair process mediated by a glycine-rich protein. Plant J 12(1):97–111

    CAS  PubMed  Google Scholar 

  • Salojärvi J, Smolander O, Nieminen K, Rajaraman S, Safronov O, Safdari P, Lamminmäki A, Immanen J, Lan T, Tanskanen J, Rastas P, Amiryousefi A, Jayaprakash B, Kammonen JI, Hagqvist R, Eswaran G, Ahonen VH, Serra JA, Asiegbu FO, de Dios Barajas-Lopez J, Blande D, Blokhina O, Blomster T, Broholm S, Brosché M, Cui F, Dardick C, Ehonen SE, Elomaa P, Escamez S, Fagerstedt KV, Fujii H, Gauthier A, Gollan PJ, Halimaa P, Heino PI, Himanen K, Hollender C, Kangasjärvi S, Kauppinen L, Kelleher CT, Kontunen-Soppela S, Koskinen JP, Kovalchuk A, Kärenlampi SO, Kärkönen AK, Lim K, Leppälä J, Macpherson L, Mikola J, Mouhu K, Mähönen AP, Niinemets Ü, Oksanen E, Overmyer K, Palva ET, Pazouki L, Pennanen V, Puhakainen T, Poczai P, Possen BJHM, Punkkinen M, Rahikainen MM, Rousi M, Ruonala R, van der Schoot C, Shapiguzov A, Sierla M, Sipilä TP, Sutela S, Teeri TH, Tervahauta AI, Vaattovaara A, Vahala J, Vetchinnikova L, Welling A, Wrzaczek M, Xu E, Paulin LG, Schulman AH, Lascoux M, Albert VA, Auvinen P, Helariutta Y, Kangasjärvi J (2017) Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat Genet 49(6):904–912

    PubMed  Google Scholar 

  • Schenk MF, Thienpont CN, Koopman WJM, Gilissen LJWJ, Smulders MJM (2008) Phylogenetic relationships in Betula (Betulaceae) based on AFLP markers. Tree Genet Genomes 4:911–924

    Google Scholar 

  • Schmittgen T, Livak K (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108

    CAS  PubMed  Google Scholar 

  • Schuster S (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5(1):16–18

    CAS  PubMed  Google Scholar 

  • Shani E, Ben G, Shleizer B, Burko Y, Weiss D, Oril N (2010) Cytokinin regulates compound leaf development in tomato. Plant Cell 22:3206–3217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Siah CH, Namasivayam P, Mohamed R (2016) Transcriptome reveals senescing callus tissue of Aquilaria malaccensis, an endangered tropical tree, triggers similar response as wounding with respect to terpenoid biosynthesis. Tree Genet Genomes 12:33

    Google Scholar 

  • Stein M, Dittgen J, Sánchez-Rodríguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18(3):731–746

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang Y, Zhao C, Tan S, Xue H (2016) Arabidopsis Type II phosphatidylinositol 4-kinase PI4 Kγ5 regulates auxin biosynthesis and leaf margin development through interacting with membrane-bound transcription factor ANAC078. PLoS Genet 12(8):e1006252

    PubMed  PubMed Central  Google Scholar 

  • Tetsuro H, Mamoru S, Masahiro S (1997) Structure and subcellular localization of a small RNA-binding protein from tobacco. Plant J 12(1):215–221

    Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31:46–53

    CAS  PubMed  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Dimerization and DNA binding of auxin response factors. Plant J 19(3):309–319

    CAS  PubMed  Google Scholar 

  • Urbas P (2000) Adaptive and inevitable morphological of three herbaceous species in a multispecies community: field experiment with manipulated nutrients and light. Acta Oecol 2:139–147

    Google Scholar 

  • Valobra CP, James DJ (1990) In vitro shoot regeneration from leaf discs of Betula pendula‘Dalecarlica’ EM 85. Plant Cell Tissue Organ Cult 21:51–54

    Google Scholar 

  • Vogel S (2009) Leaves in the lowest and highest winds: temperature, force and shape. New Phytol 183:13–26

    PubMed  Google Scholar 

  • Wang H, Chen J, Wen J, Tadege M, Li G, Liu Y, Mysore KS, Ratet P, Chen R (2008) Control of compound leaf development by floricaula/leafy ortholog single leaflet1 in Medicago truncatula. Plant Physiol 146:1759–1772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    PubMed  Google Scholar 

  • Wang W, Xu B, Wang H, Li J, Huang H, Xu L (2011) YUCCA Genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiol 157:1805–1819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Seo J, Gao S, Cui X, Jin H (2017) Silencing of AtRAP, a target gene of a bacteria-induced small RNA, triggers antibacterial defense responses through activation of LSU2 and down-regulation of GLK1. New Phytol 215:1144–1155

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weimer AK, Nowack MK, Bouyer D, Zhao X, Harashima H, Naseer S, Winter FD, Dissmeyer N, Geldner N, Schnittgera A (2012) Retinoblastoma related1 regulates asymmetric cell divisions in Arabidopsis. Plant Cell 24:4083–4095

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu W, Han R, Xu S, Jiang J, Liu G (2017) Expression of BpIAA10 from Betula platyphylla (birch) is differentially regulated by different hormones and light intensities. Plant Cell Tissue Organ Cult 132(2):371–381

    Google Scholar 

  • Yamaguchi T, Nukazuka A, Tsukaya H (2012) Leaf adaxial–abaxial polarity specification and lamina outgrowth: evolution and development. Plant Cell Physiol 53(7):1180–1194

    CAS  PubMed  Google Scholar 

  • Yan T, Chen M, Shen Q, Li L, Fu X, Pan Q, Tang Y, Shi P, Lv Z, Jiang W, Ma Y, Hao X, Sun X, Tang K (2016) Homeodomain protein 1 is required for jasmonate mediated glandular trichome initiation in Artemisia annua. New Phytol 213(3):1145–1155

    PubMed  Google Scholar 

  • Yanai O, Shalli E, Russ D, Ori N (2011) Gibberellin partly mediates lanceolate activity in tomato. Plant J 68:571–582

    CAS  PubMed  Google Scholar 

  • Yang G, Chen S, Jiang J (2015) Transcriptome analysis reveals the role of BpGH3.5 in root elongation of Betula platyphylla × Betula pendula. Plant Cell Tissue Organ Cult 121:605–617

    CAS  Google Scholar 

  • Yang Y, Li M, Yi Y, Li R, Dong C, Zhang Z (2018) The root transcriptome of Achyranthes bidentata and the identification of the genes involved in the replanting benefit. Plant Cell Rep 37:611–625

    CAS  PubMed  Google Scholar 

  • Yano S, Terashima I (2001) Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in Chenopodium album. Plant Cell Physiol 42(12):1303–1310

    CAS  PubMed  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq accounting for selection bias. Genome Biol 11:R14

    PubMed  PubMed Central  Google Scholar 

  • Zhang X, Facette M, Humphries JA, Shen Z, Park Y, Sutimantanapi D, Sylvester AW, Briggs SP, Smith LG (2012) Identification of PAN2 by quantitative proteomics as a leucine-rich repeat-receptor-like kinase acting upstream of PAN1 to polarize cell division in maize. Plant Cell 24(11):4577–4589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Lu Z, He X, Mughal MN, Fang R, Zhou Y, Zhao J, Gasser RB, Grevelding CG, Ye Q, Hu M (2018) Serine/threonine protein phosphatase 1 (PP1) controls growth and reproduction in Schistosoma japonicum. FASEB 7:6626–6642

    Google Scholar 

  • Zhou C, Hou C, Metelli A, Qi L, Tadege M, Mysore K, Wang Z (2011) Developmental analysis of a Medicago truncatula smooth leaf margin1 mutant reveals context-dependent effects on compound leaf development. Plant Cell 23:2106–2124

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Li H, Guo D, Wang Y, Dai H, Mei W, Peng S (2018) Identification, characterization and expression analysis of genes involved in steroidal saponin biosynthesis in Dracaena cambodiana. J Plant Res 131(3):555–562

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are very grateful to Professor Hairong Wei in Michigan Technological University (Houghton, USA) for the experimental design and sequencing analyses. This work was financially supported by the following foundations: (1) National Natural Science Foundation of China (NSFC) (Grant No. 31670673); (2) The 111 Project (Grant No. B16010).

Author information

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040, People’s Republic of China

    Xiuyan Bian, Chang Qu, Manman Zhang, Jing Jiang & Guifeng Liu

  2. State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing, 100091, People’s Republic of China

    Chang Qu

  3. National Center for Protein Science Tsinghua Cryo-EM Facility, Tsinghua University, Beijing, 100084, People’s Republic of China

    Danyang Li

Authors
  1. Xiuyan Bian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chang Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manman Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Danyang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jing Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guifeng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guifeng Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability

Sequencing data are available through NCBI SRP145552, BioProjectPRJNA471028. They include paired-end reads in fastq format for 12 samples that were run on an Illumina Hiseq 2500 at the Novogene, Tianjin, China, July 2014. The samples were buds (SAMN09199122) and leaves (SAMN09199123) that were collected simultaneously from 3-year-old birch trees.

Additional information

Communicated by Carlson.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 59 kb)

Supplementary material 2 (DOCX 70 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bian, X., Qu, C., Zhang, M. et al. Transcriptome analysis provides new insights into leaf shape variation in birch. Trees 33, 1265–1281 (2019). https://doi.org/10.1007/s00468-019-01856-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-019-01856-z

Keywords

Search

Navigation