Skip to main content
Log in

Transcriptome sequencing to reveal the genetic regulation of leaf margin variation at early stage in birch

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Lobe, a visual description of leaf morphology, is present in Betula pendula ‘Dalecarlica’. Although works involving leaf dehiscence have been conducted, knowledge on the genetic regulation of leaf morphology diversity at early stage remains largely elusive. Here, based on the extent of leaf margin variability, trees of B. pendula ‘Dalecarlica’ were categorized into A, B, and C. Plant materials of the apical buds from B. pendula ‘Dalecarlica’ (ASAM, BSAM, and CSAM) and B. pendula (OSAM), and young leaves from B. pendula ‘Dalecarlica’ (AYL and BYL) and B. pendula (OYL) were sampled for transcriptome sequencing. Compared with OSAM, there were 81, 6, and 17 genes in ASAM, BSAM, and CSAM. The expression of 204 genes was altered in OYL relative to OSAM. Meanwhile, the transcripts of 182 genes were changed in BYL relative to BSAM. In contrast to OYL, 337 genes and 47 genes were differentially expressed in AYL and BYL, respectively. Moreover, 91 genes with transcript changes were detected in BYL, as compared to AYL. The differentially expressed genes were annotated as having roles in antioxidant defense, cell division, and auxin synthesis at the apical bud stage. During the transition development from the apical buds to young leaves, genes showed homology with important enzymes of cell division, auxin signaling, and photosynthesis. At young leaf stage, genes were mainly involved in cell division, auxin signaling, and photosynthesis. Overall, the genes identified in our transcriptome profiles played potential roles in producing leaf splitting. This study sheds light on the genetic regulation of incised leaves at early stage in birch, which can serve as references for guiding the genetic manipulation in sculpturing leaf organ boundary.

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
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Aida M, Ishida T, Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563–1570

    Article  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

    Article  Google Scholar 

  • Bhar A, Gupta S, Chatterjee M, Sen S, Das S (2017) Differential expressions of photosynthetic genes provide clues to the resistance mechanism during Fusarium oxysporum f.sp. ciceri race 1 (Foc1) infection in chickpea (Cicer arietinum L.). Eur J Plant Pathol 148(3):533–549

    Article  CAS  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 U S A 108:3424–3429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  CAS  PubMed  Google Scholar 

  • Boureau L, How-Kit A, Teyssier E, Drevensek S, Rainieri M, Joube’s J, Stammitti L, Pribat A, Bowler C, Hong Y, Gallusci P (2016) A CURLY LEAF homologue controls both vegetative and reproductive development of tomato plants. Plant Mol Biol 90:485–501

    Article  CAS  PubMed  Google Scholar 

  • Bowman JL, Floyd SK (2008) Patterning and polarity in seed plant shoots. Annu Rev Plant Biol 59:67–88

    Article  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

    Article  CAS  Google Scholar 

  • Chen S, Zhao H, Wang Z, Zheng C, Zhao P, Guan Z, Qin H, Liu A, Lin X, Ahammed GJ (2017) Trichoderma harzianum-induced resistance against Fusarium oxysporum involves regulation of nuclear DNA content, cell viability and cell cycle-related genes expression in cucumber roots. Eur J Plant Pathol 147(1):43–53

    Article  CAS  Google Scholar 

  • Chida H, Yazawa K, Hasezawa S, Iwai H, Satoh S (2007) Involvement of a tobacco leucine-rich repeat-extensin in cell morphogenesis. Plant Biotechnol 24:171–177

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cornet D, Sierra J, Bonhomme R (2007) Characterization of the photosynthetic pathway of some tropical food yams (Dioscorea spp.) using leaf natural 13C abundance. Photosynthetica 45(2):303–305

    Article  CAS  Google Scholar 

  • Das PK, Shin DH, Choi S, Yoo S, Choi G, Park Y (2012) Cytokinins enhance sugar-induced anthocyanin biosynthesis in Arabidopsis. Mol Cell 34:93–101

    Article  CAS  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

    Chapter  Google Scholar 

  • Dharmasiri N, Estelle M (2004) Auxin signaling and regulated protein degradation. Trends Plant Sci 9:302–308

    Article  CAS  PubMed  Google Scholar 

  • Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, Cervone F, Bellincampi D, Tsernoglou D (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17:849–858

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dinesh-Kumar SP, Tham W, Baker BJ (2000) Structure–function analysis of the tobacco mosaic virus resistance gene N. PNAS 97(26):14789–14794

    Article  CAS  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Galli M, Liu Q, Moss BL, Malcomber S, Li W, Gaines C, Federici S, Roshkovan J, Meeley R, Nemhauser JL, Gallavotti A (2015) Auxin signaling modules regulate maize inflorescence architecture. Proc Natl Acad Sci U S A 112(43):13372–13377

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo H, Wang Y, Hu P, Wang Y, Jiang Y, Yang C, Wang C (2016) Gene expression profiles in different stem internodes reveal the genetic regulation of primary and secondary stem development in Betula platyphylla. Tree Genet Genomes 12:113

    Article  Google Scholar 

  • Hage AE, Koper M, Kufel J, Tollervey D (2008) Efficient termination of transcription by RNA polymerase I requires the 5′exonuclease Rat1 in yeast. Genes Dev 22(8):1069–1081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Honta H, Inamura T, Konishi T, Satoh S, Iwai H (2018) UDP-arabinopyranose mutase gene expressions are required for the biosynthesis of the arabinose side chain of both pectin and arabinoxyloglucan, and normal leaf expansion in Nicotiana tabacum. J Plant Res 131:307–317

    Article  CAS  PubMed  Google Scholar 

  • Huang H, Wang S, Jiang J, Liu G, Li H, Chen S, Xu H (2014) Overexpression of BpAP1 induces early flowering and produces dwarfism in Betula platyphylla × Betula pendula. Physiol Plant 151:495–506

    Article  CAS  PubMed  Google Scholar 

  • Itoh J, Sato Y, Nagato Y, Matsuoka M (2006) Formation, maintenance and function of the shoot apical meristem in rice. Plant Mol Biol 60:827–842

    Article  CAS  PubMed  Google Scholar 

  • Ivanchenko MG, den Os D, Monshausen GB, Dubrovsky JG, Bednárová A, Krishnan N (2013) Auxin increases the hydrogen peroxide (H2O2) concentration in tomato (Solanum lycopersicum) root tips while inhibiting root growth. Ann Bot 112:1107–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwasaki M, Takahashi H, Iwakawa H, Nakagawa A, Ishikawa T, Tanaka H, Matsumura Y, Pekker I, Eshed Y, Vial-Pradel S, Ito T, Watanabe Y, Ueno Y, Fukazawa H, Kojima S, Machida Y, Machida C (2013) Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis. Development 140:1958–1969

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb CJ, Brisson L, Bradley DJ, Kjellbom P (1993) Stimulus-dependent oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response and control point in cellular maturation. In: Fritig B, Legrand M (eds) Mechanisms of plant defense responses. Developments in plant pathology, vol 2. Springer, Dordrecht

    Google Scholar 

  • Lammers M, Follmann H (2007) The ribonucleotide reductases—a unique group of metalloenzymes essential for cell proliferation. Inorganic elements in. biochemistry 54:27–91

    Google Scholar 

  • Langmead B (2010) Aligning short sequencing reads with bowtie. Curr Protoc Bioinformatics, chapter 11, Unit 11.7

  • Leegood RC, Sharkey TD, von Caemmerer S (2000) Photosynthesis: physiology and metabolism. Advances in photosynthesis, volume 9, Kluwer Academic Publishers, AA Dordrecht, p 624

  • Leyser O (2001) Auxin signalling: the beginning, the middle and the end. Curr Opin Plant Biol 4(5):382–386

    Article  CAS  PubMed  Google Scholar 

  • Li H, Zeng X, Liu ZQ, Meng QT, Yuan M, Mao TL (2009a) Arabidopsis microtubule-associated protein AtMAP65-2 acts as a microtubule stabilizer. Plant Mol Biol 69:313–324

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lim PO, Lee IC, Kim J, Kim HJ, Ryu JS, Woo HR, Nam HG (2010) Auxin response factor 2 (ARF2) plays a major role in regulating auxin-mediated leaf longevity. J Exp Bot 61(5):1419–1430

    Article  CAS  PubMed  PubMed Central  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

    Article  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

    Article  CAS  Google Scholar 

  • Lloyd C, Hussey P (2001) Microtubule-associated proteins in plants—why we need a MAP. Nat Rev Mol Cell Biol 2:40–47

    Article  CAS  PubMed  Google Scholar 

  • Lomax J (2005) Get ready to GO! A biologist’s guide to the gene ontology. Brief Bioinform 6:298–304

    Article  CAS  PubMed  Google Scholar 

  • Ludwig M (2013) Evolution of the C4 photosynthetic pathway: events at the cellular and molecular levels. Photosynth Res 117:147–161

    Article  CAS  PubMed  Google Scholar 

  • McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709–713

    Article  CAS  PubMed  Google Scholar 

  • Millner PA (1995) The auxin signal. Curr Opin Cell Biol 7:224–231

    Article  CAS  PubMed  Google Scholar 

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52:89–118

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nakayama H, Nakayama N, Seiki S, Kojima M, Sakakibara H, Sinha N, Kimura S (2014) Regulation of the KNOX-GA gene module induces heterophyllic alteration in north American lake cress. Plant Cell 26:4733–4748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nicotra AB, Leigh A, Boyce CK, Jones CS, Niklas KJ, Royer DL, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38:535–552

    Article  PubMed  Google Scholar 

  • Nisler J, Kopečný D, Končitíková R, Zatloukal M, Bazgier V, Berka K, Zalabák D, Briozzo P, Strnad M, Spíchal L (2016) Novel thidiazuron-derived inhibitors of cytokinin oxidase/dehydrogenase. Plant Mol Biol 92:235–248

    Article  CAS  PubMed  Google Scholar 

  • Obroucheva NV (2008) Cell elongation as an inseparable component of growth in terrestrial plants. Russ J Dev Biol 39(1):13–24

    Article  Google Scholar 

  • Pan Y, Wang X, Liu H, Zhang G, Ma Z (2010) Molecular cloning of three UDP-Glucuronate decarboxylase genes that are preferentially expressed in gossypium fibers from elongation to secondary cell wall synthesis. J Plant Biol 53:367–373

    Article  CAS  Google Scholar 

  • Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu Y, X J, Du L, Poovaiah B (2012) The function of calreticulin in plant immunity. Plant Signal Behav 7(8):907–910

    Article  CAS  PubMed  PubMed Central  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

  • Rienzo FD, Gabdoulline RR, Menziani MC, Wade RC (2000) Blue copper proteins: a comparative analysis of their molecular interaction properties. Protein Sci 9:1439–1454

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato S, Fujita N, Tsuruo T (2002) Regulation of kinase activity of 3-phosphoinositide-dependent protein kinase-1 by binding to 14-3-3. J Biol Chem 277(42):39360–39367

    Article  CAS  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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Shani E, Yanai O, Ori N (2006) The role of hormones in shoot apical meristem function. Curr Opin Plant Biol 9:484–489

    Article  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

    Article  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

    Article  Google Scholar 

  • Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126:4117–4128

    Article  CAS  PubMed  Google Scholar 

  • Szakonyi D (2016) LEAFDATA: a literature-curated database for Arabidopsis leaf development. Plant Methods 12:15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13(4):178–182

    Article  CAS  PubMed  Google Scholar 

  • Tang Y, Zhao C, Tan S, Xue H (2016) Arabidopsis type II phosphatidylinositol 4-kinase PI4Kγ5 regulates auxin biosynthesis and leaf margin development through interacting with membrane-bound transcription factor ANAC078. PLoS Genet 12(8):e1006252

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57:477–496

    Article  CAS  PubMed  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

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Xu J, Nian J, Shen N, Lai K, Hu J, Zeng D, Ge C, Fang Y, Zhu L, Qian Q, Zhang G (2016) Characterization and fine mapping of the rice gene OsARVL4 regulating leaf morphology and leaf vein development. Plant Growth Regul 78:345–356

    Article  CAS  Google Scholar 

  • Wasteneys G, Galway M (2003) Remodeling the cytoskeleton for growth and form: an overview with some new views. Annu Rev Plant Biol 54:691–722

    Article  CAS  PubMed  Google Scholar 

  • Wei KF, Han P (2017) Comparative functional genomics of the TPR gene family in Arabidopsis, rice and maize. Mol Breed 37:152

    Article  CAS  Google Scholar 

  • Weijers D, Jürgens G (2005) Auxin and embryo axis formation: the ends in sight? Curr Opin Plant Biol 8:32–37

    Article  CAS  PubMed  Google Scholar 

  • Willemsen V, Scheres B (2004) Mechanisms of pattern formation in plant embryogenesis. Annu Rev Genet 38:587–614

    Article  CAS  PubMed  Google Scholar 

  • Wu T, Tian ZD, Liu J, Xie CH (2009) A novel leucine-rich repeat receptor-like kinase gene in potato, StLRPK1, is involved in response to diverse stresses. Mol Biol Rep 36:2365–2374

    Article  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

    Article  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

    Article  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Z, Zhang X (2012) Argonautes compete for miR165/166 to regulate shoot apical meristem development. Curr Opin Plant Biol 15:652–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Fowke LC, Wang H (2002) Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Rep 20:967–975

    Article  CAS  Google Scholar 

  • Zhou Y, Honda M, Zhu H, Zhang Z, Guo X, Li T, Li Z, Peng X, Nakajima K, Duan L, Zhang X (2015) Spatiotemporal sequestration of miR165/166 by Arabidopsis argonaute10 promotes shoot apical meristem maintenance. Plant Cell Rep 10:1819–1827

  • Zhou J, Zheng Z, Zhu X (2016) A mathematical model of the photosynthetic carbon metabolism has multiple steady states under the same parameter conditions. Acta Math Appl Sin Engl Ser 32(3):591–604

  • Zhu X, de Sturler E, Long SP (2007) Optimizing the distribution of resources between enzymes of carbon metabolism can dramatically increase photosynthetic rate: a numerical simulation using an evolutionary algorithm. Plant Physiol 145(2):513–526

    Article  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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Professor Hairong Wei in Michigan Technological University, Houghton, for the experimental design and English writing.

Funding

This work was financially supported by the following foundations: (1) National Natural Science Foundation of China (NSFC) (grant no. 31670673) and (2) the 111 Project (grant no. B16010).

Author information

Authors and Affiliations

Authors

Contributions

XB and CQ performed all the experiments. MZ, YL, and RH assisted with paraffin section and growth traits observation. GL and JJ together with XB designed the experiments and wrote the manuscript. The first two authors contributed equally to this work. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Guifeng Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

The raw read sequence data in FASTQ format was deposited in the National Centre for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database under the accession number SRP148344.

Additional information

Communicated by A. Brunner

Publisher’s Note

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

Key message

Transcriptome profiles revealed that the expression of genes important for antioxidant defense, cell division, and auxin synthesis during the apical bud development; cell division, auxin signaling, and photosynthesis during the transitional development from the apical buds to young leaves and during the development of young leaf, was altered in birch trees, which suggested leading roles of these identified genes in lobe formation.

Electronic supplementary material

ESM 1

(DOCX 91 kb)

ESM 2

(DOCX 1601 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 sequencing to reveal the genetic regulation of leaf margin variation at early stage in birch. Tree Genetics & Genomes 15, 4 (2019). https://doi.org/10.1007/s11295-018-1312-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-018-1312-7

Keywords

Navigation