Skip to main content
Log in

Characterization of Transcriptional Differences Between Columnar and Standard Apple Trees Using RNA-Seq

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

The columnar apple tree is a valuable resource for genetic improvement of cultivated apples due to its special architecture. To identify genes involved in the columnar architecture, expression profiles of newly developing shoots of standard and columnar trees from a segregating population of “Fuji” × “Telamon” have been analyzed using the new generation of high-throughput RNA-Seq technology. Following Blast analysis against Nr, SwissProt, KEGG, and COG databases, a total of 69,558 unigene annotations have been identified. Among them, more than 80.68% and 79.87% clean reads of Apple-Co and Apple-St samples, respectively, have been mapped to reference apple genome. Interestingly, 57% of genes were covered with more than 50% clean reads. Moreover, 1,252 and 1,443 unigenes from Apple-Co and Apple-St tissues, respectively, had alternative splicing sites. Among these, 614 and 666 were alternative 3′ splice sites and the most abundant, followed by alternative 5′ splice sites, while exon skipping sites were the least frequent. In addition, 13,142 and 13,334 novel transcript units were identified form Apple-Co and Apple-St samples, respectively. Moreover, analysis of RPKM (reads per kilobase per million reads) values found that expression of 5,237 unigenes differed by more than twofold. Among these, 1,359 were enriched in 232 metabolic pathways based on KEGG database annotation, and 2,233 were enriched in biological regulation, cellular process, etc. pathways based on GO functional annotation, and 287 unigenes were related with apple architecture. Among the 287 unigenes, 31 unigenes mapped to chromosome 10 of apple genome, and 25 unigenes were GRAS transcription factor, which were suggested to play an important role in architecture formation of columnar apple trees. Taking together, this study provided a theoretical basis for further enriching gene resources of important agronomic traits of fruit trees and for understanding the formation mechanism of columnar apple trees.

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

  • Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449

    Article  PubMed  CAS  Google Scholar 

  • Bruno VM, Wang Z, Marjani SL, Euskirchen GM, Martin J, Sherlock G, Snyder M (2010) Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-Seq. Genome Res 20:1451–1458. doi:10.1101/gr.109553.110

    Article  PubMed  CAS  Google Scholar 

  • Chen CM, Liu SQ, Hao XF, Chen GJ, CAO BH, Chen QH, Lei JJ (2011) Characterization of a pectin methylesterase gene homolog, CaPME1, expressed in anther tissues of Capsicum annuum L. Plant Mol Biol Rep. doi:10.1007/s11105-011-0358-6

  • Dai Y, Wang HZ, Li BH, Huang J, Liu XF, Zhou YH, Mou ZL, Li JY (2006) Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell 18:308–320

    Article  PubMed  CAS  Google Scholar 

  • Flachowsky H, Hättasch C, Höfer M, Peil A, Hanke MV (2010) Overexpression of LEAFY in apple leads to a columnar phenotype with shorter internodes. Planta 231:251–263

    Article  PubMed  CAS  Google Scholar 

  • Foo E, Buillier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17:464–474

    Article  PubMed  CAS  Google Scholar 

  • Gallavotti A, Zhao Q, Kyozuka J, Meeley RB, Ritter M, Doebley JF, Pe ME, Schmidt RJ (2004) The role of barren stalk1 in the architecture of maize. Nature 432:630–635

    Article  PubMed  CAS  Google Scholar 

  • Ge C, Cu X, Hu Y, Fu Z, Zhang D, Cheng Z, Li J (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194

    Article  PubMed  CAS  Google Scholar 

  • Greb T, Clarenz O, Schafer E, Muller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17:1175–1187

    Article  PubMed  CAS  Google Scholar 

  • He CY, Tian Y, Saedler R, Efremova N, Riss S, Khan MR, Yephremov A, Saedler H (2010) The MADS-domain protein MPF1 of Physalis floridana controls plant architecture, seed development and flowering time. Planta 231:767–777

    Article  PubMed  CAS  Google Scholar 

  • Hemmat M, Weeden NF, Conner PJ, Brown SK (1997) A DNA marker for columnar growth habit in apple contains a simple sequence repeat. J Am Soc Hort Sci 122:347–349

    CAS  Google Scholar 

  • Jiang BB, Miao HB, Chen SM, Zhang SM, Chen FD, Fang WM (2010) The Lateral Suppressor-like gene, DgLsL, alternated the axillary branching in transgenic chrysanthemum (Chrysanthemum × morifolium) by modulating IAA and GA content. Plant Mol Biol Rep 28:144–151. doi:10.1007/s11105-009-0130-3

    Article  CAS  Google Scholar 

  • Kim YC, Nakajima M, Nakayama A, Yamaguchi I (2005) Contribution of gibberellins to the formation of Arabidopsis seed coat through starch degradation. Plant Cell Physiol 46:1317–1325

    Article  PubMed  CAS  Google Scholar 

  • Komatsu K, Maekawa M, Ujiie S, Satake Y, Furutani I, Okamoto H, Shimamoto K, Kyozuka J (2003) LAX and SPA: major regulators of shoot branching in rice. Proc Natl Acad Sci USA 100:11765–11770

    Article  PubMed  CAS  Google Scholar 

  • Kuraparthy V, Sood S, Gill BS (2008) Genomic targeting and mapping of tiller inhibition gene (tin3) of wheat using ESTs and synteny with rice. Funct Integr Genomics 8:33–42

    Article  PubMed  CAS  Google Scholar 

  • Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131:4311–4322

    Article  PubMed  CAS  Google Scholar 

  • Li XY, Qian Q, Fu ZM, Wang YH, Xiong GS, Zeng DL, Wang XQ, Liu XF, Teng S, Hiroshi F (2003) Control of tillering in rice. Nature 422:618–621

    Article  PubMed  CAS  Google Scholar 

  • Li HY, Liu FF, Liu GF, Wang S, Guo XH, Jing J (2011) Molecular cloning and expression analysis of 13 MADS-Box genes in Betula platyphylla. Plant Mol Biol Rep. doi:10.1007/s11105-011-0326-1

  • Otsuga D, De Guzman B, Prigge MJ, Drews GN, Clark SE (2001) REVOLUTA regulates meristem initiation at lateral positions. Plant J 25:223–236

    Article  PubMed  CAS  Google Scholar 

  • Qiao F, Zhao KJ (2011) The influence of RNAi targeting of OsGA20ox2 gene on plant height in rice. Plant Mol Biol Rep 29:952–960. doi:10.1007/s11105-011-0309-2

    Article  CAS  Google Scholar 

  • Rossini L, Vecchietti A, Nicoloso L, Stein N, Franzago S, Salamini F, Pozzi C (2006) Candidate genes for barley mutants involved in plant architecture: an in silico approach. Theor Appl Genet 112:1073–1085

    Article  PubMed  CAS  Google Scholar 

  • Schumacher K, Schmitt T, Rossberg M (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA 96:290–295

    Article  PubMed  CAS  Google Scholar 

  • Takeda T, Suwa Y, Suzuki M, Kitano H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M, Ueguchi C (2003) The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33:513–520

    Article  PubMed  CAS  Google Scholar 

  • Tian YK, Wang CH, Zhang JS, James C, Dai HY (2005) Mapping Co, a gene controlling the columnar phenotype of apple, with molecular markers. Euphytica 145:181–188. doi:10.1007/s10681-005-1163-9

    Article  CAS  Google Scholar 

  • Umehara M, Hanada A, Yoshida S et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestarol A et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Guo GW, Wang C, Lin Y, Wang XN, Zhao MM, Guo Y, He MH, Zhang Y, Pan L (2010) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucleic Acids Res 38:5075–5087. doi:10.1093/nar/gkq256

    Article  PubMed  CAS  Google Scholar 

  • Watanabe M, Suzuki A, Komori S, Bessho H (2006) Effects of heading back pruning on shoot growth and IAA and cytokinins concentrations at bud burst of columnar-type apple trees. J Jap Soc Hort Sci 75:224–230

    Article  CAS  Google Scholar 

  • Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B (2004) CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131:915–922

    Article  PubMed  CAS  Google Scholar 

  • Xue J, Bao YY, Bl L, Cheng YB, Peng ZY, Liu H, Xu HJ, Zhu ZR, Lou YG, Cheng JA, Zhang CX (2010) Transcriptome analysis of the brown planthopper Nilaparvata lugens. PLoS One 5:e14233. doi:10.1371/journal.pone.0014233

    Article  PubMed  CAS  Google Scholar 

  • Zhuang J, Yao QH, Xiong AS, Zhang J (2011) Isolation, phylogeny and expression patterns of AP2-Like genes in apple (Malus × domestica Borkh). Plant Mol Biol Rep 29:209–216. doi:10.1007/s11105-010-0227-8

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by China Agriculture Research System Foundation (No. CARS-28-01-07), Shandong Provincial Young Scientist Foundation (No. BS2009NY023), Shandong Provincial Improved Variety Engineering System Foundation (No. 620902), Qingdao Scientific Research Foundation (No. 11-2-4-5-6-jch), and Qingdao Agricultural University Doctoral Foundation (No. 630732).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hongyi Dai.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig. S1

Morphological comparison of columnar with standard apple tree. a, c, f Standard apple trees. b, d, e, g Columnar apple tree. (JPEG 234 kb)

High Resolution (TIFF 1768 kb)

Supplementary Table S1

Candidate unigenes related to the architecture formation of apple trees. (DOC 54 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, Y., Zhu, J. & Dai, H. Characterization of Transcriptional Differences Between Columnar and Standard Apple Trees Using RNA-Seq. Plant Mol Biol Rep 30, 957–965 (2012). https://doi.org/10.1007/s11105-011-0396-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-011-0396-0

Keywords

Navigation