Advertisement

Molecular Breeding

, 39:1 | Cite as

Candidates responsible for dwarf pear phenotype as revealed by comparative transcriptome analysis

  • Yuxiong Xiao
  • Caihong WangEmail author
  • Yike Tian
  • Shaolan Yang
  • Junling Shen
  • Qianqian Liu
  • Haiyue Zhang
Article
  • 77 Downloads

Abstract

Dwarfism is an important character in fruit production for intensive cultivation and effective orchard management. We previously located a single dominant gene at a narrow region on scaffold00074 of pear based on simple sequence repeat markers. To identify the gene and fully understand the different developmental processes, we conducted a transcriptomic analysis of the young apical stem between dwarf and standard pears. A total of 2170 differentially expressed genes (DEGs), of which 987 were down-regulated and 1183 were up-regulated, were determined. These DEGs were mainly involved in ribosome biogenesis, phenylpropanoid biosynthesis, photosynthesis, porphyrin and chlorophyll metabolism and DNA replication. Subsequently, a classical arabinogalactan protein 7-like gene (PCP021014) and a protein WVD2-like 7 gene (PCP021015) were identified as the most likely candidates for the PcDw locus on the basis of the DEGs and annotation of scaffold00074. Furthermore, we performed qRT-PCR to validate the expression patterns of 12 DEGs associated with the dwarf character. Our results provide a systemic viewpoint into the complex regulatory networks between the dwarf and standard pear phenotypes.

Keywords

Pear Dwarf Phenotype Transcriptome DEG PcDw 

Notes

Funding information

This study was supported by the National Natural Science Foundation of China (31372049) and the Funds for Modern Agricultural Industry Technology System in Shandong Province, China (SDAIT-06-06).

Compliance with ethical standards

Conflict of interest

The authors declare that we have no conflict of interest.

Supplementary material

11032_2018_907_MOESM1_ESM.docx (1.5 mb)
Online Resource 1 Phenotype of dwarf and standard pears. (DOCX 1507 kb)
11032_2018_907_MOESM2_ESM.xlsx (2.8 mb)
Online Resource 2 Expression values (FPKM values) of all annotated genes in Pyrus communis (XLSX 2845 kb)
11032_2018_907_MOESM3_ESM.xls (91 kb)
Online Resource 3 DEGs between dwarf and standard pears (XLS 91 kb)
11032_2018_907_MOESM4_ESM.xlsx (263 kb)
Online Resource 4 GO annotation of DEGs between dwarf and standard pears (XLSX 263 kb)
11032_2018_907_MOESM5_ESM.xlsx (12 kb)
Online Resource 5 GO enrichment of DEGs between dwarf and standard pears (XLSX 11 kb)
11032_2018_907_MOESM6_ESM.xlsx (9 kb)
Online Resource 6 KEGG enrichment of DEGs between dwarf and standard pears (XLSX 8 kb)
11032_2018_907_MOESM7_ESM.docx (303 kb)
Online Resource 7 KEGG maps of enriched KEGG pathways of DEGs between dwarf and standard pears (DOCX 303 kb)
11032_2018_907_MOESM8_ESM.xlsx (31 kb)
Online Resource 8 Differentially expressed transcription factor genes between dwarf and standard pears (XLSX 31 kb)
11032_2018_907_MOESM9_ESM.docx (13 kb)
Online Resource 9 Primer sequences for qRT-PCR testing in this study (DOCX 12 kb)
11032_2018_907_MOESM10_ESM.doc (61 kb)
Online Resource 10 Genes identified on scaffold00074 (DOC 61 kb)
11032_2018_907_MOESM11_ESM.docx (13 kb)
Online Resource 11 Differential expressed genes in scaffold00074 (DOCX 12 kb)

References

  1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402.  https://doi.org/10.1093/nar/25.17.3389 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anders S (2010) Analysing RNA-Seq data with the DESeq package. Mol Biol 43(4):1–17.  https://doi.org/10.1186/gb-2010-11-10-r106 CrossRefGoogle Scholar
  3. Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Res 32:115–119.  https://doi.org/10.1093/nar/gkh131 CrossRefGoogle Scholar
  4. Arro J, Cuenca J, Yang Y, Liang Z, Cousins P, Zhong GY (2017) A transcriptome analysis of two grapevine populations segregating for tendril phyllotaxy. Hortic Res 4:17032.  https://doi.org/10.1038/hortres.2017.32 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene Ontology: tool for the unification of biology. Nat Genet 25:25–29.  https://doi.org/10.1038/75556 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bagnara GL, Rivalta L (1989) Dwarfing in pear. Acta Hortic 256:103–110.  https://doi.org/10.17660/ActaHortic CrossRefGoogle Scholar
  7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300Google Scholar
  8. Chagné D, Crowhurst RN, Pindo M, Thrimawithana A, Deng C, Ireland H, Fiers M, Dzierzon H, Cestaro A, Fontana P, Bianco L, Lu A, Storey R, Knäbel M, Saeed M, Montanari S, Kim YK, Nicolini D, Larger S, Stefani E, Allan AC, Bowen J, Harvey I, Johnston J, Malnoy M, Troggio M, Perchepied L, Sawyer G, Wiedow C, Won K, Viola R, Hellens RP, Brewer L, Bus VGM, Schaffer RJ, Gardiner SE, Velasco R (2014) The draft genome sequence of European pear (Pyrus communis L.‘Bartlett’). PLoS One 9:e92644.  https://doi.org/10.1371/journal.pone.0092644 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta 1819:120–128.  https://doi.org/10.1016/j.bbagrm.2011.09.002 CrossRefPubMedGoogle Scholar
  10. Chen B, Wang C, Tian Y, Chu Q, Hu C (2015) Anatomical characteristics of young stems and mature leaves of dwarf pear. Sci Hortic 186:172–179.  https://doi.org/10.1016/j.scienta.2015.02.025 CrossRefGoogle Scholar
  11. Deng YY, Li JQ, Wu SF, Zhu YP, Chen YW, He FC (2006) Integrated nr database in protein annotation system and its localization. Comput Eng 32:71–72Google Scholar
  12. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38(suppl_2):W64–W70.  https://doi.org/10.1093/nar/gkq310 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Goicoechea M, Lacombe E, Legay S, Mihaljevic S, Rech P, Jauneau A, Lapierre C, Pollet B, Verhaegen D, Chaubet-Gigot N, Grima-Pettenati J (2005) EgMYB2, a new transcriptional activator from Eucalyptus xylem, regulates secondary cell wall formation and lignin biosynthesis. Plant J 43:553–567.  https://doi.org/10.1111/j.1365-313X.2005.02480.x CrossRefPubMedGoogle Scholar
  14. Goujon T, Sibout R, Eudes A, Mackay J, Jouanin L (2003) Genes involved in the biosynthesis of lignin precursors in Arabidopsis thaliana. Plant Physiol Biochem 41:677–687.  https://doi.org/10.1016/S0981-9428(03)00095-0 CrossRefGoogle Scholar
  15. Guo J, Zhang Y, Hui M, Cheng Y, Zhang E, Xu Z (2016) Transcriptome sequencing and de novo analysis of a recessive genic male sterile line in cabbage (Brassica oleracea L. var. capitata). Mol Breed 36:117.  https://doi.org/10.1007/s11032-016-0542-3 CrossRefGoogle Scholar
  16. Han M, Sun Q, Zhou J, Qiu H, Guo J, Lu L, Mu W, Sun J (2017) Insertion of a solo LTR retrotransposon associates with spur mutations in ‘Red Delicious’ apple (Malus × domestica). Plant Cell Rep 36:1375–1385.  https://doi.org/10.1007/s00299-017-2160-x CrossRefPubMedGoogle Scholar
  17. Huang S, Liu Z, Yao R, Li D, Zhang T, Li X, Hou L, Wang Y, Tang X, Feng H (2016) Candidate gene prediction for a petal degeneration mutant, pdm, of the Chinese cabbage (Brassica campestris ssp. pekinensis) by using fine mapping and transcriptome analysis. Mol Breed 36:26.  https://doi.org/10.1007/s11032-016-0452-4 CrossRefGoogle Scholar
  18. Jensen PJ, Rytter J, Detwiler EA, Travis JW, McNellis TW (2003) Rootstock effects on gene expression patterns in apple tree scions. Plant Mol Biol 493:493–511.  https://doi.org/10.1023/B:PLAN.0000019122.90956.3b CrossRefGoogle Scholar
  19. Johnson FT, Zhu Y (2015) Transcriptome changes in apple peel tissues during CO2 injury symptom development under controlled atmosphere storage regimens. Hortic Res 2:15061.  https://doi.org/10.1038/hortres.2015.61 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:277–280.  https://doi.org/10.1093/nar/gkh063 CrossRefGoogle Scholar
  21. Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36:94–104.  https://doi.org/10.1046/j.1365-313X.2003.01862.x CrossRefPubMedGoogle Scholar
  22. Kirschbaum MUF (2011) Does enhanced photosynthesis enhance growth? Lessons learned from CO2 enrichment studies. Plant Physiol 155:117–124.  https://doi.org/10.1104/pp.110.166819 CrossRefPubMedGoogle Scholar
  23. Kotera M (2012) The KEGG databases and tools facilitating omics analysis: latest developments involving human diseases and pharmaceuticals. Methods Mol Biol 802:19.  https://doi.org/10.1007/978-1-61779-400-1_2 CrossRefPubMedGoogle Scholar
  24. Liu Q, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406.  https://doi.org/10.1105/tpc.10.8.1391 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  26. Lockard RG, Schneider GW (1981) Stock and scion relationships and the dwarfing mechanism in apple. Hort Rev 3:315–375.  https://doi.org/10.1002/9781118060766 CrossRefGoogle Scholar
  27. Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87.  https://doi.org/10.1016/j.tplants.2004.12.010 CrossRefPubMedGoogle Scholar
  28. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655.  https://doi.org/10.1104/pp.109.138990 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Park MH, Suzuki Y, Chono M, Knox JP, Yamaguchi I (2003) CsAGP1, a gibberellin responsive gene from cucumber hypocotyls, encodes a classical arabinogalactan protein and is involved in stem elongation. Plant Physiol 131:1450–1459.  https://doi.org/10.1104/pp.015628 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Perrin RM, Wang Y, Yuen CYL, Will J, Masson PH (2007) WVD2 is a novel microtubule-associated protein in Arabidopsis thaliana. Plant J 49:961–971.  https://doi.org/10.1111/j.1365-313X.2006.03015.x CrossRefPubMedGoogle Scholar
  31. Serpe MD, Nothnagel EA (1994) Effects of Yariv phenylglycosides on Rosa cell suspensions: evidence for the involvement of arabinogalactan-proteins in cell proliferation. Planta 193:542–550.  https://doi.org/10.1007/BF02411560 CrossRefGoogle Scholar
  32. 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 https://www.ncbi.nlm.nih.gov/pubmed/10457020. Accessed Jan 2017
  33. Singh K, Foley RC, Oñatesánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436.  https://doi.org/10.1016/S1369-5266(02)00289-3 CrossRefPubMedGoogle Scholar
  34. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:273–278.  https://doi.org/10.1016/j.pbi.2009.12.002 CrossRefGoogle Scholar
  35. Song C, Zhang D, Zhang J, Zheng L, Zhao C, Ma JJ, An N, Han M (2016) Expression analysis of key auxin synthesis, transport, and metabolism genes in different young dwarfing apple trees. Acta Physiol Plant 38:38–43.  https://doi.org/10.1007/s11738-016-2065-2 CrossRefGoogle Scholar
  36. Sun W, Kieliszewski MJ, Showalter AM (2004) Overexpression of tomato LeAGP-1 arabinogalactan-protein promotes lateral branching and hampers reproductive development. Plant J 40:870–881.  https://doi.org/10.1111/j.1365-313X.2004.02274.x CrossRefPubMedGoogle Scholar
  37. Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36.  https://doi.org/10.1093/nar/28.1.33 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859.  https://doi.org/10.1038/nrm2020 CrossRefPubMedGoogle Scholar
  39. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515.  https://doi.org/10.1038/nbt.1621 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Trapnell C, Roberts A, Goff L, Pertea G, Kim D et al (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562.  https://doi.org/10.1038/nprot.2012.016 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Van Hooijdonk B, Woolley D, Warrington I, Tustin D (2010) Initial alteration of scion architecture by dwarfing apple rootstocks may involve shoot-root-shoot signaling by auxin, gibberellin, and cytokinin. J Hortic Sci Biotechnol 85:59–65.  https://doi.org/10.1080/14620316.2010.11512631 CrossRefGoogle Scholar
  42. Wang C, Tian Y, Buck EJ, Gardiner SE, Dai H, Jia Y (2011) Genetic mapping of PcDw determining pear dwarf trait. J Am Soc Hortic Sci 136:48–53Google Scholar
  43. Wang CH, Li W, Tian YK, Hou DL, Bai MD (2016) Development of molecular markers for genetic and physical mapping of the PcDw locus in pear (Pyrus communis L.). J Hortic Sci Biotechnol 91:299–307.  https://doi.org/10.1080/14620316.2016.1155319 CrossRefGoogle Scholar
  44. Wertheim SJ (2002) Rootstocks for European pear: a review. Acta Hortic 596:299–309.  https://doi.org/10.17660/ActaHortic.2002.596.47 CrossRefGoogle Scholar
  45. Willats WGT, Knox JP (1996) A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of ß-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J 9:919–925.  https://doi.org/10.1046/j.1365-313X.1996.9060919.x CrossRefPubMedGoogle Scholar
  46. Ye J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297.  https://doi.org/10.1093/nar/gkl031 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Yuen CY, Pearlman RS, Silo-Suh L, Hilson P, Carroll KL, Masson PH (2003) WVD2 and WDL1 modulate helical organ growth and anisotropic cell expansion in Arabidopsis. Plant Physiol 131:493–506.  https://doi.org/10.1104/pp.015966 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Zhang Y, Yang J, Showalter AM (2011) AtAGP18 is localized at the plasma membrane and functions in plant growth and development. Planta 233:675–683.  https://doi.org/10.1007/s00425-010-1331-6 CrossRefPubMedGoogle Scholar
  49. Zhu L, Ni W, Liu S, Cai B, Xing H, Wang S (2017) Transcriptome analysis of apple leaves in response to Alternaria alternate apple pathotype infection. Front Plant Sci 8:22.  https://doi.org/10.3389/fpls.2017.00022 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of HorticultureQingdao Agricultural UniversityQingdaoChina
  2. 2.Qingdao Key Laboratory of Genetic Improvement and Breeding in Horticultural PlantsQingdaoChina

Personalised recommendations