Advertisement

Plant Molecular Biology Reporter

, Volume 36, Issue 2, pp 210–224 | Cite as

Genome-Wide Identification, Classification, and Expression Analysis of SNARE Genes in Chinese Cabbage (Brassica rapa ssp. pekinensis) Infected by Turnip mosaic virus

  • Changwei Zhang
  • Shanwu Lyu
  • Liwei Gao
  • Xiaoming Song
  • Yanxiao Li
  • Xilin Hou
Original Paper
  • 171 Downloads

Abstract

Turnip mosaic virus (TuMV) is a widely distributed pathogen that seriously affects the yield and quality of brassica crops. The SNARE genes in the host encode proteins that are very important for virus replication and movement. However, systematic and comprehensive analyses of these genes have not been reported for Chinese cabbage. In the present study, 78 BrSNARE genes were identified in Chinese cabbage. We analyzed the classification of these genes, their phylogenetic relationships (including their orthologous and paralogous relationships with those in Arabidopsis and rice), conserved motifs, and distribution on the ten chromosomes of Chinese cabbage. Of the 78 BrSNAREs, 77 were unevenly distributed among ten chromosomes. In the phylogenetic analyses of SNARES from Chinese cabbage, Arabidopsis, and rice, the 78 BrSNAREs were classified into four subfamilies. Analyses of the transcript levels of BrSNAREs in six different tissues revealed tissue-specific expression of some BrSNARE genes. We detected the expression of 55 BrSNAREs and grouped them according to their change trends and subcellular location in different organelles. On the basis of our analyses, we concluded that nine BrSNAREs may be associated with cell-to-cell movement and 15 BrSNAREs may be associated with long-distance transport. These results indicate that many BrSNAREs have evolved in Chinese cabbage and that some of them are related to TuMV infection.

Keywords

Genome-wide analysis SNARE genes Turnip mosaic virus (TuMV) Expression pattern Chinese cabbage 

Abbreviations

CYT

cytoplasm

ER

endoplasmic reticulum

FPKM

kilobase of exon model per million mapped reads

GET pathway

guided entry of tail-anchored protein pathway

Golgi

Golgi apparatus

LF

least fractionated

MF1

medium fractionated

MF2

most fractionated

PVC

prevacuolar compartment

qRT-PCR

quantitative real-time PCR

SYP

syntaxin of plants

TGN

trans-Golgi network

TuMV

Turnip mosaic virus

V

vacuole

CPDC

cell plate during cytokinesis

MVB

multivesicular body

PD

plasmodesma

PM

plasma membrane

Notes

Authors’ Contributions

CZ, SL, LG, YL, XS, and XH conceived the study. CZ, SL, and LG completed the experiments. YL and XS contributed to data analysis and manuscript preparation. CZ and XH participated in the planning of experiments and revising the manuscript. All authors had read and approved the final version of the manuscript.

Funding Information

This work was supported by the grants from the National Natural Science Foundation of China (31272172), the Fundamental Research Funds for the Central Universities (KYTZ201401), and the Nature Science Foundation of Jiangsu Province (BK20141364).

Compliance with Ethical Standards

Competing Interests

The authors declare that they have no competing interests.

Supplementary material

11105_2017_1060_MOESM1_ESM.pdf (313 kb)
Figure S1 Cluster analysis of expression profile of SNARE family genes in Chinese cabbage. Gene expression levels represent log2-transformedFPKM values in six tissues (flower, leaf, seed, bud, silique and root). (PDF 312 kb)
11105_2017_1060_MOESM2_ESM.pdf (6.4 mb)
Figure S2 Distribution of vascular bundle in petiole. Transverse sections of petiole are shown. Left: 40× magnification. Right: 100× magnifications (bars at top right). p: phloem, x: xylem. (PDF 6593 kb)
11105_2017_1060_MOESM3_ESM.xls (132 kb)
ESM 1 (XLS 131 kb)

References

  1. Ahlquist P, Noueiry AO, Lee W-M, Kushner DB, Dye BT (2003) Host factors in positive-strand RNA virus genome replication. J Virol 77(15):8181–8186.  https://doi.org/10.1128/JVI.77.15.8181-8186.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15(11):5118–5129.  https://doi.org/10.1091/mbc.E04-02-0140 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(Web Server):W202–W208.  https://doi.org/10.1093/nar/gkp335 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bassham DC, Brandizzi F, Otegui MS, Aa. S (2008) The secretory system of Arabidopsis Arabidopsis Book 6:1–29Google Scholar
  5. Brunt AA (1992) The general properties of potyviruses archives of virology Supplementum 5:3–16Google Scholar
  6. Brunt AA, Crabtree K, Dallwitz MJ, Gibbs AJ, Watson L (1996) Viruses of plants. Descriptions and lists from the VIDE database Viruses of Plants Descriptions & Lists from the Vide DatabaseGoogle Scholar
  7. C P (2012) Hijack it, change it: how do plant viruses utilize the host secretory pathway for efficient viral replication and spread? Front Plant Sci 3:308Google Scholar
  8. Cheng F, Mandáková T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. The Plant Cell Online 25(5):1541–1554.  https://doi.org/10.1105/tpc.113.110486 CrossRefGoogle Scholar
  9. Denic V (2012) A portrait of the GET pathway as a surprisingly complicated young man. Trends Biochem Sci 37(10):411–417.  https://doi.org/10.1016/j.tibs.2012.07.004 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fasshauer D, Sutton RB, Brunger AT, Jahn R (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A 95(26):15781–15786.  https://doi.org/10.1073/pnas.95.26.15781 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer ELL, Eddy SR, Bateman A (2010) The Pfam protein families database. Nucleic Acids Res 38(suppl_1):D211–D222.  https://doi.org/10.1093/nar/gkp985 CrossRefPubMedGoogle Scholar
  12. Guo F, McCubbin AG (2012) The pollen-specific R-SNARE/longin PiVAMP726 mediates fusion of endo- and exocytic compartments in pollen tube tip growth. J Exp Bot 63(8):3083–3095.  https://doi.org/10.1093/jxb/ers023 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Heese M, Gansel X, Sticher L, Wick P, Grebe M, Granier F, Jurgens G (2001) Functional characterization of the KNOLLE-interacting t-SNARE AtSNAP33 and its role in plant cytokinesis. J Cell Biol 155(2):239–249.  https://doi.org/10.1083/jcb.200107126 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hong W (2005) SNAREs and traffic. Biochim Biophys Acta 1744(2):120–144.  https://doi.org/10.1016/j.bbamcr.2005.03.014 CrossRefPubMedGoogle Scholar
  15. Inada N, Ueda T (2014) Membrane trafficking pathways and their roles in plant-microbe interactions. Plant Cell Physiol 55(4):672–686.  https://doi.org/10.1093/pcp/pcu046 CrossRefPubMedGoogle Scholar
  16. Jahn R, Scheller RH (2006) SNAREs—engines for membrane fusion vol 7. vol 9Google Scholar
  17. Jenner CE, Sanchez F, Nettleship SB, Foster GD, Ponz F, Walsh JA (2000) The cylindrical inclusion gene of Turnip mosaic virus encodes a pathogenic determinant to the Brassica resistance gene TuRB01. Molecular Plant-Microbe Interactions: MPMI 13(10):1102–1108.  https://doi.org/10.1094/mpmi.2000.13.10.1102 CrossRefPubMedGoogle Scholar
  18. Kalde M, Nuhse TS, Findlay K, Peck SC (2007) The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1 Proceedings of the National Academy of Sciences of the United States of America 104:11850–11855 doi: https://doi.org/10.1073/pnas.0701083104
  19. Kato N, Fujikawa Y, Fuselier T, Adamou-Dodo R, Nishitani A, Sato MH (2010) Luminescence detection of SNARE–SNARE interaction in Arabidopsis protoplasts. Plant Mol Biol 72(4–5):433–444.  https://doi.org/10.1007/s11103-009-9581-z CrossRefPubMedGoogle Scholar
  20. Kiefer IW, Slusarenko AJ (2003) The pattern of systemic acquired resistance induction within the Arabidopsis rosette in relation to the pattern of translocation. Plant Physiol 132(2):840–847.  https://doi.org/10.1104/pp.103.021709 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645.  https://doi.org/10.1101/gr.092759.109 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Kwon C, Neu C, Pajonk S, Yun HS, Lipka U, Humphry M, Bau S, Straus M, Kwaaitaal M, Rampelt H, Kasmi FE, Jürgens G, Parker J, Panstruga R, Lipka V, Schulze-Lefert P (2008) Co-option of a default secretory pathway for plant immune responses. Nature 451:835–840.  https://doi.org/10.1038/nature06545 CrossRefPubMedGoogle Scholar
  23. Laliberté J-F, Sanfaçon H (2010) Cellular remodeling during plant virus infection. Annu Rev Phytopathol 48(1):69–91.  https://doi.org/10.1146/annurev-phyto-073009-114239 CrossRefPubMedGoogle Scholar
  24. Larson ER, Domozych DS, ML. T (2014) SNARE VTI13 plays a unique role in endosomal trafficking pathways associated with the vacuole and is essential for cell wall organization and root hair growth in Arabidopsis. Ann Bot 114(6):1147–1159.  https://doi.org/10.1093/aob/mcu041 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305CrossRefPubMedGoogle Scholar
  26. Li L, Stoeckert CJ, Jr., Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189.  https://doi.org/10.1101/gr.1224503 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lipka V, Kwon C, Panstruga R (2007) SNARE-ware: the role of SNARE-domain proteins in plant biology. Annual Rev Cell Dev Biol 23(1):147–174.  https://doi.org/10.1146/annurev.cellbio.23.090506.123529 CrossRefGoogle Scholar
  28. Lobingier BT (2014) SM proteins Sly1 and Vps33 co-assemble with Sec17 and SNARE complexes to oppose SNARE disassembly by Sec18. Elife 3:e02272–e02272CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lukowitz W (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84(1):61–71.  https://doi.org/10.1016/S0092-8674(00)80993-9 CrossRefPubMedGoogle Scholar
  30. M DC (2011) Protein trafficking to the cell wall occurs through mechanisms distinguishable from default sorting in tobacco. Plant J 65:295–308CrossRefGoogle Scholar
  31. M S, N R (2004) Traffic jams affect plant development and signal transduction. Nat Rev Mol Cell Biol 5:100–109CrossRefGoogle Scholar
  32. Moore ER (2011) The trans-Golgi SNARE syntaxin 6 is recruited to the chlamydial inclusion membrane. Microbiology 157(3):830–838.  https://doi.org/10.1099/mic.0.045856-0 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Nuhse TS, Boller T, Peck SC (2003) A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin. J Biol Chem 278(46):45248–45254.  https://doi.org/10.1074/jbc.M307443200 CrossRefPubMedGoogle Scholar
  34. Roberts K, Love AJ, Laval V, Laird J, Tomos AD, Hooks MA, Milner JJ (2007) Long-distance movement of Cauliflower mosaic virus and host defence responses in Arabidopsis follow a predictable pattern that is determined by the leaf orthostichy. The New Phytologist 175(4):707–717.  https://doi.org/10.1111/j.1469-8137.2007.02136.x CrossRefPubMedGoogle Scholar
  35. Rusholme RL, Higgins EE, Walsh JA, Lydiate DJ (2007) Genetic control of broad-spectrum resistance to turnip mosaic virus in Brassica rapa (Chinese cabbage). J Gen Virol 88(11):3177–3186.  https://doi.org/10.1099/vir.0.83194-0 CrossRefPubMedGoogle Scholar
  36. Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144(1):6–17.  https://doi.org/10.1104/pp.106.092973 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sanderfoot AA (1999) The t-SNARE AtVAM3p resides on the prevacuolar compartment in Arabidopsis root cells. Plant Physiol 121(3):929–938.  https://doi.org/10.1104/pp.121.3.929 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sanfa04on H (2005) Replication of positive-strand RNA viruses in plants: contact points between plant and virus components. Can J Bot 83(1521):1529–1549Google Scholar
  39. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108.  https://doi.org/10.1038/nprot.2008.73 CrossRefPubMedGoogle Scholar
  40. Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11(11):535–542.  https://doi.org/10.1016/j.tplants.2006.09.002 CrossRefPubMedGoogle Scholar
  41. Shattuck V (1992) The biology, epidemiology, and control of turnip mosaic virus. Hortic Rev 14:199–238Google Scholar
  42. Shirin F, Yasuhiro T, Mutsumi I, Alireza G, Reza P, Kazusato O (2009) Molecular characterisation of Turnip mosaic virus isolates from Brassicaceae weeds. Eur J Plant Pathol 124:45–55CrossRefGoogle Scholar
  43. Silva P, Ul-Rehman R, Rato C, Sansebastiano GPD, Rui M (2010) Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth. Bmc Plant Biol 10:179CrossRefPubMedPubMedCentralGoogle Scholar
  44. Suh SK, Green SK, Park HG (1995) Genetics of resistance to five strains of turnip mosaic virus in Chinese cabbage. Euphytica 81(1):71–77.  https://doi.org/10.1007/BF00022460 CrossRefGoogle Scholar
  45. T U, T U, RL O, A N, K T, MH S (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29:49–65CrossRefGoogle Scholar
  46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739.  https://doi.org/10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Tomlinson J (1987) Epidemiology and control of virus diseases of vegetables. Ann Appl Biol 110(3):661–681.  https://doi.org/10.1111/j.1744-7348.1987.tb04187.x CrossRefGoogle Scholar
  48. Tong C, Wang X, Yu J, Wu J, Li W, Huang J, Dong C, Hua W, Liu S (2013) Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genomics 14(1):689.  https://doi.org/10.1186/1471-2164-14-689 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Uemura T, Ueda T, Nakano A (2012) The physiological role of SYP4 in the salinity and osmotic stress tolerances. Plant Signal Behav 7(9):1118–1120.  https://doi.org/10.4161/psb.21307 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. Cell Struct Funct 29(2):49–65CrossRefPubMedGoogle Scholar
  51. Walsh JA, Jenner CE (2002) Turnip mosaic virus and the quest for durable resistance. Mol Plant Pathol 3(5):289–300.  https://doi.org/10.1046/j.1364-3703.2002.00132.x CrossRefPubMedGoogle Scholar
  52. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun JH, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park BS, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IA, Batley J, Kim JS, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon SJ, Choi SR, Lee TH, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z (2011) Brassica rapa Genome Sequencing Project Consortium. The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039.  https://doi.org/10.1038/ng.919
  53. Wang Y, Tang H, DeBarry JD, Tan X, Li J, Wang X, Lee Th, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40(7):e49.  https://doi.org/10.1093/nar/gkr1293 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Wei T, Wang A (2008) Biogenesis of cytoplasmic membranous vesicles for plant potyvirus replication occurs at endoplasmic reticulum exit sites in a COPI- and COPII-dependent manner. J Virol 82(24):12252–12264.  https://doi.org/10.1128/jvi.01329-08 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Wei T, Zhang C, Hou X, Sanfa04on H, Wang A (2013) The SNARE protein Syp71 is essential for turnip mosaic virus infection by mediating fusion of virus-induced vesicles with chloroplasts. PLoS Pathogens 9:210–216Google Scholar
  56. Wick P, Gansel X, Oulevey C, Page V, Studer I, Dürst M, Sticher L (2003) The expression of the t-SNARE AtSNAP33 is induced by pathogens and mechanical stimulation. Plant Physiol 132(1):343–351.  https://doi.org/10.1104/pp.102.012633 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, Appel RD, Hochstrasser DF (1999) Protein identification and analysis tools in the ExPASy server Methods in molecular biology (Clifton, NJ) 112:531–552Google Scholar
  58. Zhao MA, An SJ, Lee SC, Kim DS, Kang BC (2013) Overexpression of a single-chain variable fragment (scFv) antibody confers unstable resistance to TuMV in Chinese cabbage. Plant Mol Biol Report 31(6):1203–1211.  https://doi.org/10.1007/s11105-013-0577-0 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Changwei Zhang
    • 1
  • Shanwu Lyu
    • 1
  • Liwei Gao
    • 1
  • Xiaoming Song
    • 2
  • Yanxiao Li
    • 1
  • Xilin Hou
    • 1
    • 3
  1. 1.State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of HorticultureNanjing Agricultural UniversityNanjingPeople’s Republic of China
  2. 2.Department of Life SciencesNorth China University of Science and TechnologyTangshanChina
  3. 3.Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of AgricultureNanjing Agricultural UniversityNanjingPeople’s Republic of China

Personalised recommendations