454 pyrosequencing of olive (Olea europaea L.) transcriptome in response to salinity

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Bazakos, Christos ^a,b,d   Manioudaki, Maria E ^a   Sarropoulou, Elena ^c   Spano, Thodhoraq ^a   Kalaitzis, Panagiotis ^a  

^a MEDITERRANEAN AGRONOMIC INSTITUTE OF CHANIA   (Greece)

^b ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^c INSTITUTE OF OCEANOGRAPHY   (Greece)

^d INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM CHLORIDE; TRANSCRIPTOME; MESSENGER RNA; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; CULTIVAR; DOWN REGULATION; GENE CLUSTER; GENE EXPRESSION REGULATION; NEXT GENERATION SEQUENCING; NONHUMAN; OLIVE TREE; PLANT GENETICS; PLANT GROWTH; PLANT LEAF; PLANT METABOLISM; PLANT ROOT; PYROSEQUENCING; REAL TIME POLYMERASE CHAIN REACTION; SALT STRESS; SALT TOLERANCE; TRANSCRIPTOMICS; UPREGULATION; CLUSTER ANALYSIS; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE LIBRARY; GENE ONTOLOGY; GENETICS; HIGH THROUGHPUT SEQUENCING; ION TRANSPORT; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PROCEDURES; SALINITY;

BASE SEQUENCE; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENE ONTOLOGY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; ION TRANSPORT; MOLECULAR SEQUENCE ANNOTATION; OLEA; PLANT LEAVES; PLANT ROOTS; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SALINITY; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84956690252     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0143000     Document Type: Article

References (70)

1. Tattini M, Bertoni P, Caselli S. Genotypic responses of olive plants to sodium chloride. J Plant Nutr. 1992; 15:1467-1485.
2. Klein I, Ben-Tal Y, Lavee S, De Malach Y, David I. Saline irrigation of cv. Manzanillo and Uovo di Piccione trees. Acta Hort (ISHS). 1994; 356:176-180.
3. Cresti M, Ciampolini F, Tattini M, Cimato A. Effect of salinity on productivity and oil quality of olive (Olea europaea L.) plants. Advances in Horticultural Science. 1994; 8:211-214.
4. Loreto F, Centritto M, Chartzoulakis K. Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant Cell Environ. 2003; 26:595-601.
5. Tabatabaei SJ. Effects of salinity and N on the growth, photosynthesis and N status of olive (Olea europaea L.) trees. Sci Hortic-Amsterdam. 2006; 108:432-438.
6. Therios IN. Olives. CABI, U.K; 2009.
7. Rugini E, Fedeli E. Olive (Olea europaea L) as an oilseed crop. Springer, Berlin; 1990.
8. Therios IN, Misopolinos ND. Genotypic Response to Sodium-Chloride Salinity of 4 Major Olive Cultivars (Olea-Europea L). Plant Soil. 1988; 106: 105-111.
9. Chartzoulakis KS. Salinity and olive: Growth, salt tolerance, photosynthesis and yield. Agr Water Manage. 2005; 78:108-121.
10. Bazakos C, Manioudaki ME, Therios I, Voyiatzis D, Kafetzopoulos D, Awada T, et al. Comparative transcriptome analysis of two olive cultivars in response to NaCl-stress. PloS one. 2012; 7:e42931. doi: 10. 1371/journal.pone.0042931 PMID: 22952621
11. Salem M, Rexroad CE, Wang JN, Thorgaard GH, Yao JB. Characterization of the rainbow trout transcriptome using Sanger and 454-pyrosequencing approaches. Bmc Genomics. 2010; 11.
12. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y. RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 2008; 18:1509-1517. doi: 10. 1101/gr.079558.108 PMID: 18550803
13. Wang YC, Gao CQ, Liang YN, Wang C, Yang CP, Liu GF. A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress in tobacco plants. J Plant Physiol. 2010; 167:222-230. doi: 10.1016/j.jplph.2009.09.008 PMID: 19853962
14. Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008; 5:621-628. doi: 10.1038/nmeth.1226 PMID: 18516045
15. Cloonan N, Forrest ARR, Kolle G, Gardiner BBA, Faulkner GJ, Brown MK, et al. Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods. 2008; 5:613-619. doi: 10.1038/nmeth.1223 PMID: 18516046
16. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 2005; 437:376-380. PMID: 16056220
17. Weber APM, Weber KL, Carr K, Wilkerson C, Ohlrogge JB. Sampling the arabidopsis transcriptome with massively parallel pyrosequencing, Plant Physiol. 2007; 144:32-42. PMID: 17351049
18. Sugarbaker DJ, Richards WG, Gordon GJ, Dong L, De Rienzo A, Maulik G, et al. Transcriptome sequencing of malignant pleural mesothelioma tumors. P Natl Acad Sci USA. 2008; 105:3521-3526.
19. Torres TT, Metta M, Ottenwalder B, Schlotterer C. Gene expression profiling by massively parallel sequencing. Genome Res. 2008; 18:172-177. PMID: 18032722
20. Ohtsu K, Smith MB, Emrich SJ, Borsuk LA, Zhou RL, Chen TL, et al. Global gene expression analysis of the shoot apical meristem of maize (Zea mays L.). Plant J. 2007; 52:391-404. PMID: 17764504
21. Barakat A, Di Loreto DS, Zhang Y, Smith C, Baier K, Powell WA, et al. Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection. Bmc Plant Biol. 2009; 9.
22. Al Rwahnih M, Daubert S, Urbez-Torres JR, Cordero F, Rowhani A. Deep sequencing evidence from single grapevine plants reveals a virome dominated by mycoviruses. Arch Virol. 2011; 156:397-403. doi: 10.1007/s00705-010-0869-8 PMID: 21140178
23. Novaes E, Drost DR, Farmerie WG, Pappas GJ, Grattapaglia D, Sederoff RR, et al. High-throughput gene and SNP discovery in Eucalyptus grandis, an uncharacterized genome. Bmc Genomics. 2008; 9.
24. Riggins CW, Peng YH, Stewart CN, Tranel PJ. Characterization of de novo transcriptome for waterhemp (Amaranthus tuberculatus) using GS-FLX 454 pyrosequencing and its application for studies of herbicide target-site genes. Pest Manag Sci. 2010; 66:1042-1052. doi: 10.1002/ps.2006 PMID: 20680963
25. Alagna F, D'Agostino N, Torchia L, Servili M, Rao R, Pietrella M, et al. Comparative 454 pyrosequencing of transcripts from two olive genotypes during fruit development. Bmc Genomics. 2009; 10.
26. Muñoz-Mérida A, González-Plaza JJ, Cañada A, Blanco AM, García-López MC, Rodríguez JM, et al. De Novo Assembly and Functional Annotation of the Olive (Olea europaea) Transcriptome. DNA Res. 2013; 20:93-108. doi: 10.1093/dnares/dss036 PMID: 23297299
27. Leyva-Perez MD, Valverde-Corredor A, Valderrama R, Jimenez-Ruiz J, Munoz-Merida A, Trelles O, et al. Early and delayed long-term transcriptional changes and short-term transient responses during cold acclimation in olive leaves. DNA Res. 2015; 22:1-11. doi: 10.1093/dnares/dsu033 PMID: 25324298
28. Bachem CWB, Oomen RJFJ, Visser RGF. Transcript imaging with cDNA-AFLP: A step-by-step protocol. Plant Mol Biol Rep. 1998; 16:157-173.
29. Sarropoulou E, Sepulcre P, Poisa-Beiro L. Profiling of infection specific mRNA transcripts of the European seabass Dicentrarchus labrax. Bmc Genomics. 2009; 10:157. doi: 10.1186/1471-2164-10-157 PMID: 19361338
30. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal. 2011;10-12.
31. Huang Y, Niu BF, Gao Y, Fu LM, Li WZ. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics. 2010; 26:680-682. doi: 10.1093/bioinformatics/btq003 PMID: 20053844
32. Stekel DJ, Git Y, Falciani F. The comparison of gene expression from multiple cDNA libraries. Genome Res. 2000; 10:2055-2061. PMID: 11116099
33. Thiel T, Michalek W, Varshney RK, Graner A. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet. 2003; 106:411-422. PMID: 12589540
34. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21:3674-3676. PMID: 16081474
35. Nonis A, Vezzaro A, Ruperti B. Evaluation of RNA Extraction Methods and Identification of Putative Reference Genes for Real-Time Quantitative Polymerase Chain Reaction Expression Studies on Olive (Olea europaea L.) Fruits. J. Agric. Food Chem. 2012; 60:6855-6865. doi: 10.1021/jf300419w PMID: 22703380
36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 2001; 25:402-408 PMID: 11846609
37. Munns R. Genes and salt tolerance: bringing them together. New Phytol. 2005; 167:645-663. PMID: 16101905
38. Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF. Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 2002; 130:2129-2141. PMID: 12481097
39. Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, Shi WM, et al. Osmotic stress in barley regulates expression of a different set of genes than salt stress does. J Exp Bot. 2004; 55:2213-2218. PMID: 15361537
40. Ozturk ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, et al. Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol Biol. 2002; 48:551-573. PMID: 11999834
41. Atienza SG, Faccioli P, Perrotta G, Dalfino G, Zschiesche W, Humbeck K, et al. Large scale analysis of transcripts abundance in barley subjected to several single and combined abiotic stress conditions. Plant Sci. 2004; 167:1359-1365.
42. Gu RS, Fonseca S, Puskas LG, Hackler L, Zvara A, Dudits D, et al. Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiol. 2004; 24:265-276. PMID: 14704136
43. Zhu JK. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol. 2003; 6:441-445. PMID: 12972044
44. Gautier L, Cope L, Bolstad BM, Irizarry RA. Affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004; 20:307-315. PMID: 14960456
45. Chartzoulakis K, Loupassaki M, Bertaki M, Androulakis I. Effects of NaCl salinity on growth, ion content and CO2 assimilation rate of six olive cultivars. Sci Hortic. 2002; 96:235-247.
46. Sarropoulou E, Galindo-Villegas J, Kasapidis P, Mulero V. Detection of differential expression by RNA seq in the European seabass tissues after oral vaccine against V. anguillarum. Mar Biotechnol. 2012; 14:634-642. doi: 10.1007/s10126-012-9466-z PMID: 22790793
47. Peng YH, Abercrombie LLG, Yuan JS, Riggins CW, Sammons RD, Tranel PJ, et al. Characterization of the horseweed (Conyza canadensis) transcriptome using GS-FLX 454 pyrosequencing and its application for expression analysis of candidate non-target herbicide resistance genes. Pest Manag Sci. 2010; 66:1053-1062. doi: 10.1002/ps.2004 PMID: 20715018
48. Bremer B, Bremer K, Chase MW, Reveal JL, Soltis DE, Soltis PS, et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc. 2003; 141:399-436.
49. Dang ZH, Zheng LL, Wang J, Gao Z, Wu SB, Qi Z, et al. Transcriptomic profiling of the salt-stress response in the wild recretohalophyte Reaumuria trigyna. Bmc Genomics. 2013; 14.
50. Huang JZ, Lu X, Yan H, Chen SY, Zhang WK, Huang RF, et al. Transcriptome Characterization and Sequencing-Based Identification of Salt-Responsive Genes in Millettia pinnata, a Semi-Mangrove Plant. DNA Res. 2012; 19:195-207. doi: 10.1093/dnares/dss004 PMID: 22351699
51. Reimann C. Sodium exclusion by Chenopodium species. J Exp Bot. 1992; 249:503-510.
52. Clauw P, Coppens F, De Beuf K, Dhondt S, Van Daele T, Maleux K, et al. Leaf responses to mild drought stress in natural variants of Arabidopsis thaliana. Plant Physiol. 2015; doi: 10.1104/pp.114. 254284
53. Binzel M, Ratajczak R. Function of membrane transport systems under salinity: tonoplast. In: Lauchli A, Liuttge U, eds. Salinity: Environment - Plants - Molecules. Dordrecht, the Netherlands, Kluwer; 2002.
54. Dietz KJ, Tavakoli N, Kluge C. Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot. 2001; 52:1969-1980. PMID: 11559732
55. Blumwald E. Sodium transport and salt tolerance in plants. Curr Opin Cell Biol. 2000; 12:431-434. PMID: 10873827
56. Munns R. Why Measure Osmotic Adjustment. Aust J Plant Physiol. 1988; 15:717-726.
57. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K. ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res. 2011; 124:509-525. doi: 10.1007/s10265-011-0412-3 PMID: 21416314
58. Balazadeh S, Siddiqui H, Allu AD, Matallana-Ramirez LP, Caldana C, Mehrni M, et al. A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence. Plant J. 2010; 62:250-264. doi: 10.1111/j.1365-313X.2010.04151.x PMID: 20113437
59. Pandey SP, Somssich IE. The Role of WRKY Transcription Factors in Plant Immunity. Plant Physiol. 2009; 150:1648-1655. doi: 10.1104/pp.109.138990 PMID: 19420325
60. Sottosanto B, Gelli A, Blumwald E. DNA array analyses of Arabidopsis thaliana lacking a vacuolar Na +/H+ antiporter: impact of AtNHX1 on gene expression. Plant J. 2004; 40:752-771. PMID: 15546358
61. Zhu JK. Salt and drought stress signal transduction in plants. Ann Rev Plant Physiol Plant Mol Biol. 2002; 53:247-273.
62. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, et al. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 2003; 34:137-148. PMID: 12694590
63. Fahad S, Nie L, Chen Y, Wu C, Xiong D, Saud S, Hongyan L, et al. Crop plant hormones and environmental stress. Sustain Agric Rev. 2015; 15:371-400.
64. Sharma N, Abrams SR, Waterer DR. Uptake, movement, activity, and persistence of an abscisic acid analog (80 acetylene ABA methyl ester) in marigold and tomato. J Plant Growth Regul. 2005; 24:28-35.
65. Jia W, Wang Y, Zhang S, Zhang J. Salt-stress-induced ABA accumulation is more sensitively triggered in roots than in shoots. J Exp Bot. 2002; 53:2201-2206. PMID: 12379787
66. Qing DJ, Lu HF, Li N, Dong HT, Dong DF, Li YZ. Comparative Profiles of Gene Expression in Leaves and Roots of Maize Seedlings under Conditions of Salt Stress and the Removal of Salt Stress. Plant Cell Physiol. 2009; 50:889-903. doi: 10.1093/pcp/pcp038 PMID: 19264788
67. Mantri NL, Ford R, Coram TE, Pang ECK. Transcriptional profiling of chickpea genes differentially regulated in response to high-salinity, cold and drought. BMC Genomics. 2007; 8.
68. Singh S, Hazra S. Somatic embryogenesis from the axillary meristems of peanut (Arachis hypogaea L.). Plant Biotechnol Rep. 2009; 3:333-340.
69. Ehlting J, Provart NJ, Werck-Reichhart D. Functional annotation of the Arabidopsis P450 superfamily based on large-scale co-expression analysis. Biochem Soc T. 2006; 34:1192-1198.
70. Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P, Bennett M, et al. Cell Wall Damage-Induced Lignin Biosynthesis Is Regulated by a Reactive Oxygen Species-and Jasmonic Acid-Dependent Process in Arabidopsis. Plant Physiol. 2011; 156:1364-1374. doi: 10.1104/pp.111.175737 PMID: 21546454