Variations in DREB1A and VP1.1 genes show association with salt tolerance traits in wild tomato (Solanum pimpinellifolium)

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Rao, Eguru Sreenivasa ^a,e   Kadirvel, Palchamy ^b,e   Symonds, Rachael C ^c,e   Geethanjali, Subramaniam ^d,e   Thontadarya, Ramadihalli N ^a   Ebert, Andreas W ^e  

^a INDIAN INSTITUTE OF HORTICULTURAL RESEARCH   (India)

^b DIRECTORATE OF OILSEEDS RESEARCH   (India)

^c UNIVERSITY OF NOTTINGHAM MALAYSIA CAMPUS   (Malaysia)

^d TAMIL NADU AGRICULTURAL UNIVERSITY   (India)

^e AVRDC THE WORLD VEGETABLE CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; CONTROLLED STUDY; CULTIVATED SPECIES; DREB1A GENE; GENE DELETION; GENETIC ANALYSIS; GENOTYPE; HAPLOTYPE; INTROGRESSION; NHX1 GENE; NONHUMAN; PHENOTYPIC VARIATION; PLANT GENE; SALT STRESS; SALT TOLERANCE; SOLANUM; SOLANUM PIMPINELLIFOLIUM; TIP GENE; VARIETAS; VP1.1 GENE; WILD PLANT; AMINO ACID SEQUENCE; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION STUDY; GENETIC MARKER; GENETIC VARIATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE HOMOLOGY;

GENETIC MARKER; PLANT PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRANSCRIPTION FACTOR;

ALLELES; AMINO ACID SEQUENCE; BASE SEQUENCE; GENES, PLANT; GENETIC ASSOCIATION STUDIES; GENETIC MARKERS; GENETIC VARIATION; LINKAGE DISEQUILIBRIUM; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; SALT-TOLERANCE; SEQUENCE HOMOLOGY, AMINO ACID; SOLANUM; TRANSCRIPTION FACTORS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84941332482     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0132535     Document Type: Article

References (87)

1. Erskine W, Upadhyaya HD, Malik AI. Salinity. In: Jackson M., Ford-Lloyd B., Parry M., editors. Plant Genetic Resources and Climate Change. CAB International, Oxfordshire, UK; 2014. pp. 236-250.
2. Foolad MR. Recent advances in genetics of salt tolerance in tomato. Plant Cell Tissue Organ Cult. 2004; 76:101-119.
3. Scholberg JMS, Locascio SJ. Growth response of snap bean and tomato as affected by salinity and irrigation method. HortScience. 1999; 34(2):259-264.
4. Munns R, Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 2008; 59: 651-681. doi: 10.1146/annurev.arplant.59.032607.092911 PMID: 18444910
5. Parida AK, Das AB. Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf. 2005; 60:324-349. PMID: 15590011
6. Roy SJ, Negrəo S, Tester M. Salt resistant crop plants. Current opinions in Biotechnology. 2014; 26:115-124.
7. Pardo JM. Biotechnology of water and salinity stress tolerance. Curr Opin Biotechnol. 2010; 21:185-196. doi: 10.1016/j.copbio.2010.02.005 PMID: 20189794
8. Apse MP, Aharon GS, Snedden WA, Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 1999; 285:1256-1258. PMID: 10455050
9. Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Kishitani S, Takabe T, et al. Salt tolerance of transgenic rice overexpressing yeast mitochondrial Mn-SOD in chloroplasts. Plant Sci. 1999; 148:131-138.
10. Baker SS, Wilhelm KS, Thomashow MF. The 50-region of Arabidopsis thaliana cor15a has cis-Acting elements that confer cold-, drought-And ABA-regulated gene expression. Plant Mol Biol. 1994; 24:701-713. PMID: 8193295
11. Huang XS, Luo T, Fu XZ, Fan QJ, Liu JH. Cloning and molecular characterization of a mitogen-Activated protein kinase gene from Poncirus trifoliata whose ectopic expression confers dehydration/drought tolerance in transgenic tobacco. J Exp Bot. 2011; 62:5191-5206. doi: 10.1093/jxb/err229 PMID: 21778184
12. Reuscher S, Akiyama M, Mori C, Aoki K, Shibata D, Shiratake K. Genome-wide identification and expression analysis of aquaporins in tomato. PloS ONE. 2013; 8:e79052. doi: 10.1371/journal.pone. 0079052 PMID: 24260152
13. Peleg Z, Apse MP, Blumwald E. Engineering salinity and water stress tolerance in crop plants: Getting closer to the field. Adv Bot Res. 2011; 57:405-443.
14. Bonilla P, Dvorak J, Mackill D, Deal K, Gregorio G. RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philip Agric Sci. 2002; 65:68-76.
15. Hamwieh A, Tuyen DD, Cong H, Benitez ER, Takahashi R, Xu DH. Identification and validation of a major QTL for salt tolerance in soybean. Euphytica 2011; 179:451-459.
16. Qi X, Li MW, Xie M, Liu X, Ni M, Shao G, et al. Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nature Communications 2014; 5:4340. doi: 10.1038/ncomms5340 PMID: 25004933
17. Linh LH, Linh TH, Xuan TD, Ham LH, Ismail AM, Khanh TD. Molecular breeding to improve salt tolerance of rice (Oryza sativa L.) in the Red River delta of Vietnam. Intl J Plant Genomics 2012; doi: 10. 1155/2012/949038
18. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES. Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet. 2001; 28:286-289. PMID: 11431702
19. Olsen KM, Purugganan MD. Molecular evidence on the origin and evolution of glutinous rice. Genetics 2002; 162:941-950. PMID: 12399401
20. Ranc N, Muños S, Xu J, Le Paslier MC, Chauveau A, Bounon R, et al. Genome-wide association mapping in tomato (Solanum lycopersicum) is possible using genome admixture of Solanum lycopersicum var. cerasiforme. G3: Genes, Genomes, Genetics. 2012; 2(8):853-64.
21. Sauvage C, Segura V, Bauchet G, Stevens R, Do PT, Nikoloski Z, et al. Genome-wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. 2014; 165:1120-1132. PMID: 24894148
22. Bauchet G, Muños S, Sauvage C, Bonnet J, Grivet L, Causse M. Genes involved in floral meristem in tomato exhibit drastically reduced genetic diversity and signature of selection. BMC Plant Biol. 2014; 14:279; doi: 10.1186/s12870-014-0279-2 PMID: 25325924
23. Kumar V, Singh A, Amitha Mithra SV, Krishnamurthy SL, Parida SK, Jain S, et al. Genome-wide association mapping of salinity tolerance in rice (Oryza sativa). DNA Res. 2015; 22(2):133-145; doi: 10.1093/dnares/dsu046 PMID: 25627243
24. Li Y, Böck A, Haseneyer G, Korzun V, Wilde P, Schön C-C, et al. Association analysis of frost tolerance in rye using candidate genes and phenotypic data from controlled, semi-controlled, and field phenotyping platforms. BMC Plant Biol. 2011; 11:146. doi: 10.1186/1471-2229-11-146 PMID: 22032693
25. Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet. 2006; 38:203-208. PMID: 16380716
26. Storey JD, Tibshirani R. Statistical significance for genome wide studies. Proc Natl Acad Sci USA. 2003; 100(16):9440-9445. PMID: 12883005
27. Tal M, Shannon MC. Salt tolerance in the wild relatives of the cultivated tomato: responses of Lycopersicon esculentum, L. cheesmaniae, L. peruvianum, Solanum pennellii and F1 hybrids to high salinity. Aust J Plant Physiol. 1983; 10:109-117.
28. Bolarín MC, Fernández FG, Cruz V, Cuartero J. Salinity tolerance in four wild tomato species using vegetative yield-salinity response curves. J Am Soc Hort Sci. 1991; 116:286-290.
29. Cuartero J, Yeo AR, Flowers TJ. Selection of donors for salt-tolerance in tomato using physiological traits. New Phytol. 1992; 121:63-69.
30. Blanca J, Cañizares J, Cordero L, Pascual L, Diez MJ, Fernando N. Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato. PLoS ONE. 2012; 7:e48198; doi: 10.1371/journal.pone.0048198 PMID: 23118951
31. Zuriaga E, Blanca JM, Cordero L, Sifres A, Blas-Cerdán WG, Morales R, et al. Genetic and bioclimatic variation in Solanum pimpinellifolium. Genet Resour Crop Evol. 2009; 56:39-51.
32. Zhang HX, Blumwald E. Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol. 2001; 19:765-768. PMID: 11479571
33. Sarafian V, Kim Y, Poole RJ, Rea PA. Molecular cloning and sequence of cDNA encoding the pyrophosphate-energized vacuolar membrane proton pump of Arabidopsis thaliana. Proc Natl. Acad Sci USA. 1992; 89(5):1775-1779. PMID: 1311852
34. Akhtar M, Jaiswal A, Taj G, Jaiswal JP, Qureshi MI, Singh NK. DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J Genet. 2012; 91:385-395. PMID: 23271026
35. Bassil E, Coku A, Blumwald E. Cellular ion homeostasis: emerging roles of intracellular NHX Na+/H+ antiporters in plant growth and development. J Exp Bot. 2012; 63:5727-5740. doi: 10.1093/jxb/ers250 PMID: 22991159
36. Barragan V, Leidi EO, Andreas Z, Rubio L, De Luca A, Fernandez JA, et al. Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. The Plant Cell. 2012; 24:1127-1142. doi: 10.1105/tpc.111.095273 PMID: 22438021
37. Apse MP, Aharon GS, Snedden WA, Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science. 1999; 285:1256-1258. PMID: 10455050
38. Gálvez FJ, Baghour M, Hao G, Cagnac O, Rodríguez-Rosales MP, Venema K. Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species. Plant Physiol Biochem. 2012; 51:109-115. doi: 10.1016/j.plaphy.2011.10.012 PMID: 22153246
39. Leidi EO, Barragán V, Rubio L, El-Hamdaoui A, Ruiz MT, Cubero B, et al. The AtNHX1 exchanger mediates potassium compartmentation in vacuoles of transgenic tomato. Plant J. 2010; 61(3):495-506. doi: 10.1111/j.1365-313X.2009.04073.x PMID: 19912566
40. Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, et al. Drought-And salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA. 2001; 98:11444-11449. PMID: 11572991
41. Bhaskaran S, Savithramma DL. Co-expression of Pennisetum glaucum vacuolar Na+/H+ antiporter and Arabidopsis H+-pyrophosphatase enhances salt tolerance in transgenic tomato. J Exp Bot. 2011; 62:5561-5570. doi: 10.1093/jxb/err237 PMID: 21841179
42. Sade N, Vinocur BJ, Diber A, Shantil A, Ronen G, Nissan H, et al. Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol. 2009; 181:651-661. doi: 10.1111/j.1469-8137.2008.02689.x PMID: 19054338
43. Xin S, Yu G, Sun L, Qiang X, Xu N, Cheng X. Expression of tomato SlTIP2;2 enhances the tolerance to salt stress in transgenic Arabidopsis and interacts with target proteins. J Plant Research 2014; 127:659-708.
44. Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 1999; 17:287-291. PMID: 10096298
45. Cong L, Zheng HC, Zhang YX, Chai TY. Arabidopsis DREB1A confers high salinity tolerance and regulates the expression of GA dioxygenases in tobacco. Plant Sci. 2008; 174:156-164.
46. Celebi-Toprak F, Behnam B, Serrano G, Kasuga M, Yamaguchi-Shinozaki K, Hiroshi Naka H, et al. Tolerance to salt stress of the transgenic tetrasomic tetraploid potato, Solanum tuberosum cv. Desiree appears to be induced by the DREB1A gene and RD29A promoter of Arabidopsis thaliana. Breeding Sci. 2005; 55:311-319.
47. Rao ES, Kadirvel P, Symonds RC, Geethanjali S, Ebert AW. Using SSR markers to map genetic diversity and population structure of Solanum pimpinellifolium for development of a core collection. Plant Genet Resour. 2012; 10:38-48.
48. Rao ES, Kadirvel P, Symonds RC, Ebert AW. Relationship between survival and yield related traits in Solanum pimpinellifolium under salt stress. Euphytica. 2013; 190:215-228.
49. Munns R, James RA. Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant Soil. 2003; 253:201-218.
50. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005; 14:2611-2620. PMID: 15969739
51. Barendse W. Haplotype analysis improved evidence for candidate genes for intramuscular fat percentage from a genome wide association study of cattle. PLoS ONE. 2011; 6(12):e29601. doi: 10.1371/journal.pone.0029601 PMID: 22216329
52. Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, et al. Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J. 2005; 44:1054-1064. PMID: 16359397
53. Breseghello F, Sorrells ME. Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics. 2006; 172:1165-1177. PMID: 16079235
54. Reeves PA, Panella LW, Richards CM. Retention of agronomically important variation in germplasm core collections: implications for allele mining. Theor Appl Genet. 2012; 124:1155-1171. doi: 10.1007/s00122-011-1776-4 PMID: 22228243
55. Gowda M, Zhao Y, Würschum T, Longin CFH, Miedaner T, Ebmeyer E, et al. Relatedness severely impacts accuracy of marker-Assisted selection for disease resistance in hybrid wheat. Heredity. 2014; 112:552-561. doi: 10.1038/hdy.2013.139 PMID: 24346498
56. Yu J, Zhang Z, Zhu C, Tabanao TA, Pressoir G, Tuinstra MR, et al. Simulation appraisal of the adequacy of number of background markers for relationship estimation in association mapping. Plant Genome. 2009; 2:63-77.
57. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989; 123:585-595. PMID: 2513255
58. Yu J, Buckler ES. Genetic association mapping and genome organization of maize. Curr Opin Biotechnol. 2006; 17:155-160. PMID: 16504497
59. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007; 23:2633-2635. PMID: 17586829
60. Edae EA, Byrne PF, Manmathan H, Haley SD, Moragues M, Lopes MS, et al. Association mapping and nucleotide sequence variation in five drought tolerance candidate genes in spring wheat. Plant Genome. 2013; 6:1-13.
61. Yu JM, Zhang ZW, Zhu CS, Tabanao DA, Pressoir G, et al. Simulation appraisal of the adequacy of number of background markers for relationship estimation in association mapping. The Plant Genome. 2009; 2:63-77.
62. Long NV, Dolstra O, Malosetti M, Kilian B, Graner A, Visser RGF, et al. Association mapping of salt tolerance in barley (Hordeum vulgare L.). Theor Appl Genet. 2013; 126:2335-2351. doi: 10.1007/s00122-013-2139-0 PMID: 23771136
63. Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, McDonald GK. Additive effects of Na+ and Cl-ions on barley growth under salinity stress. J Exp Bot. 2011; 62(6):2189-2203. doi: 10.1093/jxb/erq422 PMID: 21273334
64. Jia L, Yan W, Zhu C, Agrama HA, Jackson A, Kathleen Y, et al. Allelic analysis of sheath blight resistance with association mapping in rice. PLoS ONE. 2012; 7:1-10.
65. Negrao S, Cecília AM, Pires IS, Isabel AA, Joao M, Brigitte C, et al. New allelic variants found in key rice salt-tolerance genes: an association study. Plant Biotechnol J. 2013; 11:87-100. doi: 10.1111/pbi. 12010 PMID: 23116435
66. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, et al. 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. 1998; 10:1391-1406. PMID: 9707537
67. Latini A, Rasi C, Sperandei M, Cantale C, Lannetta M, Dettori M, et al. Identification of a DREB-related gene in Triticum durum and its expression under stress conditions. Ann Appl Biol. 2007; 150:187-195.
68. Pandey B, Sharma P, Saini M, Pandey DM, Sharma I. Isolation and characterization of dehydrationresponsive element-binding factor 2 (DREB2) from Indian wheat (Triticum aestivum L.) cultivars. Aust J Crop Sci. 2014; 8:44-54.
69. Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, et al. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol. 2006; 47:141-153. PMID: 16284406
70. Matsukura S, Mizoi J, Yoshida T, Todaka D, Ito Y, Maruyama K, et al. Comprehensive analysis of rice DREB2-type genes that encode transcription factors involved in the expression of abiotic stressresponsive genes. Mol Genet Genomics. 2010; 283:185-196. doi: 10.1007/s00438-009-0506-y PMID: 20049613
71. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, et al. Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol. 2004; 45:1042-1052. PMID: 15356330
72. Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran L-SP, et al. Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J. 2007; 50:54-PMID: 17346263
73. Hsieh TH, Lee JT, Charng YY, Chan MT. Tomato plants ectopically expressing Arabidopsis CBF1 show enhanced resistance to water deficit stress. Plant Physiol. 2002; 130:618-626. PMID: 12376629
74. Andersen J, Lubberstedt T. Functional markers in plants. Trends Plant Sci. 2003; 18:554-560.
75. Bagge M, Lubberstedt T. Functional markers in wheat: Technical and economic aspects. Mol Breed. 2008; 22:319-328.
76. Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang ZW, Costich DE, et al. Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell. 2009; 21:2194-2202. doi: 10. 1105/tpc.109.068437 PMID: 19654263
77. AVRDC Vegetable Genetic Resources Information System (AVGRIS) (2014) http://203.64.245.173/search-result.asp?VINO=&ACCNO=&TEMPNO=&SPECIE=TM%3A +SOLANUMPIMPINELLIFOLIUM&PEDCUL=&SUBTAX=&COUNTR=&NOTES=. Accessed 5 May 2014
78. Slavich PG, Petterson GH. Estimating the electrical conductivity of saturated paste extracts from 1:5 soil, water suspensions and texture. Aust J Soil Res. 1993; 31: 73-81.
79. GENRES Data entry module for genres statistical software pascal intl software solution. Version 3.11 (1994).
80. Geethanjali S, Kadirvel P, de la Peña R, Rao ES, Wang JF. Development of tomato SSR markers from anchored BAC clones of chromosome 12 and their application for genetic diversity analysis and linkage mapping. Euphytica. 2011; 178:283-295.
81. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000; 155:945-959. PMID: 10835412
82. Gamerman D, Lopes HF. Markov chain Monte Carlo: stochastic simulation for Bayesian inference. Chapman & Hall/CRC Press, Boca Raton; 2006.
83. Ritland K. Estimators for pairwise relatedness and individual inbreeding coefficients. Genet. Res., Camb. 1996; 67:175-185.
84. Hardy OJ, Vekemans X. Spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes. 2002; 2:618-620.
85. Rozen S, Skaletsky HJ. Primer3 on theWWWfor general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, New Jersey; 2000; pp. 365-386.
86. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999; 41:95-98.
87. Agrama HA, Eizenga GC, Yan W. Association mapping of yield and its components in rice cultivars. Mol Breed. 2007; 19:341-356.