In-silico prediction of novel genes responsive to drought and salinity stress tolerance in bread wheat (Triticum aestivum)


Autoři: Laila Dabab Nahas aff001;  Naim Al-Husein aff002;  Ghinwa Lababidi aff001;  Aladdin Hamwieh aff003
Působiště autorů: Biotechnology Engineering Dept/Technological Engineering Faculty/University of Aleppo, Aleppo, Syria aff001;  General Commission for Scientific Agricultural Research (GCSAR)/Ministry of Agriculture, Aleppo, Syria aff002;  International Center for Agricultural Research in the Dry Areas (ICARDA), Cairo, Egypt aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223962

Souhrn

Common wheat (Triticum aestivum) is the most widely grown cereal crop and is cultivated extensively in dry regions. Water shortage, resulting from either drought or salinity, leads to slow growth and loss of wheat yield. In order to predict new genes responsive to the drought and salt stresses in wheat, 6,717 expressed sequence tags (ESTs), expressed in drought and salinity stress conditions were collected from the National Center for Biotechnology Information (NCBI). The downloaded ESTs were clustered and assembled into 354 contigs; 14 transcription factor families in 29 contigs were identified. In addition, 119 contigs were organized in five enzyme classes. Biological functions were obtained for only 324 of the 354 contigs using gene ontology. In addition, using Kyoto Encyclopedia of Genes and Genomes database, 191 metabolic pathways were identified. The remaining contigs were used for further analysis and the search for new genes responsive to drought and salt stresses. These contigs were mapped on the International Wheat Genome Sequencing Consortium RefSeq v1.0 assembly, the most complete version of the reference sequence of the bread wheat variety Chinese Spring. They were found to have from one to three locations on the subgenomes A, B, and D. Full-length gene sequences were designed for these contigs, which were further validated using promoter analysis. These predicted genes may have applications in molecular breeding programs and wheat drought and salinity research.

Klíčová slova:

Gene ontologies – Gene prediction – Plant resistance to abiotic stress – Salinity – Sequence databases – Sequence motif analysis – Wheat – Expressed sequence tags


Zdroje

1. Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, et al. Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature. 2012 Nov;491(7426):705. doi: 10.1038/nature11650 23192148

2. Moore G, Devos KM, Wang Z, Gale MD. Cereal genome evolution: grasses, line up and form a circle. 1995 Jul 1;5(7):737–9.

3. Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, et al. Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. The Plant Cell. 2010 Jun 1;22(6):1686–701. doi: 10.1105/tpc.110.074187 20581307

4. Appels R, Eversole K, Feuillet C, Keller B, Rogers J, Stein N, et al. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science. 2018 Aug 17;361(6403):eaar7191. doi: 10.1126/science.aar7191 30115783

5. Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, eat al The transcriptional landscape of polyploid wheat. Science. 2018 Aug 17;361(6403):eaar6089. doi: 10.1126/science.aar6089 30115782

6. Nevo E, Chen G Drought and salt tolerances in wild relatives for wheat and barley improvement. Plant, cell & environment. 2010 Apr;33(4):670–85. doi: 10.1111/j.1365-3040.2009.02107.x

7. Ahmed IM, Nadira UA, Bibi N, Zhang G, Wu F. Tolerance to combined stress of drought and salinity in barley. Combined Stresses in Plants. InCombined Stresses in Plants 2015 (pp. 93-121). Springer, Cham.

8. Sairam RK, Tyagi A. Physiology and molecular biology of salinity stress tolerance in plants. Current science. 2004 Feb 10:407–21.

9. Bartels D, Sunkar R. Drought and salt tolerance in plants. Critical reviews in plant sciences. 2005 Feb 23;24(1):23–58. doi: 10.1080/07352680590910410

10. Pastori GM, Foyer CH. Common components, networks, and pathways of cross-tolerance to stress. The central role of “redox” and abscisic acid-mediated controls. Plant physiology. 2002 Jun 1;129(2):460–8. doi: 10.1104/pp.011021 12068093

11. Tuteja A, Choi W, Ma M, Mabry JM, Mazzella SA, Rutledge GC, et al. Designing superoleophobic surfaces. Science. 2007 Dec 7;318(5856):1618–22. doi: 10.1126/science.1148326 18063796

12. Ashraf M, O’leary JW. Responses of some newly developed salt-tolerant genotypes of spring wheat to salt stress: 1. Yield components and ion distribution. Journal of Agronomy and Crop Science. 1996 Apr;176(2):91–101. doi: 10.1111/j.1439-037X.1996.tb00451.x

13. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J. A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science. 2006 Nov 24;314(5803):1298–301. doi: 10.1126/science.1133649 17124321

14. Nagaraj SH, Gasser RB, Ranganathan S. A hitchhiker’s guide to expressed sequence tag (EST) analysis. 2006 May 23;8(1):6–21.

15. Guo JW, Li Q, Chen WQ, Li X, Li LQ, Liu TG, et al. In silico cloning and chromosomal localization of EST sequences that are related to leaf senescence using nulli-tetrasomes in wheat. Cereal research communications. 2015 Sep;43(3):364–73. doi: 10.1556/0806.43.2015.014

16. Ding Q, Li J, Wang F, Zhang Y, Li H, Zhang J, Gao J. Characterization and development of EST-SSRs by deep transcriptome sequencing in Chinese cabbage (Brassica rapa L. ssp. pekinensis). International journal of genomics. 2015;2015. doi: 10.1155/2015/473028

17. Kent WJ. BLAT—the BLAST-like alignment tool. Genome research. 2002 Apr 1;12(4):656–64. doi: 10.1101/gr.229202 11932250

18. Rombauts S, Florquin K, Lescot M, Marchal K, Rouzé P, Van de Peer Y. Computational approaches to identify promoters and cis-regulatory elements in plant genomes. Plant physiology. 2003 Jul 1;132(3):1162–76. doi: 10.1104/pp.102.017715 12857799

19. Bhati J, Chaduvula PK, Rani R, Kumar S, Rai A. In-silico prediction and functional analysis of salt stress responsive genes in maize (Zea mays). European J Mol Biol Biochem. 2014;1:151–7.

20. Chaduvula PK, Bhati J, Rai A, Gaikwad K, Marla SS, Elangovan M, Kumar S. ‘In-silico’ expressed sequence tag analysis in identification and characterization of salinity stress responsible genes in Sorghum bicolor. Australian Journal of Crop Science. 2015 Sep;9(9):799.

21. Bhati J, Chaduvula KP, Rai A, Gaikwad K, Soma Marla S. In-silico prediction and functional analysis of salt stress responsive genes in rice (Oryza sativa). J Rice Res. 2016;4(164):2.

22. Masoudi-Nejad A, Tonomura K, Kawashima S, Moriya Y, Suzuki M, Itoh M, et al. EGassembler: online bioinformatics service for large-scale processing, clustering and assembling ESTs and genomic DNA fragments. Nucleic acids research. 2006 Jul 1;34(suppl 2):W459–62. doi: 10.1093/nar/gkl066 16845049

23. Huang X, Madan A. CAP3: a DNA sequence assembly program. 1999 Sep 1;9(9):868–77.

24. Conesa A, Götz S. Blast2GO: a comprehensive suite for functional analysis in plant genomics. International journal of plant genomics. 2008;2008. doi: 10.1155/2008/619832 18483572

25. Salamov AA, Solovyev VV. Ab initio gene finding in Drosophila genomic DNA. Genome research. 2000 Apr 1;10(4):516–22. doi: 10.1101/gr.10.4.516 10779491

26. Chow CN, Zheng HQ, Wu NY, Chien CH, Huang HD, Lee TY, et al. PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic acids research. 2015 Oct 17;44(D1):D1154–60. doi: 10.1093/nar/gkv1035 26476450

27. Hattori T, Totsuka M, Hobo T, Kagaya Y, Yamamoto-Toyoda A. Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant and Cell Physiology. 2002 Jan 15;43(1):136–40. doi: 10.1093/pcp/pcf014 11828032

28. Xue GP. Characterisation of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid, quantitative and high-throughput analysis of the DNA-binding activity. Nucleic Acids Research. 2002 Aug 1;30(15):e77-. doi: 10.1093/nar/gnf076 12140339

29. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. The Plant Cell. 2003 Jan 1;15(1):63–78. doi: 10.1105/tpc.006130 12509522

30. Abe H, Yamaguchi-Shinozaki K, Urao T, Iwasaki T, Hosokawa D, Shinozaki K. Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. The Plant Cell. 1997 Oct 1;9(10):1859–68. doi: 10.1105/tpc.9.10.1859 9368419

31. Pan YJ, Cho CC, Kao YY, Sun CH. A novel WRKY-like protein involved in transcriptional activation of cyst wall protein genes in Giardia lamblia. Journal of Biological Chemistry. 2009 Jul 3;284(27):17975–88. doi: 10.1074/jbc.M109.012047 19423705

32. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, et al. The population biology of invasive species. Annual review of ecology and systematics. 2001 Nov;32(1):305–32. doi: 10.1146/annurev.ecolsys.32.081501.114037

33. Yanagisawa S, Schmidt RJ. Diversity and similarity among recognition sequences of Dof transcription factors. The Plant Journal. 1999 Jan;17(2):209–14. doi: 10.1046/j.1365-313x.1999.00363.x 10074718

34. Kagaya Y, Ohmiya K, Hattori T. RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic acids research. 1999;27(2):470–8. doi: 10.1093/nar/27.2.470 9862967

35. Chen XL, Song RT, Yu MY, Sui JM, Wang JS, Qiao LX. Cloning and functional analysis of the chitinase gene promoter in peanut. Genet. Mol. Res. 2015 Oct 19;14:12710–22. doi: 10.4238/2015.October.19.15 26505422

36. Quinn JM, Barraco P, Eriksson M, Merchant S. Coordinate copper-and oxygen-responsive Cyc6 andCpx1 expression in Chlamydomonas is mediated by the same element. Journal of Biological Chemistry. 2000 Mar 3;275(9):6080–9. doi: 10.1074/jbc.275.9.6080 10692397

37. Janiak A, Kwaśniewski M, Szarejko I. Gene expression regulation in roots under drought. Journal of experimental botany. 2015 Dec 11;67(4):1003–14. doi: 10.1093/jxb/erv512 26663562

38. Oyiga BC, Sharma RC, Shen J, Baum M, Ogbonnaya FC, Léon J, et al. Identification and characterization of salt tolerance of wheat germplasm using a multivariable screening approach. Journal of Agronomy and Crop Science. 2016 Dec;202(6):472–85. doi: 10.1111/jac.12178

39. Nezhadahmadi A, Prodhan ZH, Faruq G. Drought tolerance in wheat. The Scientific World Journal. 2013;2013. doi: 10.1155/2013/610721

40. Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, et al. Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant physiology. 2007 Apr 1;143(4):1739–51. doi: 10.1104/pp.106.094532 17293435

41. Xiong H, Li J, Liu P, Duan J, Zhao Y, Guo X, et al. Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS One. 2014 Mar 25;9(3):e92913. doi: 10.1371/journal.pone.0092913 24667379

42. Shani E, Salehin M, Zhang Y, Sanchez SE, Doherty C, Wang R, et al. Plant stress tolerance requires auxin-sensitive Aux/IAA transcriptional repressors. Current Biology. 2017 Feb 6;27(3):437–44. doi: 10.1016/j.cub.2016.12.016 28111153

43. Kong D, Li M, Dong Z, Ji H, Li X. Identification of TaWD40D, a wheat WD40 repeat-containing protein that is associated with plant tolerance to abiotic stresses. Plant cell reports. 2015 Mar 1;34(3):395–410. doi: 10.1007/s00299-014-1717-1 25447637

44. Jisha V, Dampanaboina L, Vadassery J, Mithöfer A, Kappara S, Ramanan R. Overexpression of an AP2/ERF type transcription factor OsEREBP1 confers biotic and abiotic stress tolerance in rice. PloS one. 2015 Jun 2;10(6):e0127831. doi: 10.1371/journal.pone.0127831 26035591

45. Huang J, Sun SJ, Xu DQ, Yang X, Bao YM, Wang ZF, et al. Increased tolerance of rice to cold, drought and oxidative stresses mediated by the overexpression of a gene that encodes the zinc finger protein ZFP245. Biochemical and Biophysical Research Communications. 2009 Nov 20;389(3):556–61. doi: 10.1016/j.bbrc.2009.09.032 19751706

46. Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, et al. Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. Journal of experimental botany. 2010 May 11;61(10):2807–18. doi: 10.1093/jxb/erq120 20460361

47. Liu Q, Wang Z, Xu X, Zhang H, Li C. Genome-wide analysis of C2H2 Zinc-finger family transcription factors and their responses to abiotic stresses in poplar (Populus trichocarpa). PloS one. 2015 Aug 3;10(8):e0134753. doi: 10.1371/journal.pone.0134753 26237514

48. Park HY, Seok HY, Park BK, Kim SH, Goh CH, Lee BH, et al. Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress. Biochemical and biophysical research communications. 2008 Oct 10;375(1):80–5. doi: 10.1016/j.bbrc.2008.07.128 18680727

49. Varshney RK, Hiremath PJ, Lekha P, Kashiwagi J, Balaji J, Deokar AA, et al. A comprehensive resource of drought-and salinity-responsive ESTs for gene discovery and marker development in chickpea (Cicer arietinum L.). BMC genomics. 2009 Dec;10(1):523. doi: 10.1186/1471-2164-10-523 19912666

50. Chardin C, Girin T, Roudier F, Meyer C, Krapp A. The plant RWP-RK transcription factors: key regulators of nitrogen responses and of gametophyte development. Journal of Experimental Botany. 2014 Jul 1;65(19):5577–87. doi: 10.1093/jxb/eru261 24987011

51. Zhichang Z, Wanrong Z, Jinping Y, Jianjun Z, Xufeng LZ, Yang Y. Over-expression of Arabidopsis DnaJ (Hsp40) contributes to NaCl-stress tolerance. African Journal of Biotechnology. 2010;9(7):972–8. doi: 10.5897/AJB09.1450

52. Hartl FU. Molecular chaperones in cellular protein folding. Nature. 1996 Jun;381(6583):571. doi: 10.1038/381571a0 8637592

53. Frydman J. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annual review of biochemistry. 2001 Jul;70(1):603–47. doi: 10.1146/annurev.biochem.70.1.603 11395418

54. Lee KW, Rahman MA, Kim KY, Choi GJ, Cha JY, Cheong MS, et al. Overexpression of the alfalfa DnaJ-like protein (MsDJLP) gene enhances tolerance to chilling and heat stresses in transgenic tobacco plants. Turkish Journal of Biology. 2018 Feb 15;42(1):12–22. doi: 10.3906/biy-1705-30 30814866

55. Fu Q, Li S, Yu D. Identification of an Arabidopsis Nodulin-related protein in heat stress. Molecules and cells. 2010 Jan 1;29(1):77–84. doi: 10.1007/s10059-010-0005-3 20016941

56. Reddy AS, Shad Ali G. Plant serine/arginine-rich proteins: roles in precursor messenger RNA splicing, plant development, and stress responses. Wiley Interdisciplinary Reviews: RNA. 2011 Nov;2(6):875–89. doi: 10.1002/wrna.98 21766458

57. Kariola T, Brader G, Helenius E, Li J, Heino P, Palva ET. EARLY RESPONSIVE TO DEHYDRATION 15, a negative regulator of abscisic acid responses in Arabidopsis. Plant Physiology. 2006 Dec 1;142(4):1559–73. doi: 10.1104/pp.106.086223 17056758

58. Alves MS, Fontes EP, Fietto LG. Early responsive to dehydration 15, a new transcription factor that integrates stress signaling pathways. Plant signaling & behavior. 2011 Dec 1;6(12):1993–6. doi: 10.4161/psb.6.12.18268

59. Akagi A, Engelberth J, Stotz HU. Interaction between polygalacturonase-inhibiting protein and jasmonic acid during defense activation in tomato against Botrytis cinerea. European journal of plant pathology. 2010 Dec 1;128(4):423–8. doi: 10.1007/s10658-010-9684-z

60. Mahalingam R, Wang G, Knap HT. Polygalacturonase and polygalacturonase inhibitor protein: gene isolation and transcription in Glycine max-Heterodera glycines interactions. Molecular plant-microbe interactions. 1999 Jun;12(6):490–8. doi: 10.1094/MPMI.1999.12.6.490 10356800

61. Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, et al. AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nature cell biology. 2008 Feb;10(2):220. doi: 10.1038/ncb1683 18193034

62. Tata SK, Choi JY, Jung JY, Lim KY, Shin JS, Ryu SB. Laticifer tissue-specific activation of the Hevea SRPP promoter in Taraxacum brevicorniculatum and its regulation by light, tapping and cold stress. Industrial Crops and Products. 2012 Nov 1;40:219–24. doi: 10.1016/j.indcrop.2012.03.012

63. Guo D, Li HL, Tang X, Peng SQ. Molecular and functional characterization of the HbSRPP promoter in response to hormones and abiotic stresses. Transgenic research. 2014 Apr 1;23(2):331–40. doi: 10.1007/s11248-013-9753-0 24043397

64. Dombrowski JE. Salt stress activation of wound-related genes in tomato plants. Plant Physiology. 2003 Aug 1;132(4):2098–107. doi: 10.1104/pp.102.019927 12913164

65. Becerra-Moreno A, Redondo-Gil M, Benavides J, Nair V, Cisneros-Zevallos L, Jacobo-Velázquez DA. Combined effect of water loss and wounding stress on gene activation of metabolic pathways associated with phenolic biosynthesis in carrot. Frontiers in plant science. 2015 Oct 15;6:837. doi: 10.3389/fpls.2015.00837 26528305

66. Qi Y, Yamauchi Y, Ling J, Kawano N, Li D, Tanaka K. The submergence-induced gene OsCTP in rice (Oryza sativa L.) is similar to Escherichia coli cation transport protein ChaC. Plant science. 2005 Jan 1;168(1):15–22. doi: 10.1016/j.plantsci.2004.07.004

67. Baisakh N, RamanaRao MV, Rajasekaran K, Subudhi P, Janda J, Galbraith D, et al. Enhanced salt stress tolerance of rice plants expressing a vacuolar H ATPase subunit c1 (SaVHAc1) gene from the halophyte grass Spartina alterniflora Löisel. Plant biotechnology journal. 2012 May;10(4):453–64. doi: 10.1111/j.1467-7652.2012.00678.x 22284568

68. Song M, Xu W, Xiang Y, Jia H, Zhang L, Ma Z. Association of jacalin-related lectins with wheat responses to stresses revealed by transcriptional profiling. Plant molecular biology. 2014 Jan 1;84(1-2):95–110. doi: 10.1007/s11103-013-0121-5

69. Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Deng XW. Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. The Plant Cell. 2007 Mar 1;19(3):731–49. doi: 10.1105/tpc.106.047688 17337630

70. Du XQ, Wang FL, Li H, Jing S, Yu M, Li J, et al. The Transcription Factor MYB59 Regulates K+/NO3-Translocation in the Arabidopsis Response to Low K+ Stress. The Plant Cell. 2019 Mar 1;31(3):699–714. doi: 10.1105/tpc.18.00674 30760559

71. Amar SB, Safi H, Ayadi M, Azaza J, Khoudi H, Masmoudi K, et al. Analysis of the promoter activity of a wheat dehydrin gene (DHN-5) under various stress conditions. Australian Journal of Crop Science. 2013 Nov;7(12):1875.


Článek vyšel v časopise

PLOS One


2019 Číslo 10