Molecular Mechanism of Salinity Stress Tolerance in Barley (Hordeum vulgare L.) via Meta-Analysis of Transcriptome Data

Document Type : Original Research

Authors
1 Department of Biotechnology, Institute of Science and Modern Technology, Rojava University, Qamishlo, Syria.
2 Department of Biotechnology, Halophyte Biotechnology Research Centre, Azarbaijan Shahid Madani University, Tabriz, Islamic Republic of Iran.
Abstract
Salt stress, as the most important abiotic stress, limits growth of plants and causes extensive damage to agricultural production worldwide. Therefore, it is necessary to identify genes that play a key role in tolerance to salt stress in plants through the analysis of transcriptome data such as microarray and High-Throughput Sequencing (HTS or NGS). In the present research, the combined analysis of microarray data by R packages for Hordeum vulgare L. under salinity stress identified 685 upregulated meta-DEGs (differentially expressed genes) and 766 downregulated meta-DEGs. The upregulated genes mostly belong to abiotic stress tolerance and hormone biosynthesis, and the downregulated genes pertain to late embryogenesis abundant protein and salinity stress response. GO terms in the upregulated genes are mostly associated with response to external and internal stresses; and in the downregulated genes, they are mostly associated with cellular metabolism. In the up and down meta-DEGs by KEGG, most of the genes connected to salinity stress included PP2C, ABF, AGT, and ChiB and F-box connected to the downregulated genes. Moreover, Transcription Factors (TFs) in the up and downregulated meta-DEGs with high frequency included AP2, ERF, bZIP, and bHLH. Most of the hub upregulated genes acquired from this research were metabolite biosynthesis and photosynthesis-related; and the hub downregulated genes were mainly the tricarboxylic acid cycle and glycolysis processes-related. Finally, a comparison was made between this meta-analysis and data obtained from other investigations. The findings validated their up and down expression. Our results give a new understanding about the molecular mechanism and present many TFs and candidate genes for salt stress tolerance in barley breeding programs.

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Adem GD, Roy SJ, Zhou M, Bowman JP, Shabala S (2014) Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biol 14:113.
Aharoni A, Vorst O (2002) DNA microarrays for functional plant genomics. Plant Mol Biol 48(1–2): 99–118.
Ariel FD, Diet A, Crespi M, Chan RL (2010) The LOB-like transcription factor MtLBD1 controls Medicago truncatula root architecture under salt stress. Plant Signal Behav 5: 1666–1668.
Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang YH, Schaller GE, Loraine A, Kieber JJ (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol 162: 272-294.
Boscari A, Clément M, Volkov V, Golldack D, Hybiak J, Miller AJ, Amtmann A, Fricke W (2009) Potassium channels in barley: cloning, functional characterization and expression analyses in relation to leaf growth and development. Plant Cell Environ 32:1761–1777.
Chen X, Tao Y, Ali A, Zhuang Zh, Guo D, Guo Q, Riaz A, Zhang H, Xu P, Liao Y, Wang J, Sun Ch, Xiang Q, Wu X (2019) Transcriptome and Proteome Profiling of Different Colored Rice Reveals Physiological Dynamics Involved in the Flavonoid Pathway. Int J Mol Sci 20: 2463
Chin CH, Chen SH, Wu HH, Ho CW, Ko MT, Lin CY (2014) CytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol 8: 1-7.
Colmer TD, Munns R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Aust J Exp Agric 45: 1425-1443.
Dai H, Cao F, Chen X, Zhang M, Ahmed IM, Chen ZH, Li C, Zhang GP, Wu F (2013) Comparative proteomic analysis of aluminium tolerance in tibetan wild and cultivated barleys. PLoS One 8: e63428.
de Abreu Neto JB, Frei M (2016) Microarray meta-analysis focused on the response of genes involved in redox homeostasis to diverse abiotic stresses in rice. Front Plant Sci 6:1260.
del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53: 1255–1272.
Dou M, Fan S, Yang S, Huang R, Yu H, Feng X (2016) Overexpression of AmRosea1 gene confers drought and salt tolerance in rice. Int J Mol Sci 8 (1): 2.
Fan W, Zhang Zh, Zhang Y (2009) Cloning and molecular characterization of fructose-1,6-bisphosphate aldolase gene regulated by high-salinity and drought in Sesuvium portulacastrum. Plant Cell Rep 28: 975–984.
Gagne JM, Downes BP, Shiu ShH, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. PNAS 99 (17): 11519–11524.
Gao R, Duan K, Guo G, Du Z, Chen Z, Li L, He T, Lu R, Huang J (2013) Comparative transcriptional profiling of two contrasting barley genotypes under salinity stress during the seedling stage. Int J Genomics 1–19.
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124: 1854–1865.
Huang ShH, Zhang JY, Wang LH, Huang LQ (2013) Effect of abiotic stress on the abundance of different vitamin B6 vitamers in tobacco plants. Plant Physiol Biochem 66: 63-67
Igarashi D, Miwa T, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Ohsumi C (2003) Identification of photorespiratory glutamate: glyoxylate aminotransferase (GGAT) gene in Arabidopsis. Plant J 33: 975–987.
Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7: 106–111.
Janská A, Aprile A, Zámečník J, Cattivelli L, Ovesná J (2011) Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct Integr Genomics 11: 307–325.
Jaradat AA, Shahid M, Al-Maskri A (2004) Genetic diversity in the Batini barley landrace from Oman: II. Response to salinity stress. Crop Sci 44 (3): 997–1007.
Jesús MB, Borja CM, Jose MM (2009) Plastidial Glyceraldehyde-3-Phosphate Dehydrogenase Deficiency Leads to Altered Root Development and Affects the Sugar and Amino Acid Balance in Arabidopsis. Plant Physiol 151: 541–558.
Kadotani N, Akagi A, Takatsuji H, Miwa T, Igarashi D (2016) Exogenous proteinogenic amino acids induce systemic resistance in rice. BMC Plant Biology 16: 60.
Kilian J, Peschke F, Berendzen KW, Harter K, Wanke D (2012) Prerequisites, performance and profits of transcriptional profiling the abiotic stress response. Biochim Biophys Acta 1819:166–175.
Kottapalli KR, Satoh K, Rakwal R, Shibato J, Doi K, Nagata T, Kikuchi Sh (2007) Combining In Silico Mapping and Arraying: an Approach to Identifying Common Candidate Genes for Submergence Tolerance and Resistance to Bacterial Leaf Blight in Rice. Mol Cells 24 (3): 394-408.
Li D, Fu F, Zhang H, Song F (2015) Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genomics 16 (1): 771.
Liu Y, Song Q, Li D, Yang X, Li D (2017) Multifunctional roles of plant dehydrins in response to environmental stresses. Front Plant Sci 8:1018.
Moreau Y, Aerts S, De MB, De SB, Dabrowski M (2003) Comparison and metaanalysis of microarray data: from the bench to the computer desk. Trends Genet 19: 570-577.
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozak K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819: 97–103.
Nouri MZ, Moumeni A, Komatsu S (2015) Abiotic stresses: Insight into gene regulation and protein expression in photosynthetic pathways of plants. Int J Mol Sci 16: 20392–20416.
Ozturk ZN, Talame V, Deyhoyos M, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573.
Pinto MC, Lavermicocca P, Evidente A, Corsaro MM, Lazzaroni S, Gara LD (2003) Exopolysaccharides produced by plant pathogenic bacteria affect ascorbate metabolism in Nicotiana tabacum. Plant Cell Physiol 44 (8): 803-810.
Potuschak T, Lechner E, Parmentier Y, Yanagisawa S, Grava S, Koncz C, Genschik P (2003) EIN3-dependent regulation of plant ethylene hormone signalling by two Arabidopsis Fbox protein:EBF1 and EBF2. Cell 115:679–689.
Rodrigues FA, Laia MLD, Zingaretti SM (2009) Analysis of gene expression profiles under water stress in tolerant and sensitive sugarcane plants. Plant Science 176: 286–302.
Roslyakova TV, Molchan OV, Vasekina AV, Lazareva EM, Sokolik AI, Yurin VM, de Boer AH, Babakov AV (2011) Salt tolerance of barley: relations between expression of isoforms of vacuolar Na+/H+-antiporter and 22Na+ accumulation. Russ J Plant Physiol 58:24–35.
Roy SJ, Huang W, Wang XJ, Evrard A, Schmöckel SM, Zafar ZU, Tester M (2013) A novel protein kinase involved in Na+ exclusion revealed from positional cloning. Plant Cell Environ 36:553–568.
Tsuda K, Tsvetanov S, Takumi S, Mori N, Atanoassov A, Nakamura C (2000) New members of a cold-responsive group-3 Lea/Rab-related Cor gene family from common wheat (Triticum aestivum L.). Genes Genet Syst 75:179–188.
Ueda A, Kathiresan A, Inada M, Narita Y, Nakamura T, Shi W, Takabe T, Bennett J (2004) Osmotic stress in barley regulates expression of a different set of genes than salt stress does. J Exp Bot 55:2213–2218.
Usadel B, Schlüter U, Mølhøj M, Gipmans M, Verma R, Kossmann J, Reiter WD, Pauly M (2004) Identification and characterization of a UDP-d-glucuronate 4-epimerase in Arabidopsis. FEBS Letters 569: 327–331
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Close TJ (2007) Large-scale expression profiling and physiological characterization of jasmonic acid-mediated adaptation of barley to salinity stress. Plant Cell Environ 30: 410–421.
Walia H, Wilson C, Wahid A, Condamine P, Cui X, Close TJ (2005) Expression analysis of barley (Hordeum vulgare L.) during salinity stress. Funct Integr Genomics 6 (2): 143–156.
Yang Q, Gilmartin GM, Doublié S (2010) Structural basis of UGUA recognition by the Nudix protein CFI (m) 25 and implications for a regulatory role in mRNA 3′ processing. Proc Natl Acad Sci 107: 10062 –10067.
Ying S, Jing-Yu X, Bian-Yun Y, Ben-Zhong Z, Yun-Bo L (2004) Influence of salt stress on expression of some genes involved in the ethylene signalling pathway in tomato seedlings. Chin J Agric Biotechnol 1(2):115–118.
You C, Chen L, He H, Wu L, Wang Sh, Ding Y, Ma Ch (2017) iTRAQ-based proteome profile analysis of superior and inferior Spikelets at early grain filling stage in japonica Rice. BMC Plant Biology 17:100
Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4: 401e406.