Abstract
Salinity adversely affects growth and yield of crop plants. Plants respond to salinity using a series of physiological and biochemical mechanisms through an orchestrated regulation of many genes. Halophyte species have attracted attention of plant biologists to explore their salinity tolerance mechanisms. This knowledge may provide novel routes to improve salinity stress tolerance in crop plants resulting in higher sustainable yields. Salicornia persica is an Iranian native halophyte species that can tolerate extreme salinity. We performed Illumina high-throughput RNA sequencing and functional annotation on shoots of S. persica under control and salinity conditions to investigate the molecular mechanisms controlling salinity adaptation in this halophyte. Over 68 million and 65 million clean reads were generated from control and salinity-treated libraries, respectively. We identified 1595 differentially expressed genes including several transcription factors, protein kinases and transporters. Functional annotation analysis suggested that energy homeostasis and synthesis of primary metabolites play key roles for salinity adaptation in S. persica. Furthermore, gene network analysis indicated that abscisic acid and calcium signaling as well as sodium compartmentalization are major components to confer tolerance to salinity in S. persica. This first report on transcriptome analysis of the halophyte S. persica provided insight into the mechanisms underlying salinity tolerance and served as a platform for future studies.
Similar content being viewed by others
References
Adams E, Shin R (2014) Transport, signaling, and homeostasis of potassium and sodium in plants. J Integr Plant Biol 56(3):231–249. https://doi.org/10.1111/jipb.12159
Aghaleh M, Niknam V, Ebrahimzadeh H, Razavi K (2014) Antioxidative enzymes in two in vitro cultured Salicornia species in response to increasing salinity. Biol Plant 58(2):391–394. https://doi.org/10.1007/s10535-014-0389-6
Ahmad ST, Sima NAKK, Mirzaei HH (2013) Effects of sodium chloride on physiological aspects of Salicornia persica growth. J Plant Nutr 36(3):401–414. https://doi.org/10.1080/01904167.2012.746366
Akhani H (2003) Salicornia persica Akhani (Chenopodiaceae), a remarkable new species from Central Iran. Linz Biol Beitr 35(1):607–612
Ali A, Yun D-J (2017) Salt stress tolerance; what do we learn from halophytes? J Plant Biol 60(5):431–439. https://doi.org/10.1007/s12374-017-0133-9
Altenbach D, Robatzek S (2007) Pattern recognition receptors: from the cell surface to intracellular dynamics. Mol Plant Microbe Interact 20(9):1031–1039. https://doi.org/10.1094/MPMI-20-9-1031
Assenov Y, Ramírez F, Schelhorn S-E, Lengauer T, Albrecht M (2007) Computing topological parameters of biological networks. Bioinformatics 24(2):282–284. https://doi.org/10.1093/bioinformatics/btm554
Bar M, Avni A (2009) EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J 59(4):600–611. https://doi.org/10.1111/j.1365-313X.2009.03897.x
Bedre R, Mangu VR, Srivastava S, Sanchez LE, Baisakh N (2016) Transcriptome analysis of smooth cordgrass (Spartina alterniflora Loisel), a monocot halophyte, reveals candidate genes involved in its adaptation to salinity. BMC Genom 17(1):657. https://doi.org/10.1186/s12864-016-3017-3
Boccaletti S, Latora V, Moreno Y, Chavez M, Hwang D-U (2006) Complex networks: structure and dynamics. Phys Rep 424(4):175–308. https://doi.org/10.1016/j.physrep.2005.10.009
Chaumont F, Tyerman SD (2014) Aquaporins: highly regulated channels controlling plant water relations. Plant Physiol 164(4):1600–1618. https://doi.org/10.1104/pp.113.233791
Chen L, Wang Q-Q, Zhou L, Ren F, Li D-D, Li X-B (2013) Arabidopsis CBL-interacting protein kinase (CIPK6) is involved in plant response to salt/osmotic stress and ABA. Mol Biol Rep 40(8):4759–4767. https://doi.org/10.1007/s11033-013-2572-9
Cheng N-H, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138(4):2048–2060. https://doi.org/10.1104/pp.105.061218
Contento AL, Bassham DC (2012) Structure and function of endosomes in plant cells. J Cell Sci 125(15):3511–3518. https://doi.org/10.1242/jcs.093559
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379. https://doi.org/10.1016/j.tplants.2014.02.001
Diray-Arce J, Clement M, Gul B, Khan MA, Nielsen BL (2015) Transcriptome assembly, profiling and differential gene expression analysis of the halophyte Suaeda fruticosa provides insights into salt tolerance. BMC Genom 16(1):353. https://doi.org/10.1186/s12864-015-1553-x
Diray-Arce J, Gul B, Khan MA, Nielsen B (2016) Halophyte transcriptomics: understanding mechanisms of salinity tolerance. Halophytes for food security in dry lands. Elsevier, New York, pp 157–175
Ebine K, Ueda T (2009) Unique mechanism of plant endocytic/vacuolar transport pathways. J Plant Res 122(1):21–30. https://doi.org/10.1007/s10265-008-0200-x
Fan P, Nie L, Jiang P, Feng J, Lv S, Chen X, Bao H, Guo J, Tai F, Wang J (2013) Transcriptome analysis of Salicornia europaea under saline conditions revealed the adaptive primary metabolic pathways as early events to facilitate salt adaptation. PLoS ONE 8(11):e80595. https://doi.org/10.1371/journal.pone.0080595
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol. https://doi.org/10.1111/j.1469-8137.2008.02531.x
Gangola MP, Ramadoss BR (2018) Sugars play a critical role in abiotic stress tolerance in plants. Biochemical physiological and molecular avenues for combating abiotic stress tolerance in plants. Elsevier, Amsterdam, pp 17–38
Girvan M, Newman ME (2002) Community structure in social and biological networks. Proc Natl Acad Sci USA 99(12):7821–7826. https://doi.org/10.1073/pnas.122653799
Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151. https://doi.org/10.3389/fpls.2014.00151
Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics. https://doi.org/10.1155/2014/701596
Hossain MA, Cho J-I, Han M, Ahn C-H, Jeon J-S, An G, Park PB (2010) The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J Plant Physiol 167(17):1512–1520. https://doi.org/10.1016/j.jplph.2010.05.008
Isayenkov SV, Maathuis FJ (2019) Plant salinity stress: many unanswered questions remain. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00080
Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68:405–434. https://doi.org/10.1146/annurev-arplant-042916-040936
Jaradat MR, Feurtado JA, Huang D, Lu Y, Cutler AJ (2013) Multiple roles of the transcription factor AtMYBR1/AtMYB44 in ABA signaling, stress responses, and leaf senescence. BMC Plant Biol 13(1):192. https://doi.org/10.1186/1471-2229-13-192
Jha B, Lal S, Tiwari V, Yadav SK, Agarwal PK (2012) The SbASR-1 gene cloned from an extreme halophyte Salicornia brachiata enhances salt tolerance in transgenic tobacco. Mar Biotechnol 14(6):782–792. https://doi.org/10.1007/s10126-012-9442-7
Jha RK, Patel J, Mishra A, Jha B (2019) 18 Introgression of halophytic salt stress-responsive genes for developing stress tolerance in crop plants. Halophytes and climate change: adaptive mechanisms and potential uses, 275
Ji H, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6(2):275–286. https://doi.org/10.1093/mp/sst017
Kaleem F, Shabir G, Aslam K, Rasul S, Manzoor H, Shah SM, Khan AR (2018) An overview of the genetics of plant response to salt stress: present status and the way forward. Appl Biochem Biotechnol 186(2):306–334. https://doi.org/10.1007/s12010-018-2738-y
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Khan MA (2008) Crop and forage production using saline waters. Daya Books, Delhi
Khedia J, Agarwal P, Agarwal PK (2018) AlNAC4 transcription factor from halophyte Aeluropus lagopoides mitigates oxidative stress by maintaining ROS homeostasis in transgenic tobacco. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01522
Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47(3):343–355. https://doi.org/10.1111/j.1365-313X.2006.02782.x
Kumar K, Mosa KA (2015) Ion transporters: a decisive component of salt stress tolerance in plants. managing salt tolerance in plants. Mol Genom Perspect. 5:372–390
Kumari J, Udawat P, Dubey AK, Haque MI, Rathore MS, Jha B (2017) Overexpression of SbSI-1, a nuclear protein from salicornia brachiata confers drought and salt stress tolerance and maintains photosynthetic efficiency in transgenic tobacco. Front Plant Sci 8:1215. https://doi.org/10.3389/fpls.2017.01215
Lee D-K, Ahn S, Cho HY, Yun HY, Park JH, Lim J, Lee J, Kwon SW (2016) Metabolic response induced by parasitic plant-fungus interactions hinder amino sugar and nucleotide sugar metabolism in the host. Sci Rep 6:37434. https://doi.org/10.1038/srep37434
Leshem Y, Seri L, Levine A (2007) Induction of phosphatidylinositol 3-kinase-mediated endocytosis by salt stress leads to intracellular production of reactive oxygen species and salt tolerance. Plant J 51(2):185–197. https://doi.org/10.1111/j.1365-313X.2007.03134.x
Liu J, Niu Y, Zhang J, Zhou Y, Ma Z, Huang X (2017) Ca2+ channels and Ca2+ signals involved in abiotic stress responses in plant cells: recent advances. Plant Cell Tiss Org. https://doi.org/10.1007/s11240-017-1350-0
Liu Q, Tang J, Wang W, Zhang Y, Yuan H, Huang S (2018) Transcriptome analysis reveals complex response of the medicinal/ornamental halophyte Iris halophila Pall. to high environmental salinity. Ecotox Environ Safe 165:250–260. https://doi.org/10.1016/j.ecoenv.2018.09.003
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Li W, Wang D, Jinn T, Chang Q, Yin D, Xu S, Liu B, Liu L (2011) The vacuolar Na+/H+ antiporter gene SsNHX1 from the halophyte Salsola soda confers salt tolerance in transgenic alfalfa (Medicago sativa L.). Plant Mol Biol Rep 29(2):278–290. https://doi.org/10.1007/s11105-010-0224-y
Luo L, Zhang P, Zhu R, Fu J, Su J, Zheng J, Wang Z, Wang D, Gong Q (2017) Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front Plant Sci 8:1459. https://doi.org/10.3389/fpls.2017.01459
Lv S, Jiang P, Chen X, Fan P, Wang X, Li Y (2012) Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiol Biochem 51:47–52. https://doi.org/10.1016/j.plaphy.2011.10.015
Ma J, Zhang M, Xiao X, You J, Wang J, Wang T, Yao Y, Tian C (2013) Global transcriptome profiling of Salicornia europaea L shoots under NaCl treatment. PLoS ONE 8(6):65877. https://doi.org/10.1371/journal.pone.0065877
Mansouri M, Naghavi MR, Alizadeh H, Mohammadi-Nejad G, Mousavi SA, Salekdeh GH, Tada Y (2019) Transcriptomic analysis of Aegilops tauschii during long-term salinity stress. Funct Integr Genom 19(1):13–28. https://doi.org/10.1007/s10142-018-0623-y
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621. https://doi.org/10.1038/nmeth.1226
Munns R, Wallace PA, Teakle NL, Colmer TD (2010) Measuring soluble ion concentrations Na+, K+, Cl− in salt-treated plants. In: Plant stress tolerance. Springer, New York. https://doi.org/10.1007/978-1-60761-702-0_23
Nejad ES, Askari H, Gholami M (2014) Evaluation of cellular responses of the halophyte 'Aeluropus littoralis' to salinity stress through cell growth, sugars and polyamines content. PKJ 3 (1):1. https://www.sciencej.com/sadeghnejad_3
Nikalje GC, Nikam D, Suprasanna P (2017) Looking at halophytic adaptation to high salinity through genomics landscape. Curr Genom 18(6):542–552. https://doi.org/10.2174/1389202918666170228143007
Nikitin A, Egorov S, Daraselia N, Mazo I (2003) Pathway studio: the analysis and navigation of molecular networks. Bioinformatics 19(16):2155–2157. https://doi.org/10.1093/bioinformatics/btg290
Paez Valencia J, Goodman K, Otegui MS (2016) Endocytosis and endosomal trafficking in plants. Annu Rev Plant Biol 67:309–335. https://doi.org/10.1146/annurev-arplant-043015-112242
Parida AK, Veerabathini SK, Kumari A, Agarwal PK (2016) Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front Plant Sci 7:351. https://doi.org/10.3389/fpls.2016.00351
Patel S (2016) Salicornia: evaluating the halophytic extremophile as a food and a pharmaceutical candidate. Biotech 6(1):104. https://doi.org/10.1007/s13205-016-0418-6
Penna S, Teixeira da Silva J, Anant BV (2006) Plant abiotic stress, sugars and transgenics: a perspective. Floricult Ornament Plant Biotechnol 3:86–93
Persak H, Pitzschke A (2014) Dominant repression by Arabidopsis transcription factor MYB44 causes oxidative damage and hypersensitivity to abiotic stress. IJMS 15(2):2517–2537. https://doi.org/10.3390/ijms15022517
Rapaport F, Khanin R, Liang Y, Pirun M, Krek A, Zumbo P, Mason CE, Socci ND, Betel D (2013) Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol 14(9):3158. https://doi.org/10.1186/gb-2013-14-9-r95
Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotech 26:115–124. https://doi.org/10.1016/j.copbio.2013.12.004
Saier MH Jr, Tran CV, Barabote RD (2006) TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res 34(1):181–186. https://doi.org/10.1093/nar/gkj001
Sairam R, Srivastava G (2002) Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. Plant Sci 162(6):897–904. https://doi.org/10.1016/S0168-9452(02)00037-7
Scardoni G, Petterlini M, Laudanna C (2009) Analyzing biological network parameters with CentiScaPe. Bioinformatics 25(21):2857–2859. https://doi.org/10.1093/bioinformatics/btp517
Seifert GJ (2004) Nucleotide sugar interconversions and cell wall biosynthesis: how to bring the inside to the outside. Curr Opin Plant Biol 7(3):277–284. https://doi.org/10.1016/j.pbi.2004.03.004
Shamloo-Dashtpagerdi R, Razi H, Ebrahimie E, Niazi A (2018) Molecular characterization of Brassica napus stress related transcription factors, BnMYB44 and BnVIP1, selected based on comparative analysis of Arabidopsis thaliana and Eutrema salsugineum transcriptomes. Mol Biol Rep 45(5):1111–1124. https://doi.org/10.1007/s11033-018-4262-0
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498–2504. https://doi.org/10.1101/gr.1239303
Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44. https://doi.org/10.1038/nprot.2008.211
Sheng Q, Vickers K, Zhao S, Wang J, Samuels DC, Koues O, Shyr Y, Guo Y (2016) Multi-perspective quality control of Illumina RNA sequencing data analysis. Brife Funct Genom 16(4):194–204. https://doi.org/10.1093/bfgp/elw035
Shin D, Koo YD, Lee J, Lee H-j, Baek D, Lee S, Cheon C-I, Kwak S-S, Lee SY, Yun D-J (2004) Athb-12, a homeobox-leucine zipper domain protein from Arabidopsis thaliana, increases salt tolerance in yeast by regulating sodium exclusion. Biochem Bioph Res Co 323(2):534–540. https://doi.org/10.1016/j.bbrc.2004.08.127
Shpigel M, Ben-Ezra D, Shauli L, Sagi M, Ventura Y, Samocha T, Lee J (2013) Constructed wetland with Salicornia as a biofilter for mariculture effluents. Aquaculture 412:52–63. https://doi.org/10.1016/j.aquaculture.2013.06.038
Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P (2016) The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw937
Sicilia A, Testa G, Santoro DF, Cosentino SL, Lo Piero AR (2019) RNASeq analysis of giant cane reveals the leaf transcriptome dynamics under long-term salt stress. BMC Plant Biol 19(1):355. https://doi.org/10.1186/s12870-019-1964-y
Sutter J-U, Sieben C, Hartel A, Eisenach C, Thiel G, Blatt MR (2007) Abscisic acid triggers the endocytosis of the Arabidopsis KAT1 K+ channel and its recycling to the plasma membrane. Curr Biol 17(16):1396–1402. https://doi.org/10.1016/j.cub.2007.07.020
Tabas-Madrid D, Nogales-Cadenas R, Pascual-Montano A (2012) GeneCodis3: a non-redundant and modular enrichment analysis tool for functional genomics. Nucleic Acids Res 40(W1):W478–W483. https://doi.org/10.1093/nar/gks402
Tiwari V, Chaturvedi AK, Mishra A, Jha B (2015) Introgression of the SbASR-1 gene cloned from a halophyte Salicornia brachiata enhances salinity and drought endurance in transgenic groundnut (Arachis hypogaea) and acts as a transcription factor. PLoS ONE 10(7):e0131567. https://doi.org/10.1371/journal.pone.0131567
Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J 58(5):778–790. https://doi.org/10.1111/j.1365-313X.2009.03812.x
Tsukagoshi H, Suzuki T, Nishikawa K, Agarie S, Ishiguro S, Higashiyama T (2015) RNA-seq analysis of the response of the halophyte, Mesembryanthemum crystallinum (ice plant) to high salinity. PLoS ONE 10(2):e0118339. https://doi.org/10.1371/journal.pone.0118339
Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Method enzymol. Elsevier, Amsterdam, pp 419–438
Udawat P, Jha RK, Mishra A, Jha B (2017) Overexpression of a plasma membrane-localized SbSRP-like protein enhances salinity and osmotic stress tolerance in transgenic tobacco. Front Plant Sci 8:582. https://doi.org/10.3389/fpls.2017.00582
Wang Y, Jiang L, Chen J, Tao L, An Y, Cai H, Guo C (2018) Overexpression of the alfalfa WRKY11 gene enhances salt tolerance in soybean. PLoS ONE 13(2):e0192382. https://doi.org/10.1371/journal.pone.0192382
Wu G-Q, Wang J-L, Li S-J (2019) Genome-wide identification of Na+/H+ antiporter (NHX) genes in sugar beet (Beta vulgaris L.) and their regulated expression under salt stress. Genes 10(5):401. https://doi.org/10.3390/genes10050401
Yamamoto N, Takano T, Tanaka K, Ishige T, Terashima S, Endo C, Kurusu T, Yajima S, Yano K, Tada Y (2015) Comprehensive analysis of transcriptome response to salinity stress in the halophytic turf grass Sporobolus virginicus. Front Plant Sci 6:241. https://doi.org/10.3389/fpls.2015.00241
Yao L, Wang J, Li B, Meng Y, Ma X, Si E, Ren P, Yang K, Shang X, Wang H (2018) Transcriptome sequencing and comparative analysis of differentially-expressed isoforms in the roots of Halogeton glomeratus under salt stress. Gene 646:159–168. https://doi.org/10.1016/j.gene.2017.12.058
Ye W, Wang T, Wei W, Lou S, Lan F, Zhu S, Li Q, Ji G, Lin C, Wu X (2019) The full-length transcriptome of Spartina alterniflora reveals the complexity of high salt tolerance in monocotyledonous halophyte. bioRxiv:680819. https://doi.org/10.1101/680819
Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61(4):672–685. https://doi.org/10.1111/j.1365-313X.2009.04092.x
Zeng D-E, Hou P, Xiao F, Liu Y (2015) Overexpression of Arabidopsis XERICO gene confers enhanced drought and salt stress tolerance in rice (Oryza sativa L.). J Plant Biochem Biot 24(1):56–64. https://doi.org/10.1007/s13562-013-0236-4
Zhang L, Niu Y, Huridu H, Hao J, Qi Z, Hasi A (2014) Salicornia europaea L. Na+/H+ antiporter gene improves salt tolerance in transgenic alfalfa (Medicago sativa L.). Genet Mol Res 13(3):5350–5360. https://doi.org/10.4238/2014.July.24.14
Zhang W, Chen J, Yang Y, Tang Y, Shang J, Shen B (2011) A practical comparison of de novo genome assembly software tools for next-generation sequencing technologies. PLoS ONE 6(3):e17915. https://doi.org/10.1371/journal.pone.0017915
Zhang X, Liu X, Wu L, Yu G, Wang X, Ma H (2015) The SsDREB transcription factor from the succulent halophyte Suaeda salsa enhances abiotic stress tolerance in transgenic tobacco. Int J Genom. https://doi.org/10.1155/2015/875497
Zhang Y, Shi S, Li F, Zhao C, Li A, Hou L, Xia H, Wang B, Baltazar JL, Wang X (2019) Global transcriptome analysis provides new insights in Thellungiella salsuginea stress response. Plant Biol. https://doi.org/10.1111/plb.13006
Zheng Y, Jiao C, Sun H, Rosli HG, Pombo MA, Zhang P, Banf M, Dai X, Martin GB, Giovannoni JJ (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9(12):1667–1670. https://doi.org/10.1016/j.molp.2016.09.014
Zhao Y, Yang Z, Ding Y, Liu L, Han X, Zhan J, Wei X, Diao Y, Qin W, Wang P (2019) Over-expression of an R2R3 MYB gene, GhMYB73, increases tolerance to salt stress in transgenic Arabidopsis. Plant Sci 286:28–36. https://doi.org/10.1016/j.plantsci.2019.05.021
Zhao Z, Zhang G, Zhou S, Ren Y, Wang W (2017) The improvement of salt tolerance in transgenic tobacco by overexpression of wheat F-box gene TaFBA1. Plant Sci 259:71–85. https://doi.org/10.1016/j.plantsci.2017.03.010
Zhang Y, Lai J, Sun S, Li Y, Liu Y, Liang L, Chen M, Xie Q (2008) Comparison analysis of transcripts from the halophyte Thellungiella halophila. J Integr Plant Biol 50(10):1327–1335. https://doi.org/10.1111/j.1744-7909.2008.00740.x
Zhu J-K (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324. https://doi.org/10.1016/j.cell.2016.08.029
Acknowledgments
The authors would like to thank Shiraz University for funding this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Aliakbari, M., Razi, H., Alemzadeh, A. et al. RNA-seq Transcriptome Profiling of the Halophyte Salicornia persica in Response to Salinity. J Plant Growth Regul 40, 707–721 (2021). https://doi.org/10.1007/s00344-020-10134-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-020-10134-z