Abstract
Key message
The first transcriptome analyses of Tetraena mongolica provided 224,618 Unigenes and identified the genes that were differentially expressed under salt and drought conditions, giving some insights into the unique adaptive capacity of this relic plant.
Abstract
Tetraena mongolica Maxim, the only member of the Tetraena genus in the Zygophyllaceae, is endemic to the northwest of China. As one of the relic shrubs of the Paleo-Mediterranean flora, T. mongolica plays a key role in preserving the local ecological environment. To investigate its good adaptability in desert, we studied the transcriptome of T. mongolica under NaCl and PEG6000 stresses. Three libraries were constructed from a mixture of seedlings and mature plants of T. mongolica, and the de novo transcriptome was sequenced using an Illumina HiSeq 4000. Approximately 218.15 million clean reads were assembled de novo into 383,612 transcripts, and 116,027 All-Unigenes were identified. By aligning All-Unigene sequences against the NR database, we found that most of the All-Unigenes had very low matches with the sequences from other plants. A total of 21,112 SSRs and 6 types of SNP variants were identified. The RNA-Seq data revealed 60 transcription factor (TF) families with 3163 genes in total. Six libraries were constructed from the separate control or stressed seedlings, and the transcriptome was sequenced using a BGISEQ-500 platform. There are 1105 and 1383 differentially expressed genes (DEGs) with 42 and 54 TFs under NaCl and PEG6000 treatment, respectively. The genes that were putatively involved in salt and osmotic stresses were searched and analyzed. Quantitative reverse transcription PCR (qRT-PCR) showed that DEG expression profiles were consistent with those from RNA-seq (RNA sequencing). Overall, this study provides new insights into the molecular mechanisms that control salt and drought stress responses in T. mongolica.
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Availability of supporting data
The transcriptome sequencing raw data were deposited in the National Center for Biotechnology Information with the Accession No. PRJNA490096 and PRJNA490438.
Abbreviations
- BLAST:
-
Basic local alignment search tool
- DEGs:
-
Differentially expressed genes
- GO:
-
Gene ontology
- KEGG:
-
Kyoto encyclopedia of genes and genomes
- KOG:
-
Eukaryotic Orthologous Groups
- Nr/Nt:
-
Non-redundant database and nucleotide collection
- PEG:
-
Polyethylene glycol
- QC:
-
Quality control
- qRT-PCR:
-
Quantitative reverse transcription PCR
- RNA-seq:
-
RNA sequencing
- TFs:
-
Transcription factors
References
Abdallah SB, Aung B, Amyot L, Lalin I, Lachaal M, Karray-Bouraoui N, Hannoufa A (2016) Salt stress (NaCl) affects plant growth and branch pathways of carotenoid and flavonoid biosyntheses in Solanum nigrum. Acta Physiol Plant 38(3):1–13
Allakhverdiev SI, Murata N (2008) Salt stress inhibits photosystems II and I in cyanobacteria. Photosynth Res 98(1–3):529–539
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123(3):1047–1056
Bhattacharjee A, Khurana JP, Jain M (2016) Characterization of rice homeobox genes, OsHOX22 and OsHOX24, and over-expression of OsHOX24 in transgenic Arabidopsis suggest their role in abiotic stress response. Front Plan Sci 7:627
Chen G, Komatsuda T, Ma J, Li C, Yamaji N, Nevo E (2011) A functional cutin matrix is required for plant protection against water loss. Plant Signal Behav 6:1297–1299
Chen J, Zhang D, Zhang C, Xia X, Yin W, Tian Q (2015) A putative PP2C-encoding gene negatively regulates ABA signaling in Populus euphratica. PLoS One 10(10):e0139466
Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genom 2008:1–12
Dang Z, Zheng L, Wang J, Gao Z, Wu S, Qi Z, Wang Y (2013) Transcriptomic profiling of the salt-stress response in the wild recretohalophyte Reaumuria trigyna. BMC Genomics 14(1):29
Ding Y, Liu N, Virlouvet L, Riethoven JJ, Fromm M, Avramova Z (2013) Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol 13(1):229
Doddamani D, Katta MA, Khan AW, Agarwal G, Shah TM, Varshney RK (2014) CicArMiSatDB: the chickpea microsatellite database. BMC Bioinform 15(1):212
Fu LK, Jin JM (1992) China plant red data book—rare and endangered plants. Science Press, Beijing
Gao F, Li H, Xiao Z, Wei C, Feng J, Zhou Y (2018) De novo transcriptome analysis of Ammopiptanthus nanus and its comparative analysis with A. mongolicus. Trees 32(1):287–300
Ge X, Hwang C, Liu Z, Huang C, Huang W, Hung K, Wang W, Chiang T (2011) Conservation genetics and phylogeography of endangered and endemic shrub Tetraena mongolica (Zygophyllaceae) in Inner Mongolia, China. BMC Genetics 12(1):1
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma FD, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotech 29:644–652
Guo Y, Jiang Q, Hu Z, Sun X, Fan S, Zhang H (2018) Function of the auxin-responsive gene TaSAUR75 under salt and drought stress. Crop J 6(2):181–190
Haynsen MS, Vatanparast M, Mahadwar G, Zhu D, Moger-Reischer RZ, Doyle JJ, Crandall KA, Egan AN (2018) De novo transcriptome assembly of Pueraria montana var. lobata and Neustanthus phaseoloides for the development of eSSR and SNP markers: narrowing the US origin(s) of the invasive kudzu. BMC Genomics 19(1):439
He Y, Li W, Lv J, Jia Y, Wang M, Xia G (2012) Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. J Exp Bot 63:1511–1522
Heer K, Ullrich KK, Liepelt S, Rensing SA, Zhou J, Ziegenhagen B, Opgenoorth L (2016) Detection of SNPs based on transcriptome sequencing in Norway spruce (Picea abies (L.) Karst). Conserv Genet Resour 8(2):105–107
Iqbal N, Umar S, Khan NA, Khan MIR (2014) A new perspective of phytohormones in salinity tolerance: regulation of proline metabolism. Environ Exp Bot 100:34–42
Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30(5):435–458
Jin J, Zhang H, Kong L, Gao G, Luo J (2014) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:1182–1187
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Toshiaki T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484
Kawaguchi R, Girke T, Bray EA, Bailey-Serres J (2004) Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J 38(5):823–839
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):25–34
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323
Li M, Zhao M, Wu H, Wu W, Xu Y (2013) Cloning, characterization and functional analysis of two type 1 diacylglycerol acyltransferases (DGAT1 s) from Tetraena mongolica. J Integr Plant Biol 55(6):490–503
Li S, Fan C, Li Y, Zhang J, Sun J, Chen Y, Tian C, Su X, Lu M, Liang C, Hu Z (2016) Effects of drought and salt-stresses on gene expression in Caragana korshinskii seedlings revealed by RNA-seq. BMC Genomics 17(1):200
Li K, Xing C, Yao Z, Huang XS (2017) PbrMYB21, a novel MYB protein of Pyrus betulaefolia, functions in drought tolerance and modulates polyamine levels by regulating arginine decarboxylase gene. Plant Biotech J 15:1186–1203
Li N, Zheng YQ, Ding HM, Li HP, Peng HZ (2018) Development and validation of SSR markers based on transcriptome sequencing of Casuarina equisetifolia. Tree 32(1):41–49
Liska AJ, Shevchenko A, Pick U, Katz A (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136(1):2806–2817
Liu GH, Zhou SQ, Thang L, Ren L (1993) Study on the biological characteristics and the endangering factors of the Tetraena mongolica. J Inner Mong For Coll 2:33–39
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△CT method. Methods 25(4):402–408
Long Y, Zhang J, Tian X, Wu S, Zhang Q, Zhang J, Zhang J, Dang Z, Pei X (2014) De novo assembly of the desert tree Haloxylon ammodendron (C.A. Mey.) based on RNA-Seq data provides insight into drought response, gene discovery and marker identification. BMC Genomics 15(1):1111
Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324(5930):1064–1068
Ma Q, Yue L, Zhang J, Wu G, Bao A, Wang S (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32(1):4–13
Ma X, Wang P, Zhou S, Sun Y, Liu N, Li X, Hou Y (2015) De novo transcriptome sequencing and comprehensive analysis of the drought-responsive genes in the desert plant Cynanchum komarovii. BMC Genomics 16:753
Ma Q, Hu J, Zhou X, Yuan H, Kumar T, Luan S, Wang S (2017) ZxAKT1 is essential for K + uptake and K +/Na + homeostasis in the succulent xerophyte Zygophyllum xanthoxylum. Plant J 90(1):48–60
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297–1303
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628
Mudado MA, Ortega JM (2006) A picture of gene sampling/expression in model organisms using ESTs and KOG proteins. Genet Mol Res 5(1):242–253
Naser V, Shani E (2016) Auxin response under osmotic stress. Plant Mol Biol 91:661–672
Pan Y, Niu M, Liang J, Lin E, Tong Z, Zhang J (2017) Identification of heat-responsive miRNAs to reveal the miRNA mediated regulatory network of heat stress response in Betula luminifera. Trees 31(5):1635–1652
Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652
Rossia L, Borghi M, Francini A, Lin X, Xie D, Sebastiani L (2016) Salt stress induces differential regulation of the phenylpropanoid pathway in Olea europaea cultivars Frantoio (salt-tolerant) and Leccino (salt-sensitive). J Plant Phys 204:8–15
Sakuraba Y, Kim YS, Han SH, Lee BD, Paek NC (2015) The Arabidopsis transcription factor NAC016 promotes drought stress responses by repressing AREB1 transcription through a trifurcate feed-forward regulatory loop involving NAP. Plant Cell 27:1771–1787
Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828
Seo PJ, Xiang F, Qiao M, Park JY, Lee YN, Kim SG, Lee YH, Park WJ, Park CM (2009) The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol 151:275–289
Shi S, Wang Y, Zhou H, Zhou J (2012) Comparative analysis of water related parameters and photosynthetic characteristics in the endangered plant Tetraena mongolica Maxim. and the closely related Zygophyllum xanthoxylon (Bunge) Maxim. Acta Ecol Sinica 32(4):1163–1173
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221–227
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6(5):410–417
Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MH, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong EL, Cutler S, Zhu JK, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335(6064):85–88
Strickler SR, Bombarely A, Mueller LA (2012) Designing a transcriptome next-generation sequencing project for a nonmodel plant species. Am J Bot 99:257–266
Tang S, Ding L, Zhai H, Qin N, Duan H (2012) Four new triterpenes from the endemic relict shrub Tetraena mongolica. J Asian Nat Prod Res 14(1):838–843
Tarazona S, Garcia-Alcalde F, Dopazo J, Ferrer A, Conesa A (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21(12):2213–2223
Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress1 promoter. Plant Cell 16:2481–2498
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):research0034.1–research0034.11
Varshney RK, Chabane K, Hendre PS, Aggarwal RK, Graner A (2007) Comparative assessment of EST-SSR, EST-SNP and AFLP markers for evaluation of genetic diversity and conservation of genetic resources using wild, cultivated and elite barleys. Plant Sci 173:638–649
Wang G (2005) The western Ordos plateau as a biodiversity center of relic shrubs in arid areas of China. Biodivers Conserv 14(13):3187–3200
Wang Y, Ma H, Zheng R (2000) Studies on the reproductive characteristics of Tetraena mongolica Maxim. Acta Botanica Boreal Occident Sinica 20(4):661–665
Wang G, Lin Q, Xu Y (2007) Tetraena mongolica Maxim can accumulate large amounts of triacylglycerol in phloem cells and xylem parenchyma of stems. Phytochemistry 68(15):2112–2117
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63
Wang L, Du H, Li T, Wuyun T (2017) De novo transcriptome sequencing and identification of genes related to salt stress in Eucommia ulmoides Oliver. Trees 32(1):1–13
Wu Y, Deng Z, Lai J, Zhang Y, Yang C, Yin B, Zhao Q, Zhang L, Li Y, Yang C, Xie Q (2009) Dual function of Arabidopsis ATAF1 in abiotic and biotic stress responses. Cell Res 19:1279–1290
Wu H, Zhang Z, Wang J, Oh DH, Dassanayake M, Liu B, Huang Q, Sun H, Xia R, Wu Y, Wang Y, Yang Z, Liu Y, Zhang W, Zhang H, Chu J, Yan C, Fang S, Zhang J, Wang Y, Zhang F, Wang G, Lee SY, Cheeseman JM, Yang B, Li B, Min J, Yang L, Wang J, Chu C, Chen S, Bohnert HJ, Zhu J, Wang X, Xie Q (2012) Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci USA 109(30):12219–12224
Wu Z, Raven PH, Hong D (2013) Flora of China. Science Press, Beijing
Xu Q, Jiang C, Liu S, Guo Q (2003) Study on pollination ecology of endangered plant Tetraena mongolica population. For Res 16(4):391–397
Xu XJ, Feng JC, Lü SY, Lohrey GT, An HL, Zhou YJ, Jenks MA (2014) Leaf cuticular lipids on the Shandong and Yukon ecotypes of saltwater cress, Eutrema salsugineum, and their response to water deficiency and impact on cuticle permeability. Physiol Plantarum 151:446–458
Xu XJ, Xiao L, Feng JH, Chen NM, Chen Y, Song B, Xue K, Shi S, Zhou YJ, Jenks MA (2016) Cuticle lipids on heteromorphic leaves of Populus euphratica Oliv. growing in riparian habitats differing in available soil moisture. Physiol Plantarum 158:318–330
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297
Zhang Y, Yang C (2000) Comparative analysis of genetic diversity in the endangered shrub Tetraena mongolica and its related congener Zygophyllum xanthoxylon. Acta Phytoecologica Sinica 24(4):425–429
Zhang J, Li X, He Z, Zhao X, Wang Q, Zhou B, Yu D, Huang X, Tang D, Guo X, Liu X (2013) Molecular character of a phosphatase 2C (PP2C) gene relation to stress tolerance in Arabidopsis thaliana. Mol Biol Rep 40(3):2633–2644
Zhu J (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4(5):401–406
Zhu J (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zhu G, Li H, Zhao L, Man L, Liu Q (2016) Mapping the ecological dimensions and potential distributions of endangered relic shrubs in western Ordos biodiversity center. Sci Rep 6:26268–26276
Acknowledgements
This research was supported by the National Natural Science Foundation of China (31470392, 31570407), the First Class University and Discipline Construction Project of Minzu University of China (Yldxxk201819).
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XX designed the experiments. NC performed the experiments, data analysis, and drafted the manuscript. JF helped conceive the study. BS and JH helped analyze data. ST helped draft the manuscript. YZ and SS helped in design and coordination. All authors read and approved the final manuscript.
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T mongolica is endemic to the western part of Inner Mongolia and Ningxia, Gansu province and also subjected as nationally endangered in China. Before collecting the seeds, an oral permission was obtained from the local management of forestry after applying with introduction letters from College of Life and Environmental Sciences, Minzu University of China.
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Chen, N., Feng, J., Song, B. et al. De novo transcriptome sequencing and identification of genes related to salt and PEG stress in Tetraena mongolica Maxim. Trees 33, 1639–1656 (2019). https://doi.org/10.1007/s00468-019-01886-7
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DOI: https://doi.org/10.1007/s00468-019-01886-7