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Transcriptome profiling of mild-salt responses in Lycium ruthenicum early seedlings to reveal salinity-adaptive strategies

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Abstract

The traditional Chinese desert shrub Lycium ruthenicum is widely distributed in arid environments such as north-west China, exhibiting ideal salt tolerance to cope with soil desertification, salinity, and alkalinity. However, the salt-tolerance mechanism of L. ruthenicum, especially of its young seedlings at early vegetative stages, remains largely unknown. In the present study, we collected whole-seedling samples from Lycium ruthenicum at a-pair-leaf stage with and without a mild salt (75 mM sodium chloride) treatment, and then performed transcriptome profiling to compare their gene expression patterns. The de novo assembly achieved 94,651 unigenes with 55,156 annotated. Among them, 199 differentially expressed genes (DEGs) were identified between salt-treated seedlings and control, with 41 up-regulated and 158 down-regulated. These DEGs were highly enriched into gene ontology (GO) classifications ‘metabolic process’ and ‘catalytic activity’, into Clusters of Orthologous Groups (COG) function classifications ‘translation, ribosomal structure and biogenesis’ and ‘energy production and conversion’, and into Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways ‘ribosome’ and ‘oxidative phosphorylation’. Specifically, genes involved in energy metabolism (oxidative phosphorylation) and related energy-consuming metabolisms, including ribosome-associated biogenesis and biosynthesis of organic nitrogen-derived compatible solutes (i.e., arginine and proline), were generally down-regulated. Specific genes involved in abscisic acid (ABA) biosynthesis and signaling pathway were simultaneously up-regulated. Changes in the transcript levels of salt-responsive DEGs selected from the transcriptomic profiling were further validated by real-time quantitative polymerase chain reaction (RT-qPCR) analysis. Based on these results, salinity-adaptive strategies for the L. ruthenicum early seedlings are discussed.

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Abbreviations

AASCL:

Amino acid solute carrier like

ABA:

Abscisic acid

BP:

Biological process

CC:

Cellular component

COG:

Clusters of Orthologous Groups

DEG:

Differentially expressed gene

EDTA:

Ethylenediaminetetraacetic acid

EF:

Elongation factor

ELISA:

Enzyme-linked immunosorbent assay

FPKM:

Fragments per kb per million fragments

GA:

Gibberellic acid

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

GDH:

Glutamate dehydrogenase

GO:

Gene ontology

GS:

Glutamine synthetase

JA:

Jasmonate

KEGG:

Kyoto Encyclopedia of Genes and Genomes

KOG:

EuKaryotic Orthologous Groups

MAPKKK:

Mitogen-activated protein kinase kinase kinase

MAPKs:

Mitogen-activated protein kinases

MF:

Molecular function

NADH-UQ:

NADH-ubiquinone oxidoreductase

NCED:

9-Cis-epoxycarotenoid dioxygenase

NDPK:

Nucleoside-diphosphate kinase

NR:

Non-redundant

ODC:

Ornithine decarboxylase

Pfm:

Protein family

PP2C:

Protein phosphatase 2C

RT-qPCR:

Real-time quantitative PCR

ROS:

Reactive oxygen species

RPL:

Ribosome protein large unit (60S)

RPS:

Ribosome protein small unit (40S

References

  • Abid MA, Liang C, Malik W, Meng Z, Tao Z, Meng Z, Ashraf J, Guo S, Zhang R (2018) Cascades of ionic and molecular networks involved in expression of genes underpin salinity tolerance in cotton. J Plant Growth Regul 37:668–679

    Article  CAS  Google Scholar 

  • Ahammed GJ, Li X, Zhang G, Zhang H, Shi J, Pan C, Yu J, Shi K (2018) Tomato photorespiratory glycolate-oxidase-derived H2O2 production contributes to basal defense against Pseudomonas syringae. Plant Cell Environ 41:1126–1138

    Article  CAS  PubMed  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:106

    Article  CAS  Google Scholar 

  • Annunziata MG, Ciarmiello LF, Woodrow P, Maximova E, Fuggi A, Carillo P (2017) Durum wheat roots adapt to salinity remodeling the cellular content of nitrogen metabolites and sucrose. Front Plant Sci 7:2035

    Article  PubMed  PubMed Central  Google Scholar 

  • Asrar H, Hussain T, Gul B, Khan MA, Nielsen BL (2018) Differential protein expression reveals salt tolerance mechanisms of Desmostachya bipinnata at moderate and high levels of salinity. Funct Plant Biol 45:793–812

    Article  CAS  PubMed  Google Scholar 

  • Bai J, Qin Y, Liu J, Wang Y, Sa R, Zhang N, Jia R (2017) Proteomic response of oat leaves to long-term salinity stress. Environ Sci Pollut Res 24:3387–3399

    Article  CAS  Google Scholar 

  • Baranova YN, Akanov EN, Gulevich AA, Kurenina LV, Danilova SA, Khaliluev MR (2014) Dark respiration rate of transgenic tomato plants expressing FeSOD1 gene under chloride and sulfate salinity. Russ Agr Sci 1:14–17

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple hypothesis testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Bhattacharjee A, Sharma R, Jain M (2017) Over-expression of OsHOX24 confers enhanced susceptibility to abiotic stresses in transgenic rice via modulating stress-responsive gene expression. Front Plant Sci 8:628

    Article  PubMed  PubMed Central  Google Scholar 

  • Bottino MC, Rosario S, Grativol C, Thiebaut F, Rojas CA, Farrineli L, Hemerly AS, Gomes Ferreira PC (2013) High-throughput sequencing of small RNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS ONE 8(3):e59423

    Article  Google Scholar 

  • Brugière N, Zhang WJ, Xu QZ, Scolaro EJ, Lu C, Kahsay RY, Kise R, Trecker L, Williams RW, Hakimi S, Niu XP, Lafitte R, Habben JE (2017) Overexpression of RING domain E3 ligase ZmXerico1 confers drought tolerance through regulation of ABA homeostasis. Plant Physiol 175:1350–1369

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chandrasekaran U, Xu W, Liu AZ (2014) Transcriptome profiling identifies ABA mediated regulatory changes towards storage filling in developing seeds of castor bean (Ricinus communis L.). Cell Biosci 4:33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen H, Pu L, Cao J, Ren X (2008) Current research state and exploitation of Lycium ruthenicum Murr. Heilongjiang Agric Sci 5:155–157

    Google Scholar 

  • Chen HK, Feng Y, Wang LN, Yonezawa TC, Crabbe MJ, Zhang X, Zhong Y, (2015) Transcriptome profiling of the UV-B stress response in the desert shrub Lycium ruthenicum. Mol Biol Rep 42:639–649

  • Chen JH, Zhang DZ, Zhang C, Xu ML, Yin WL (2017) Physiological characterization, transcriptomic profiling, and microsatellite marker mining of Lycium ruthenicum. J Zhejiang Univ-Sci B 18(11):1002–1021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Z, Dong K, Ge P, Bian Y, Dong L, Deng X, Li X, Yan Y (2015) Identification of leaf proteins differentially accumulated between wheat cultivars distinct in their levels of drought tolerance. PLoS ONE 10(5):e0125302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choi S, Lee S, Na Y, Jeung S, Kim SY (2017) Arabidopsis MAP3K16 and other salt-inducible MAP3Ks regulate ABA response redundantly. Mol Cells 40(3):230–242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Das P, Majumder AL (2019) Transcriptome analysis of grapevine under salinity and identification of key genes responsible for salt tolerance. Funct Integr Genom 19:61–73

    Article  CAS  Google Scholar 

  • de Hoon MJL, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454

    Article  PubMed  CAS  Google Scholar 

  • de Oliveira TM, Cidade LC, Gesteira AS, Coelho Filho MA, Soares Filho WS, Costa CMG (2011) Analysis of the NAC transcription factor gene family in citrus reveals a novel member involved in multiple abiotic stress responses. Tree Genet Genom 7:1123–1134

    Article  Google Scholar 

  • Dixit A, Tomar P, Vaine E, Abdullah H, Hazen S, Dhankher OP (2018) A stress-associated protein, AtSAP13, from Arabidopsis thaliana provides tolerance to multiple abiotic stresses. Plant Cell Environ 41:1171–1185

    Article  CAS  PubMed  Google Scholar 

  • Dong JZ, Yang JJ, Wang Y (2008) Resources of Lycium species and related research progress. China Mater Med 33:2020–2027

    Google Scholar 

  • Duan M, Chang SX (2017) Nitrogen fertilization improves the growth of lodgepole pine and white spruce seedlings under low salt stress through enhancing photosynthesis and plant nutrition. Forest Ecol Manag 404:197–204

    Article  Google Scholar 

  • Duan M, Feng HL, Wang LY, Li D, Meng QW (2012) Overexpression of thylakoidal ascorbate peroxidase shows enhanced resistance to chilling stress in tomato. J Plant Physiol 169:867–877

    Article  CAS  PubMed  Google Scholar 

  • Fan L, Wang G, Hu W, Pantha P, Tran KN, Zhang H, An L, Dassanayake M, Qiu QS (2018) Transcriptomic view of survival during early seedling growth of the extremophyte Haloxylon ammodendron. Plant Physiol Biochem 132:475–489

    Article  CAS  PubMed  Google Scholar 

  • Fan ZL, Ma YJ, Ma YJ (2001) Salinized soils and their improvement and utilization in west China. Arid Zone Res 18(3):1–6 (in Chinese)

    CAS  Google Scholar 

  • Gerszberg A, Hnatuszko-Konka K (2017) Tomato tolerance to abiotic stress: a review of most often engineered target sequences. Plant Growth Regul 83:175–198

    Article  CAS  Google Scholar 

  • Gharbi E, Martínez J, Benahmed H, Fauconnier M, Lutts S, Quinet M (2016) Salicylic acid differently impacts ethylene and polyamine synthesis in the glycophyte Solanum lycopersicum and the wild-related halophyte Solanum chilense exposed to mild salt stress. Physiol Plant 158:152–167

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han DH, Li SJ, Wang EJ, Meng HM, Chen Y, Zhang Y (2014) Effect of exogenous calcium on seed germination and seedling physiological characteristics of Lycium ruthenium. China J Chin Mater Med 39:34–39

    Google Scholar 

  • Horváth E, Csiszár J, Gallé Á, Poór P, Szepesi Á, Tari I (2015) Hardening with salicylic acid induces concentration-dependent changes in abscisic acid biosynthesis of tomato under salt stress. J Plant Physiol 183:54–63

    Article  PubMed  CAS  Google Scholar 

  • Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiol 77:483–485

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang K, Moe-Lange J, Hennet L, Feldman LJ (2016) Salt stress affects the redox status of Arabidopsis root meristems. Front Plant Sci 7:81

    PubMed  PubMed Central  Google Scholar 

  • Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20(9):586–594

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36(Database issue):D480–D484

    CAS  PubMed  Google Scholar 

  • Kang M, Lee S, Abdelmageed H, Reichert A, Lee H-K, Fokar M, Mysore KS, Allen RD (2017) Arabidopsis stress associated protein 9 mediates biotic and abiotic stress responsive ABA signaling via the proteasome pathway. Plant Cell Environ 40:702–716

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Choi H, Ryu HJ, Park JH, Kim MD, Kim SY (2004) ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol 136:3639–3648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kissoudis C, Sunarti S, van de Wiel C, Visser R, van der Linden CG, Bai YL (2016) Responses to combined abiotic and biotic stress in tomato are governed by stress intensity and resistance mechanism. J Exp Bot 67:5119–5132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lechner E, Leonhardt N, Eisler H, Parmentier Y, Alioua M, Jacquet H, Leung J, Genschik P (2011) MATH/BTB CRL3 receptors target the homeodomain-leucine zipper ATHB6 to modulate abscisic acid signaling. Dev Cell 21:1116–1128

    Article  CAS  PubMed  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323

    Article  CAS  Google Scholar 

  • Liu D, Han C, Deng X, Liu Y, Liu N, Yan Y (2019) Integrated physiological and proteomic analysis of embryo and endosperm reveals central salt stress response proteins during seed germination of winter wheat cultivar Zhengmai 366. BMC Plant Biol 19:29

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lou D, Wang H, Liang G, Yu D (2017) OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Front Plant Sci 8:993

    Article  PubMed  PubMed Central  Google Scholar 

  • Loulakakis KA, Roubelakis-Angeiakis KA (1996) The seven NAD(H)-glutamate dehydrogenase isoenzymes exhibit similar anabolic and catabolic activities. Physiol Plant 96:29–35

    Article  CAS  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ludwig A, Tenhaken R (2001) Suppression of the ribosomal L2 gene reveals a novel mechanism for stress adaptation in soybean. Planta 212:792–798

    Article  CAS  PubMed  Google Scholar 

  • Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793

    Article  CAS  PubMed  Google Scholar 

  • Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuoka D, Soga K, Yasufuku T, Nanmori T (2018) Control of plant growth and development by overexpressing MAP3K17, an ABA-inducible MAP3K, in Arabidopsis. Plant Biotechnol 35:171–176

    Article  CAS  Google Scholar 

  • Moin M, Bakshi A, Saha A, Kumar MU, Reddy AR, Rao KV, Siddiq EA, Kirti PB (2016) Activation tagging in indica rice identifies ribosomal proteins as potential targets for manipulation of water-use efficiency and abiotic stress tolerance in plants. Plant Cell Environ 39:2440–2459

    Article  CAS  PubMed  Google Scholar 

  • Möller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Muchate NS, Nikalje GC, Rajurkar NS, Suprasanna P, Nikam TD (2016) Plant salt stress: adaptive responses, tolerance mechanism and bioengineering for salt tolerance. Bot Rev 82:371–406

    Article  Google Scholar 

  • Mukhopadhyay P, Reddy MK, Singla-Pareek SL, Sopory SK (2011) Transcriptional downregulation of rice rpL32 gene under abiotic stress is associated with removal of transcription factors within the promoter region. PLoS ONE 6(11):e28058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nam MH, Bang E, Kwon TY, Kim Y, Kim EH, Cho K, Park WJ, Kim B, Yoon IS (2015) Metabolite profiling of diverse rice germplasm and identification of conserved metabolic markers of rice roots in response to long-term mild salinity stress. Int J Mol Sci 16:21959–21974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsson A, Engström P, Söderman E (2004) The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis. Plant Mol Biol 55:663–677

    Article  CAS  PubMed  Google Scholar 

  • Othman AB, Ellouzi H, Planchais S, Vos DD, Faiyue B, Carol P, Abdelly C, Savouré A (2017) Phospholipases dζ1 and dζ2 have distinct roles in growth and antioxidant systems in Arabidopsis thaliana responding to salt stress. Planta 246:721–735

    Article  PubMed  CAS  Google Scholar 

  • Peng Y, Ma HQ, Chen SW (2017) De novo characterization of the Lycium ruthenicum transcriptome and analysis of its digital gene expression profiles during fruit development and ripening. Arch Biol Sci 69(1):181–190

    Article  Google Scholar 

  • Rhodes D, Rendon GA, Stewart GR (1975) The control of glutamine synthetase level in Lemna minor L. Planta 125:201–211

    Article  CAS  PubMed  Google Scholar 

  • Sales L, Ohara H, Ohkawa K, Saito T, Todoroki Y, Srilaong V, Kondo S (2017) Salt tolerance in apple seedlings is affected by an inhibitor of ABA 8’-Hydroxylase CYP707A. J Plant Growth Regul 36:643–650

    Article  CAS  Google Scholar 

  • Shin D, Koo YD, Lee J, Lee H, Baek D, Lee S, Cheon CI, Kwak SS, Lee SY, Yun DJ (2004) Athb-12, a homeobox-leucine zipper domain protein from Arabidopsis thaliana, increases salt tolerance in yeast by regulating sodium exclusion. Biochem Biophys Res Commun 323:534–540

    Article  CAS  PubMed  Google Scholar 

  • Silva N, de Souza GA, Pimenta TM, Brito F, Picoli E, Zsögön A, Ribeiro DM (2018) Salt stress inhibits germination of Stylosanthes humilis seeds through abscisic acid accumulation and associated changes in ethylene production. Plant Physiol Biochem 130:399–407

    Article  CAS  PubMed  Google Scholar 

  • Singh M, Singh VP, Prasad SM (2016) Responses of photosynthesis, nitrogen and proline metabolism to salinity stress in Solanum lycopersicum under different levels of nitrogen supplementation. Plant Physiol Biochem 109:72–83

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Sun YF, Zhang M, Wang L, Ren J, Cui MM, Wang YP, Ji K, Li P, Li Q, Chen P, Dai SJ, Duan CR, Wu Y, Leng P (2012) Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol 158:283–298

    Article  PubMed  PubMed Central  Google Scholar 

  • Szypulska E, Jankowski K, Weidner S (2017) ABA pretreatment can limit salinity-induced proteome changes in growing barley sprouts. Acta Physiol Plant 39:190

    Article  CAS  Google Scholar 

  • Tada Y, Kawano R, Komatsubara S, Nishimura H, Katsuhara M, Ozaki S, Terashima S, Yano K, Endo C, Sato M, Okamoto M, Sawada Y, Hirai MY, Kurusu T (2019) Functional screening of salt tolerance genes from a halophyte Sporobolus virginicus and transcriptomic and metabolomic analysis of salt tolerant plants expressing glycine-rich RNA-binding protein. Plant Sci 278:54–63

    Article  CAS  PubMed  Google Scholar 

  • Takahashi F, Tilbrook J, Trittermann C, Berger B, Roy SJ, Seki M, Shinozaki K, Tester M (2015) Comparison of leaf sheath transcriptome profiles with physiological traits of bread wheat cultivars under salinity stress. PLoS ONE 10(8):e0133322

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28(1):33–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian X, Wang Z, Zhang Q, Ci H, Wang P, Yu L, Jia G (2018) Genome-wide transcriptome analysis of the salt stress tolerance mechanism in Rosa chinensis. PLoS ONE 13(7):e0200938

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tian XW, Ji J, Wang G, Jin C, Guan CF, Wu DY, Li ZD (2015) Cloning and expression analysis of 9-cis-epoxycarotenoid dioxygenase gene 1 involved in fruit maturation and abiotic stress response in Lycium chinense. J Plant Growth Regul 34:465–474

    Article  CAS  Google Scholar 

  • Wang GL, Ren XQ, Liu JX, Yang F, Wang YP, Xiong AS (2019) Transcript profiling reveals an important role of cell wall remodeling and hormone signaling under salt stress in garlic. Plant Physiol Biochem 135:87–98

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Lin J, Li XG, Chang Y (2015) Genome-wide identification of pear HD-Zip gene family and expression patterns under stress induced by drought, salinity, and pathogen. Acta Physiol Plant 37:189

    Article  CAS  Google Scholar 

  • Wang L, Zhao ZY, Zhang K, Tian CY (2013) Reclamation and utilization of saline soils in arid northwestern China: a promising halophyte drip-irrigation system. Environ Sci Technol 47:5518–5519

    Article  CAS  PubMed  Google Scholar 

  • Wang LK, Feng ZX, Wang X, Wang XW, Zhang XG (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136–138

    Article  PubMed  CAS  Google Scholar 

  • Wang ZQ, Yuan YZ, Ou JQ, Lin QH, Zhang CF (2007) Glutamine synthetase and glutamate dehydrogenase contribute differentially to proline accumulation in leaves of wheat (Triticum aestivum) seedlings exposed to different salinity. J Plant Physiol 164:695–701

    Article  CAS  PubMed  Google Scholar 

  • Xue GP, Way HM, Richardson T, Drenth J, Joyce PA, McIntyre CL (2011) Overexpression of TaNAC69 leads to enhanced transcript levels of stress up-regulated genes and dehydration tolerance in bread wheat. Mol Plant 4:697–712

    Article  CAS  PubMed  Google Scholar 

  • 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(Web Server issue):W293–W297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye J, Zhang Y, Cui H, Liu J, Wu Y, Cheng Y, Xu H, Huang X, Li S, Zhou A, Zhang X, Bolund L, Chen Q, Wang J, Yang H, Fang L, Shi C (2018) WEGO 2.0: a web tool for analyzing and plotting GO annotations, 2018 update. Nucleic Acids Res 46(Web Server issue):W71–W75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Zelicourt A, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21(8):677–685

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Ni Z, Chen Q, Guo Z, Gao W, Su X, Qu Y (2016) Proteomic responses of drought-tolerant and drought-sensitive cotton varieties to drought stress. Mol Genet Genom 291:1293–1303

    Article  CAS  Google Scholar 

  • Zhao KF, Harris PJ (1992) The effects of iso-osmotic salt and water stresses on the growth of halophytes and non-halophytes. J Plant Physiol 139:761–763

    Article  CAS  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by Xinjiang Key Laboratory of Special Species Conservation and Regulatory Biology Project (Grant no. XJDX1414-2015-01) and the National Natural Science Foundations of China (Grant nos. 31371669 and 31101595). We sincerely thank Dr. Xuemin Wang (Department of Biology, University of Missouri, United States; Donald Danforth Plant Science Center, United States) for his helpful suggestions in the research and English language editing.

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Wang, H., Guo, J., Tian, Z. et al. Transcriptome profiling of mild-salt responses in Lycium ruthenicum early seedlings to reveal salinity-adaptive strategies. Acta Physiol Plant 42, 63 (2020). https://doi.org/10.1007/s11738-020-03048-6

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