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De novo transcriptome analysis for exploration of genes responding to salinity in a halophyte New Zealand spinach (Tetragonia tetragonioides)

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Abstract

New Zealand spinach (Tetragonia tetragonioides) is a coastal plant species with a variety of medicinal uses in Korea. Due to its salt-tolerant capabilities, land reclamation using coastal plants such as Tetragonia have been widely employed. So far, the information about the dynamics or differentially expressed genes related to salt response in New Zealand spinach (NZS) is scarce. We analyzed the expressed sequence tags of the seawater-treated NZS, to identify key genes and pathways involved in salt tolerance. Our results indicated that the salt responsive DEGs were related to ion transport, signal transduction and secondary metabolite synthesis. Further analysis of the transcriptome profile of NZS subjected to seawater treatment highlighted the roles in scavenging and abscisic acid signal transduction. The DEGs, regulating pectin remodeling and ROS scavenging may be the key genes for NZS to adapt to salinity environment. Furthermore, genes such as senescence-associated genes (SAGs) that are highly upregulated in glycophytes during salt stress were downregulated in NZS. Similarly, during abiotic stresses the transcription of genes involved in photosynthesis is severely reduced, but the transcripts of light responsive factors in NZS were slightly downregulated, showing the efficiency of the salt regulation mechanism in NZS. This study represents the first large-scale transcriptome analysis of New Zealand spinach. Elucidating the salt tolerant properties of halophytes can provide novel findings to enhance the salt sensitive plants. Our findings could further help the understanding of the stress tolerance mechanisms in plants in general and New Zealand Spinach can be used as a halophytic model in stress-tolerance studies.

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The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

Abbreviations

BLAST:

Basic Local Alignment Search Tool

COG:

Clusters of Orthologous genes

DEGs:

Differentially Expressed Genes

EST:

Expressed Sequence Tag

GO:

Gene Ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes database

NCBI:

National Center for Biotechnology Information

RPKM:

Reads Per Kilobase of transcript per Million mapped reads

References

  • Abbasi-Vineh MA, Sabet MS, Karimzadeh G (2021) Identification and functional analysis of two purple acid phosphatases AtPAP17 and AtPAP26 involved in salt tolerance in Arabidopsis thaliana plant. Front Plant Sci. https://doi.org/10.3389/fpls.2020.618716

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    Article  CAS  Google Scholar 

  • Ayarpadikannan S, Chung E, Cho CW, So HA, Kim SO, Jeon JM, Kwak MH, Lee SW, Lee JH (2012) Exploration for the salt stress tolerance genes from a salt-treated halophyte, Suaeda asparagoides. Plant Cell Rep 31:35–48

    Article  CAS  Google Scholar 

  • Baba SA, Vishwakarma RA, Ashraf N (2017) Functional characterization of CsBGlu12, a β-Glucosidase from Crocus sativus, provides insights into its role in abiotic stress through accumulation of antioxidant flavonols. J Biol Chem 292:4700–4713

    Article  CAS  Google Scholar 

  • Baisakh N, Subudhi PK, Varadwaj P (2008) Primary responses to salt stress in a halophyte, smooth cordgrass (Spartina alterniflora Loisel.). Funct Integr Genomics 8:287–300

    Article  CAS  Google Scholar 

  • Baruah A, Simková K, Apel K, Laloi C (2009) Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development. Plant Mol Biol 70:547–563

    Article  CAS  Google Scholar 

  • Carstensen A, Herdean A, Schmidt SB, Sharma A, Spetea C, Pribil M, Husted S (2018) The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiol 177:271–284

    Article  CAS  Google Scholar 

  • Che-Othman MH, Millar AH, Taylor NL (2017) Connecting salt stress signaling pathways with salinity-induced changes in mitochondrial metabolic processes in C3 plants. Plant, Cell Environ 40:2875–2905

    Article  CAS  Google Scholar 

  • Chinnusamy V, Jagendorf A, Zhu J-K (2005) Understanding and improving salt tolerance in plants. Crop Sci 45:437–448

    Article  CAS  Google Scholar 

  • Du Y-T, Zhao M-J, Wang C-T, Gao Y, Wang Y-X, Liu Y-W, Chen M, Chen J, Zhou Y-B, Xu Z-S (2018) Identification and characterization of GmMYB118 responses to drought and salt stress. BMC Plant Biol 18:1–18

    Article  Google Scholar 

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    Article  CAS  Google Scholar 

  • Guo R, Xu X, Carole B, Li X, Gao M, Zheng Y, Wang X (2013) Genome-wide identification, evolutionary and expression analysis of the aspartic protease gene superfamily in grape. BMC Genomics 14:554

    Article  CAS  Google Scholar 

  • Guo J, Huang Z, Sun J, Cui X, Liu Y (2021) Research progress and future development trends in medicinal plant transcriptomics. Front Plant Sci. https://doi.org/10.3389/fpls.2021.691838

    Article  Google Scholar 

  • Hajlaoui H, Ayeb NE, Garrec JP, Denden M (2010) Differential effects of salt stress on osmotic adjustment and solutes allocation on the basis of root and leaf tissue senescence of two silage maize (Zea mays L.) varieties. Ind Crops Prod 31:122–130

    Article  CAS  Google Scholar 

  • Hara M, Tokunaga K, Kuboi T (2008) Isolation of a drought-responsive alkaline galactosidase gene from New Zealand spinach. Plant Biotechnol 25:497–501

    Article  CAS  Google Scholar 

  • Hsu PK, Dubeaux G, Takahashi Y, Schroeder JI (2021) Signaling mechanisms in abscisic acid-mediated stomatal closure. Plant J 105:307–321

    Article  CAS  Google Scholar 

  • Hu M, Shi Z, Zhang Z, Zhang Y, Li H (2012) Effects of exogenous glucose on seed germination and antioxidant capacity in wheat seedlings under salt stress. Plant Growth Regul 68:177–188

    Article  CAS  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44–57

    Article  CAS  Google Scholar 

  • Huang X, Yang L, Jin Y, Lin J, Liu F (2017) Generation, annotation, and analysis of a large-scale expressed sequence tag library from Arabidopsis pumila to explore salt-responsive genes. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00955

    Article  Google Scholar 

  • Jaworska G (2005) Nitrates, nitrites, and oxalates in products of spinach and New Zealand spinach: effect of technological measures and storage time on the level of nitrates, nitrites, and oxalates in frozen and canned products of spinach and New Zealand spinach. Food Chem 93:395–401

    Article  CAS  Google Scholar 

  • Jiang H, Wong WH (2008) SeqMap: mapping massive amount of oligonucleotides to the genome. Bioinformatics (oxford, England) 24:2395–2396

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  Google Scholar 

  • Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7:e1002243

    Article  CAS  Google Scholar 

  • Li J, Sun X, Yu G, Jia C, Liu J, Pan H (2014) Generation and analysis of expressed sequence tags (ESTs) from halophyte Atriplex canescens to explore salt-responsive related genes. Int J Mol Sci 15:11172–11189

    Article  Google Scholar 

  • Liu H, Ma Y, Chen N, Guo S, Liu H, Guo X, Chong K, Xu Y (2014) Overexpression of stress-inducible OsBURP16, the β subunit of polygalacturonase 1, decreases pectin content and cell adhesion and increases abiotic stress sensitivity in rice. Plant, Cell Environ 37:1144–1158

    Article  CAS  Google Scholar 

  • Liu L, Xia W, Li H, Zeng H, Wei B, Han S, Yin C (2018) Salinity inhibits rice seed germination by reducing α-amylase activity via decreased bioactive gibberellin content. Front Plant Sci 9:275

    Article  Google Scholar 

  • Liu P, Zhang S, Zhou B, Luo X, Zhou XF, Cai B, Jin YH, Niu D, Lin J, Cao X, Jin JB (2019) The histone H3K4 demethylase JMJ16 represses leaf senescence in Arabidopsis. Plant Cell 31:430–443

    Article  CAS  Google Scholar 

  • Lutts S, Lefèvre I (2015) How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas? Ann Bot 115:509–528

    Article  CAS  Google Scholar 

  • Ma C, Wang Y, Gu D, Nan J, Chen S, Li H (2017) Overexpression of S-Adenosyl-l-Methionine Synthetase 2 from sugar beet M14 increased Arabidopsis tolerance to salt and oxidative stress. Int J Mol Sci 18:847

    Article  Google Scholar 

  • Matsuo M, Oelmüller R (2015) Redox responsive transcription factor1 is involved in age-dependent and systemic stress signaling. Plant Signal Behav 10:e1051279

    Article  Google Scholar 

  • Mittelheuser CJ, Van Steveninck RF (1969) Stomatal closure and inhibition of transpiration induced by (RS)-abscisic acid. Nature 221:281–282

    Article  CAS  Google Scholar 

  • Morozova O, Hirst M, Marra MA (2009) Applications of new sequencing technologies for transcriptome analysis. Annu Rev Genomics Hum Genet 10:135–151

    Article  CAS  Google Scholar 

  • Negrão S, Schmöckel S, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11

    Article  Google Scholar 

  • Noh B, Lee S-H, Kim H-J, Yi G, Shin E-A, Lee M, Jung K-J, Doyle MR, Amasino RM, Noh Y-S (2004) Divergent roles of a pair of homologous Jumonji/zinc-finger–class transcription factor proteins in the regulation of Arabidopsis flowering time. Plant Cell 16:2601–2613

    Article  CAS  Google Scholar 

  • Pandian BA, Sathishraj R, Djanaguiraman M, Prasad PV, Jugulam M (2020) Role of cytochrome P450 enzymes in plant stress response. Antioxidants 9:454

    Article  CAS  Google Scholar 

  • Rasouli F, Kiani-Pouya A, Shabala L, Li L, Tahir A, Yu M, Hedrich R, Chen Z, Wilson R, Zhang H, Shabala S (2021) Salinity effects on guard cell proteome in Chenopodium quinoa. Int J Mol Sci 22:428

    Article  CAS  Google Scholar 

  • Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124

    Article  CAS  Google Scholar 

  • Sakuraba Y, Kim D, Paek N-C (2018) Salt treatments and induction of senescence. Plant senescence: methods and protocols. Springer, NY, pp 141–149

    Chapter  Google Scholar 

  • Salzman J, Jiang H, Wong WH (2011) Statistical modeling of RNA-Seq Data. Stat Sci 26(62–83):22

    Google Scholar 

  • Schulz MH, Zerbino DR, Vingron M, Birney E (2012) Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics 28:1086–1092

    Article  CAS  Google Scholar 

  • Seki M, Narusaka M, Kamiya A, Ishida J, Satou M, Sakurai T, Nakajima M, Enju A, Akiyama K, Oono Y (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296:141–145

    Article  Google Scholar 

  • Shen Y, Conde e Silva N, Audonnet L, Servet C, Wei W, Zhou D-X (2014) Over-expression of histone H3K4 demethylase gene JMJ15 enhances salt tolerance in Arabidopsis. Front Plant Sci 5:290

    Article  Google Scholar 

  • Shi F, Dong Y, Zhang Y, Yang X, Qiu D (2017) Overexpression of the PeaT1 elicitor gene from Alternaria tenuissima improves drought tolerance in rice plants via interaction with a myo-inositol oxygenase. Front Plant Sci 8:970

    Article  Google Scholar 

  • Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123

    Article  CAS  Google Scholar 

  • Sun Z, Wang X, Qiao K, Fan S, Ma Q (2021) Genome-wide analysis of JMJ-C histone demethylase family involved in salt-tolerance in Gossypium hirsutum L. Plant Physiol Biochem 158:420–433

    Article  CAS  Google Scholar 

  • Tang Y, Bao X, Zhi Y, Wu Q, Guo Y, Yin X, Zeng L, Li J, Zhang J, He W (2019) Overexpression of a MYB family gene, OsMYB6, increases drought and salinity stress tolerance in transgenic rice. Front Plant Sci 10:168

    Article  Google Scholar 

  • Van Nguyen T, Kim J-I, Park C-R, Chung M-S, Kim CS (2021) Increased cysteine accumulation is essential for salt stress tolerance in Arabidopsis Halotolerance 2-Like (AHL)-Overexpressing transgenic plants. J Plant Biol 64:475–485

    Article  Google Scholar 

  • Voelckel C, Gruenheit N, Lockhart P (2017) Evolutionary transcriptomics and proteomics: insight into plant adaptation. Trends Plant Sci 22:462–471

    Article  CAS  Google Scholar 

  • Wai AH, Naing AH, Lee D-J, Kim CK, Chung M-Y (2020) Molecular genetic approaches for enhancing stress tolerance and fruit quality of tomato. Plant Biotechnol Rep 14:515–537

    Article  Google Scholar 

  • Wang Z-L, Li P-H, Fredricksen M, Gong Z-Z, Kim C, Zhang C, Bohnert HJ, Zhu J-K, Bressan RA, Hasegawa PM (2004) Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerance. Plant Sci 166:609–616

    Article  CAS  Google Scholar 

  • Wang H, Ni D, Shen J, Deng S, Xuan H, Wang C, Xu J, Zhou L, Guo N, Zhao J (2022) Genome-wide identification of the AP2/ERF gene family and functional analysis of GmAP2/ERF144 for drought tolerance in soybean. Front Plant Sci. https://doi.org/10.3389/fpls.2022.848766

    Article  Google Scholar 

  • Wilson C, Lesch SM, Grieve CM (2000) Growth stage modulates salinity tolerance of New Zealand spinach (Tetragonia tetragonioides, Pall.) and red orach (Atriplex hortensis L.). Ann Bot 85:501–509

    Article  CAS  Google Scholar 

  • Winter G, Todd CD, Trovato M, Forlani G, Funck D (2015) Physiological implications of arginine metabolism in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00534

    Article  Google Scholar 

  • Wong C, Li Y, Whitty B, Diaz-Camino C, Akhter S, Brandle J, Golding G, Weretilnyk E, Moffatt B, Griffith M (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol Biol 58:561–574

    Article  CAS  Google Scholar 

  • Wormit A, Usadel B (2018) The multifaceted role of pectin methylesterase inhibitors (PMEIs). Int J Mol Sci 19:2878

    Article  Google Scholar 

  • Yan J, He H, Fang L, Zhang A (2018) Pectin methylesterase31 positively regulates salt stress tolerance in Arabidopsis. Biochem Biophys Res Commun 496:497–501

    Article  CAS  Google Scholar 

  • Yang J, Yang J, Zhao L, Gu L, Wu F, Tian W, Sun Y, Zhang S, Su H, Wang L (2021) Ectopic expression of a Malus hupehensis Rehd myo- inositol oxygenase gene (MhMIOX2) enhances tolerance to salt stress. Sci Hortic 281:109898

    Article  CAS  Google Scholar 

  • Yousif BS, Nguyen NT, Fukuda Y, Hakata H, Okamoto Y, Masaoka Y, Saneoka H (2010) Effect of salinity on growth, mineral composition, photosynthesis and water relations of two vegetable crops; New Zealand spinach (Tetragonia tetragonioides) and water spinach (Ipomoea aquatica). Int J Agric Biol 12:211–216

    CAS  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  CAS  Google Scholar 

  • Zhang L, Becker D (2015) Connecting proline metabolism and signaling pathways in plant senescence. Front Plant Sci 6:552

    Article  Google Scholar 

  • Zhang J, Zhang Y, Du Y, Chen S, Tang H (2011) Dynamic metabonomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 10:1904–1914

    Article  CAS  Google Scholar 

  • Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67

    Article  Google Scholar 

  • Zhen-Hua Z, Qiang L, Hai-Xing S, Xiang-Min R, Ismail AM (2012) Responses of different rice (Oryza sativa L.) genotypes to salt stress and relation to carbohydrate metabolism and chlorophyll content. Afr J Agric Res 7:19–27

    Google Scholar 

  • Zhu J-K (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by Basic Science Research Program (NRF-2020R1A2C1015119) funded by National Research Foundation (NRF), Ministry of Science and ICT, Republic of Korea.

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Basic Science research Program, National Research Foundation (NRF), Ministry of Science and ICT, Republic of Korea, NRF-2020R1A2C1015119, Geung-Joo Lee.

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Kaur, C., Kanth, B., Lee, K. et al. De novo transcriptome analysis for exploration of genes responding to salinity in a halophyte New Zealand spinach (Tetragonia tetragonioides). Plant Biotechnol Rep 16, 741–755 (2022). https://doi.org/10.1007/s11816-022-00800-x

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