Skip to main content
SpringerLink
Log in

Transcriptomic and Physiological Analyses Reveal the Dynamic Response to Salinity Stress of the Garden Asparagus (Asparagus officinalis L.)

  • Original Article
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

Soil salinity is a major abiotic stress that affects crop productivity. Garden asparagus (Asparagus officinalis L.) is a perennial plant with some salt tolerance. However, little is known about its response mechanism to salinity stress. In this study, we conducted transcriptome analysis in the leaves of A. officinalis seedlings treated with NaCl solution for 0 h, 1 h, 24 h, and 72 h using the Illumina HiSeq™ 2500 sequencing platform. Compared with the control (0 h), 1027, 3387, and 3358 differentially expressed genes (DEGs) were identified at 1 h, 24 h, and 72 h, respectively. The Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses revealed that these DEGs were highly enriched in carbon metabolism, ion transport, and reactive oxygen species (ROS) metabolism functional categories, suggesting their key positions in salinity stress responses. Moreover, k-means clustering categorized these DEGs into five kinds of expression patterns at four time points. Of these, DEGs involved in carbon metabolism, ion transport, and ROS metabolism and the groups which they belonged to were identified, which demonstrated their time-dependent response mechanisms. Overall, the transcriptome analysis shed light on the salinity stress response mechanisms in A. officinalis and provided a basis for future studies on salt-tolerance molecular improvement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Almeida DM, Margarida Oliveira M, Saibo NJM (2017) Regulation of Na+ and K+ homeostasis in plants: towards improved salt stress tolerance in crop plants. Genet Mol Biol 40:326–345

    CAS  PubMed  PubMed Central  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    CAS  PubMed  Google Scholar 

  • Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    CAS  Google Scholar 

  • Assaha DVM, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol 8:509

    PubMed  PubMed Central  Google Scholar 

  • Bernardi P, Lippe G (2019) Editorial: structure and function of F- and V-ATPases. Front Physiol 10:358

    PubMed  PubMed Central  Google Scholar 

  • Bose J, Munns R, Shabala S, Gilliham M, Pogson B, Tyerman SD (2017) Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes. J Exp Bot 68:3129–3143

    CAS  PubMed  Google Scholar 

  • Cao YP, Dai P, Dai SY (2014) Effects of salt stress on the growth of Asparagus officinalis L. seedlings and on Na+, K+ and Ca2+ distribution in them. J Southwest Univ (Nat Sci Ed) 36:31–36 (in Chinese)

    CAS  Google Scholar 

  • Cao YP, Dai P, Dai SY (2017) Effects of arbuscular mycorrhiza fungi (AMF) on osmoregulation substances and antioxidant enzyme activities of asparagus plant under salt stress. J Southwest Univ (Nat Sci Ed) 39:43–48 (in Chinese)

    Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    CAS  PubMed  Google Scholar 

  • Dong Y, Fan G, Zhao Z, Xu E, Deng M, Wang L, Niu S (2017) Transcriptome-wide profiling and expression analysis of two accessions of Paulownia australis under salt stress. Tree Genet Genomes 13:97

    Google Scholar 

  • ElSayed AI, Rafudeen MS, Golldack D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol 16:1–8

    CAS  PubMed  Google Scholar 

  • Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu MC, Maman J, Steinhorst L, Schmitz-Thom I, Yvon R, Kudla J, Wu HM, Cheung AY, Dinneny JR (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28:666–675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fernie AR, Carrari F, Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 7:254–261

    CAS  PubMed  Google Scholar 

  • Flowers TJ, Munns R, Colmer TD (2015) Sodium chloride toxicity and the cellular basis of salt tolerance in halophytes. Ann Bot 115:419–431

    CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    CAS  PubMed  PubMed Central  Google Scholar 

  • George S, Manoharan D, Li J, Britton M, Parida A (2018) Drought and salt stress in Macrotyloma uniflorum leads to common and specific transcriptomic responses and reveals importance of raffinose family oligosaccharides in stress tolerance. Gene Rep 10:7–16

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    CAS  PubMed  Google Scholar 

  • Gruber MY, Xia J, Yu M, Steppuhn H, Wall K, Messer D, Sharpe AG, Acharya SN, Wishart DS, Johnson D, Miller DR, Taheri A (2017) Transcript analysis in two alfalfa salt tolerance selected breeding populations relative to a non-tolerant population. Genome 60:104–127

    CAS  PubMed  Google Scholar 

  • Gu C, Xu S, Wang Z, Liu L, Zhang Y, Deng Y, Huang S (2018) De novo sequencing, assembly, and analysis of Iris lactea var. chinensis roots’ transcriptome in response to salt stress. Plant Physiol Biochem 125:1–12

    CAS  PubMed  Google Scholar 

  • Ji X, Van den Ende W, Van Laere A, Cheng S, Bennett J (2005) Structure, evolution, and expression of the two invertase gene families of rice. J Mol Evol 60:615–634

    CAS  PubMed  Google Scholar 

  • Jiang Z, Zhou X, Tao M, Yuan F, Liu L, Wu F, Wu X, Xiang Y, Niu Y, Liu F, Li C, Ye R, Byeon B, Xue Y, Zhao H, Wang HN, Crawford BM, Johnson DM, Hu C, Pei C, Zhou W, Swift GB, Zhang H, Vo-Dinh T, Hu Z, Siedow JN, Pei ZM (2019) Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572:341–346

    CAS  PubMed  Google Scholar 

  • Karami A, Sepehri A (2018) Beneficial role of MWCNTs and SNP on growth, physiological and photosynthesis performance of barley under NaCl stress. J Soil Sci Plant Nutr 18:752–771

    CAS  Google Scholar 

  • Kito K, Yamane K, Yamamori T, Matsuhira H, Tanaka Y, Takabe T (2018) Isolation, functional characterization and stress responses of raffinose synthase genes in sugar beet. J Plant Biochem Biotechnol 27:36–45

    CAS  Google Scholar 

  • Kong F, Li H, Sun P, Zhou Y, Mao Y (2014) De novo assembly and characterization of the transcriptome of seagrass Zostera marina using Illumina paired-end sequencing. PLoS One 9:e112245

    PubMed  PubMed Central  Google Scholar 

  • Liu A, Xiao Z, Li MW, Wong FL, Yung WS, Ku YS, Wang Q, Wang X, Xie M, Yim AKY, Chan TF, Lam HM (2018) Transcriptomic reprogramming in soybean seedlings under salt stress. Plant Cell Environ 42:98–114

    PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Mahajan MM, Goyal E, Singh AK, Gaikwad K, Kanika K (2017) Transcriptome dynamics provide insights into long-term salinity stress tolerance in Triticum aestivum cv. Kharchia Local. Plant Physiol Biochem 121:128–139

    CAS  PubMed  Google Scholar 

  • Manishankar P, Wang N, Köster P, Alatar AA, Kudla J (2018) Calcium signaling during salt stress and in the regulation of ion homeostasis. J Exp Bot 69:4215–4226

    CAS  Google Scholar 

  • Mansour MMF (2014) The plasma membrane transport systems and adaptation to salinity. J Plant Physiol 171:1787–1800

    CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    CAS  PubMed  Google Scholar 

  • Munns R, Gilliham M (2015) Salinity tolerance of crops—what is the cost? New Phytol 208:668–673

    CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    CAS  PubMed  Google Scholar 

  • Nakamura A, Fukuda A, Sakai S, Tanaka Y (2006) Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). Plant Cell Physiol 47:32–42

    CAS  PubMed  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    CAS  PubMed  PubMed Central  Google Scholar 

  • Obata T, Fernie AR (2012) The use of metabolomics to dissect plant responses to abiotic stresses. Cell Mol Life Sci 69:3225–3243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22:4056–4075

    CAS  Google Scholar 

  • Peterbauer T, Lahuta LB, Blöchl A, Mucha J, Jones DA, Hedley CL, Gòrecki RJ, Richter A (2001) Analysis of the raffinose family oligosaccharide pathway in pea seeds with contrasting carbohydrate composition. Plant Physiol 127:1764–1772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214

    CAS  PubMed  Google Scholar 

  • Qiu J, Henderson SW, Tester M, Roy SJ, Gilliham M (2016) SLAH1, a homologue of the slow type anion channel SLAC1, modulates shoot Cl- accumulation and salt tolerance in Arabidopsis thaliana. J Exp Bot 67:4495–4505

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman H, Jagadeeshselvam N, Valarmathi R, Sachin B, Sasikala R, Senthil N, Sudhakar D, Robin S, Muthurajan R (2014) Transcriptome analysis of salinity responsiveness in contrasting genotypes of finger millet (Eleusine coracana L.) through RNA-sequencing. Plant Mol Biol 85:485–503

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421

    CAS  Google Scholar 

  • Shao F, Zhang L, Wilson IW, Qiu D (2018) Transcriptomic analysis of Betula halophila in response to salt stress. Int J Mol Sci 19:3412

    PubMed Central  Google Scholar 

  • Skorupa M, Gołębiewski M, Domagalski K, Kurnik K, Abu Nahia K, Złoch M, Tretyn A, Tyburski J (2016) Transcriptomic profiling of the salt stress response in excised leaves of the halophyte Beta vulgaris ssp. maritime. Plant Sci 243:56–70

    CAS  PubMed  Google Scholar 

  • Sui N, Yang Z, Liu M, Wang B (2015) Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics 16:534

    PubMed  PubMed Central  Google Scholar 

  • Sui N, Wang Y, Liu S, Yang Z, Wang F, Wan S (2018) Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut. Front Plant Sci 9:7

    PubMed  PubMed Central  Google Scholar 

  • Sun Z, Qi X, Wang Z, Li P, Wu C, Zhang H, Zhao Y (2013) Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol Biochem 69:82–89

    CAS  PubMed  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Shinozaki K (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    CAS  PubMed  Google Scholar 

  • Thalmann M, Santelia D (2017) Starch as a determinant of plant fitness under abiotic stress. New Phytol 214:943–951

    CAS  PubMed  Google Scholar 

  • Van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:24.1–24.31

    Google Scholar 

  • Verma AK, Upadhyay SK, Verma PC, Solomon S, Singh SB (2011) Functional analysis of sucrose phosphate synthase (SPS) and sucrose synthase (SS) in sugarcane (Saccharum) cultivars. Plant Biol 13:325–332

    CAS  PubMed  Google Scholar 

  • Wang Z, Liu Y, Wei J, Deng X (2012) Cloning and expression of a gene encoding a raffinose synthase in the resurrection plant Boea hygrometrica. Chin Bull Bot 47:44–54 (in Chinese)

    CAS  Google Scholar 

  • Wang N, Qian Z, Luo M, Fan S, Zhang X, Zhang L (2018) Identification of salt stress responding genes using transcriptome analysis in green alga Chlamydomonas reinhardtii. Int J Mol Sci 19:3359

    PubMed Central  Google Scholar 

  • Wang Q, Cao K, Zhu G, Fang W, Chen C, Wang X, Wang L (2019) Comparative transcriptome analysis of genes involved in the response of resistant and susceptible peach cultivars to water stress. Sci Hortic 245:29–38

    CAS  Google Scholar 

  • Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. J Integr Plant Biol 60:796–804

    CAS  PubMed  Google Scholar 

  • Yang H, Sun M, Lin S, Guo Y, Yang Y, Zhang T, Zhang J (2017) Transcriptome analysis of Crossostephium chinensis provides insight into the molecular basis of salinity stress responses. PLoS One 12:e0187124

    PubMed  PubMed Central  Google Scholar 

  • Yang Z, Li JL, Liu LN, Xie Q, Sui N (2020) Photosynthetic regulation under salt stress and

  • Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Front Plant Sci 7:997

    Google Scholar 

  • Yue C, Cao H, Wang L, Zhou Y, Hao X, Zeng J, Wang X, Yang Y (2014) Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol Biochem 83:65–76

    CAS  PubMed  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

    PubMed  Google Scholar 

  • Zhang Q, Song X, Bartels D (2018) Sugar metabolism in the desiccation tolerant grass Oropetium thomaeum in response to environmental stresses. Plant Sci 270:30–36

    CAS  PubMed  Google Scholar 

  • Zheng L, Meng Y, Ma J, Zhao X, Cheng T, Ji J, Chang E, Meng C, Deng N, Chen L, Shi S, Jiang Z (2015) Transcriptomic analysis reveals importance of ROS and phytohormones in response to short-term salinity stress in Populus tomentosa. Front Plant Sci 6:678

    PubMed  PubMed Central  Google Scholar 

  • Zhong M, Yuan Y, Shu S, Sun J, Guo S, Yuan R, Tang Y (2015) Effects of exogenous putrescine on glycolysis and Krebs cycle metabolism in cucumber leaves subjected to salt stress. Plant Growth Regul 79:319–330

    Google Scholar 

  • Zhou J, Wang X, Jiao Y, Qin Y, Liu X, He K, Chen C, Ma L, Wang J, Xiong L, Zhang Q, Fan L, Deng XW (2007) Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol Biol 63:591–608

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou ML, Zhang Q, Zhou M, Sun ZM, Zhu XM, Shao JR, Tang YX, Wu YM (2012) Genome-wide identification of genes involved in raffinose metabolism in maize. Glycobiology 22:1775–1785

    CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu H, Yu X, Xu T, Wang T, Du L, Ren G, Dong K (2015) Transcriptome profiling of cold acclimation in bermudagrass (Cynodon dactylon). Sci Hortic 194:230–236

    CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (No. 31960314), Key R&D Projects of Hebei Province (No. 19226334D), Applied Basic Research Projects of Yunnan Province (No. 2018FG001-028), Scientific and Technological Innovation Projects of Hebei Province (No. 20193-01-01), and “Giant Project” of Hebei Province (No. 2018-3).

Author information

Author notes

  1. Xuhong Zhang and Changzhi Han contributed equally to this work.

Authors and Affiliations

  1. Institute of Cash Crops, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang, 050051, China

    Xuhong Zhang & Yanpo Cao

  2. College of Biodiversity Conservation and Utilization, Southwest Forestry University, Kunming, 650224, China

    Changzhi Han

Authors
  1. Xuhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Changzhi Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yanpo Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Yanpo Cao designed the project and performed the experiments. Xuhong Zhang and Changzhi Han analyzed the data and wrote the manuscript. All authors contributed to the revision of this manuscript and approved the final manuscript.

Corresponding author

Correspondence to Yanpo Cao.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Key Message

• RNA-Seq analysis of asparagus leaves under salt stress was performed.

• Total 4803 DEGs and their temporal expression patterns were identified.

• DEGs related to carbon metabolism, ion transport, and ROS metabolism may be crucial.

Electronic Supplementary Material

ESM 1

(XLS 446 kb)

ESM 2

(XLS 118 kb)

ESM 3

(XLS 462 kb)

ESM 4

(XLS 454 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, X., Han, C. & Cao, Y. Transcriptomic and Physiological Analyses Reveal the Dynamic Response to Salinity Stress of the Garden Asparagus (Asparagus officinalis L.). Plant Mol Biol Rep 38, 613–627 (2020). https://doi.org/10.1007/s11105-020-01226-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-020-01226-x

Keywords

Search

Navigation