Skip to main content

Advertisement

Log in

Identification of cold tolerance genes from leaves of mangrove plant Kandelia obovata by suppression subtractive hybridization

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Low temperature is a major abiotic stress that seriously limits mangrove productivity and distribution, the molecular mechanisms of cold tolerance involved in mangroves are still poorly understood at present. It was used to identify the potential cold-related genes in Kandelia obovata (K. obovata) by suppression subtractive hybridization. 334 cold-related expressed sequence tags (ESTs) out of 670 clones were isolated and sequenced. Among these ESTs, 143 unique cDNAs were identified and classified into ten groups, such as metabolism, energy, cell rescue and defense, transcription and photosynthesis according to NCBI blast. Based on bioinformatics analysis, these ESTs were mainly related to response to stimulus and metabolic process, and were included to 72 KEGG pathways. Two selected genes (e.g., aquaporin gene and zinc family protein gene) from the library were further analyzed by quantitative real-time PCR analysis. Both the two genes were found to be transcriptionally up-regulated under cold stress, which partly approve the construction of the subtractive cDNA library. The diversity of the putative functions of these genes indicated that cold stress resulted in a complex response in K. obovata. Further investigation on the functions and potential pathways of these genes will facilitate the understanding of the molecular adaptations to cold tolerance in mangrove plants.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Berardini TZ, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller LA, Yoon J, Doyle A, Lander G (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135:745–755

    Article  CAS  Google Scholar 

  • Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol Plant Mol Biol 31:491–543

    Article  Google Scholar 

  • Bohnert HJ, Ayoubi P, Borchert C, Bressan RA, Burnap RL, Cushman JC, Cushman MA, Deyholos M, Fischer R, Galbraith DW (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39:295–311

    Article  CAS  Google Scholar 

  • Brandle J, Richman A, Swanson A, Chapman B (2002) Leaf ESTs from Stevia rebaudiana: a resource for gene discovery in diterpene synthesis. Plant Mol Biol 50:613–622

    Article  CAS  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  CAS  Google Scholar 

  • Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25:288–289

    Article  CAS  Google Scholar 

  • Chen LZ, Wang WQ, Zhang YH, Zhao CL, Yang SC, Yang ZW, Chen YC, Xu HL, Zhogn CR, Su B, Fang BZ, Chen NM, Zeng CZ, Lin GH (2010) Damage to mangroves from extreme cold in early 2008 in Southern China. J Plant Ecol-UK (Chinese Version) 34:186–194

    Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  Google Scholar 

  • Chołuj D, Kalaji H, Niemyska B (1998) Analysis of the gas exchange components in chilled tomato plants. Photosynthetica 34:583–589

    Google Scholar 

  • Dos Santos CV, Delavault P, Letousey P, Thalouarn P (2003) Identification by suppression subtractive hybridization and expression analysis of Arabidopsis thaliana putative defence genes during Orobanche ramosa infection. Physiol Mol Plant 62:297–303

    Article  Google Scholar 

  • Ellis WL, Bowles JW, Erickson AA, Stafford N, Bell SS, Thomas M (2006) Alteration of the chemical composition of mangrove (Laguncularia racemosa) leaf litter fall by freeze damage. Estuar Coast Shelf S 68:363–371

    Article  CAS  Google Scholar 

  • Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • Fortunato AS, Lidon FC, Batista-Santos P, Leitao AE, Pais IP, Ribeiro AI, Ramalho JC (2010) Biochemical and molecular characterization of the antioxidative system of Coffea sp. under cold conditions in genotypes with contrasting tolerance. J Plant Physiol 167:333–342

    Article  CAS  Google Scholar 

  • Fu XH, Huang YL, Deng SL, Zhou RC, Yang GL, Ni XW, Li WJ, Shi SH (2005) Construction of a SSH library of Aegiceras corniculatum under salt stress and expression analysis of four transcripts. Plant Sci 169:147–154

    Article  CAS  Google Scholar 

  • Gao Y, Yang FQ, Cao X, Li CM, Wang Y, Zhao YB, Zeng GJ, Chen DM, Han ZH, Zhang XZ (2014) Differences in gene expression and regulation during ontogenetic phase change in apple seedlings. Plant Mol Biol Rep 32:357–371

    Article  CAS  Google Scholar 

  • Javot H, Maurel C (2002) The role of aquaporins in root water uptake. Ann Bot 90:301–313

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30

    Article  CAS  Google Scholar 

  • Kao WY, Shih CN, Tsai TT (2004) Sensitivity to chilling temperatures and distribution differ in the mangrove species Kandelia candel and Avicennia marina. Tree Physiol 24:859–864

    Article  Google Scholar 

  • Kim JC, Lee SH, Cheong YH, Yoo CM, Lee SI, Chun HJ, Yun DJ, Hong JC, Lee SY, Lim CO (2001) A novel cold-inducible zinc finger protein from soybean, SCOF-1, enhances cold tolerance in transgenic plants. Plant J 25:247–259

    Article  CAS  Google Scholar 

  • Komarova TV, Pozdyshev DV, Petrunia IV, Sheshukova EV, Dorokhov YL (2014) Pectin methylesterase-generated methanol may be involved in tobacco leaf growth. Biochemistry (Moscow) 79:102–110

    Article  CAS  Google Scholar 

  • Li XY, Xiao N, Zhang YH (2014) Toxic effects of octylphenol on the expression of genes in liver identified by suppression subtractive hybridization of Rana chensinensis. Ecotoxicology 23:1–10

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Maurel C, Chrispeels MJ (2001) Aquaporins. A molecular entry into plant water relations. Plant Physiol 125:135–138

    Article  CAS  Google Scholar 

  • Mishra S, Srivastava S, Nautiyal CS (2014) Differential gene expression profile in Pseudomonas putida NBRIC19-treated wheat (Triticum aestivum) plants subjected to biotic stress of Parthenium hysterophorus. Mol Biol Rep 41:1385–1399

    Article  CAS  Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Kanehisa M (2005) KAAS: KEGG automatic annotation server. Genome Inf 5:2005

    Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314

    Article  CAS  Google Scholar 

  • Pardossi A, Vernieri P, Tognoni F (1992) Involvement of abscisic acid in regulating water status in Phaseolus vulgaris L. during chilling. Plant Physiol 100:1243–1250

    Article  CAS  Google Scholar 

  • Peng Y, Lin W, Cai W, Arora R (2007) Overexpression of a Panax ginseng tonoplast aquaporin alters salt tolerance, drought tolerance and cold acclimation ability in transgenic Arabidopsis plants. Planta 226:729–740

    Article  CAS  Google Scholar 

  • Peng YL, Wang YS, Cheng H, Sun CC, Wu P, Wang LY, Fei J (2013) Characterization and expression analysis of three CBF/DREB1 transcriptional factor genes from mangrove Avicennia marina. Aquat Toxicol 140:68–76

    Article  Google Scholar 

  • Posmyk MM, Bailly C, Szafrańska K, Janas KM, Corbineau F (2005) Antioxidant enzymes and isoflavonoids in chilled soybean (Glycine max (L.) Merr.) seedlings. J Plant Physiol 162:403–412

    Article  CAS  Google Scholar 

  • Prabu G, Kawar PG, Pagariya MC, Prasad DT (2011) Identification of water deficit stress upregulated genes in sugarcane. Plant Mol Biol Rep 29:291–304

    Article  Google Scholar 

  • Ren H, Lu H, Shen W, Huang C, Guo Q, Li ZA, Jian S (2009) Sonneratia apetala Buch. Ham in the mangrove ecosystems of China: an invasive species or restoration species? Ecol Eng 35:1243–1248

    Article  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  CAS  Google Scholar 

  • Shen YH, Chen YH, Liu HY, Chiang FY, Wang YC, Hou LY, Jeng ST (2014) Expression of a gene encoding β-ureidopropionase is critical for pollen germination in tomatoes. Physiol Plant 150:425–435

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  Google Scholar 

  • Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  Google Scholar 

  • Song H, Wang YS, Sun CC, Wang YT, Peng YL, Cheng H (2012) Effects of pyrene on antioxidant systems and lipid peroxidation level in mangrove plants, Bruguiera gymnorrhiza. Ecotoxicology 21:1625–1632

    Article  CAS  Google Scholar 

  • Tomlinson P (1986) The botany of mangroves. Cambridge tropical biology series. Cambridge University Press, Cambridge

    Google Scholar 

  • Wang WQ, You SY, Wang YB, Huang L, Wang M (2011) Influence of frost on nutrient resorption during leaf senescence in a mangrove at its latitudinal limit of distribution. Plant Soil 342:105–115

    Article  CAS  Google Scholar 

  • Wong YY, Ho CL, Nguyen PD, Teo SS, Harikrishna JA, Rahim RA, Wong MCVL (2007) Isolation of salinity tolerant genes from the mangrove plant, Bruguiera cylindricaby using suppression subtractive hybridization (SSH) and bacterial functional screening. Aquat Bot 86:117–122

    Article  CAS  Google Scholar 

  • Xu H, He X, Wang K, Chen L, Li K (2012) Identification of early nitrate stress response genes in Spinach roots by suppression subtractive hybridization. Plant Mol Biol Rep 30:633–642

    Article  CAS  Google Scholar 

  • Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6:486–503

    Article  CAS  Google Scholar 

  • Zou C, Jiang W, Yu D (2010) Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J Exp Bot 61:3901–3914

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 41430966 and No. 41176101), the key projects in the National Science & Technology Pillar Program in the Eleventh Five-year Plan Period (No. 2012BAC07B0402) and the Knowledge Innovation Programs of the Chinese Academy of Sciences (No. KSCX2-SW-132).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to You-Shao Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fei, J., Wang, YS., Jiang, ZY. et al. Identification of cold tolerance genes from leaves of mangrove plant Kandelia obovata by suppression subtractive hybridization. Ecotoxicology 24, 1686–1696 (2015). https://doi.org/10.1007/s10646-015-1486-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-015-1486-9

Keywords