Skip to main content
Log in

Differential salt tolerance in seedlings derived from dimorphic seeds of Atriplex centralasiatica: from physiology to molecular analysis

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Seed dimorphism provides plants with alternative strategies for survival in unfavorable environments. Here, we investigated the physiological responses and differential gene expression caused by salinity exposure in Atriplex centralasiatica plants grown from the two different seed morphs. Seedlings derived from yellow seeds (YS) showed a greater salt tolerance than those derived from brown seeds (BS). Salt treatment induced nitric oxide (NO) synthesis in roots, and seedlings derived from YS produced greater amounts of NO than did those from BS. Analyses of NO scavenging during salt stress revealed that NO contributed to the differential salt tolerance in seedlings derived from the two seed morphs by modulating antioxidative enzyme activity, hydrogen peroxide accumulation and the ion equilibrium. We also applied transcriptomics and subsequent microarray analysis to evaluate the differential gene expression during salt treatment. These genes encoded proteins related to osmotic and ionic homeostasis, redox equilibrium and signal transduction. A select group of genes including GH3.3, CAT1/2, TIP1, SIHP1 and EXP1 were further confirmed with RT-PCR analysis. These results revealed that the enhanced salt tolerance of seedlings from YS appeared to be governed by a superior ability to achieve ionic homeostasis and redox equilibrium, a rapid response to salt stress, and ultimately better growth potential. NO serves as a vital regulator in these processes.

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

Access this article

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 a
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

BS:

Brown seeds

cPTIO:

2-(4-Carboxyphenyl)-4,4,5,5-tetramethyl imidazoline-1-oxyl- 3-oxide

DAF-2 DA:

4,5-Diaminofluorescein diacetate

DCFH-DA:

2,7-Dichlorfluorescein-diacetate

L-NAME:

N G-Nitro-l-Arg-methyl ester

NO:

Nitric oxide

PI:

Propidium iodide

SNP:

Sodium nitroprusside

YS:

Yellow seeds

References

  • Bethke PC, Gubler F, Jacobsen JV, Jones RL (2004) Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219:847–855

    Article  CAS  PubMed  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde NM, Graziano ML, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2000) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • De Cnodder T, Vissenberg K, Van Der Straeten D, Verbelen JP (2005) Regulation of cell length in the Arabidopsis thaliana root by the ethylene precursor aminocyclopropane-1-carboxylic acid: a matter of apoplastic reactions. New Phytol 168:541–550

    Article  PubMed  Google Scholar 

  • De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, Sanità di Toppi L, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228

    Article  PubMed Central  PubMed  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Throne TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Durner J, Klessig DF (1999) Nitric oxide as a signal in plants. Curr Opin Plant Biol 2:369–372

    Article  CAS  PubMed  Google Scholar 

  • Esser C, Alberti S, Hohfeld J (2004) Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim Biophys Acta 1695:171–188

    Article  CAS  PubMed  Google Scholar 

  • Ellison AM (1987) Effects of seed dimorphism on the density-dependent dynamics of experimental populations of Atriplex triangularis (Chenopodiaceae). Am J Bot 74:1280–1288

    Article  Google Scholar 

  • Geisler M, Frangne N, Gome`s E, Martinoia E, Palmgren MG (2000) The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124:1814–1827

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103

    Article  CAS  PubMed  Google Scholar 

  • He YK, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing LF, Yang ZG, Chen LE, Guo FQ, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971

    Article  CAS  PubMed  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture for growing plants without soil. California Agricultural Experiment Station Circular, 347, Berkeley

  • Hu X, Neill SJ, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee S, Lee DW, Lee Y, Mayer U, Stierhof YD, Lee S, Jurgens G, Hwang I (2009) Heat shock protein cognate 70–4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome aystem in Arabidopsis. Plant Cell 21:3984–4001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li W, An P, Liu X, Khan MA, Tanaka K (2008) The effect of light, temperature and bracteoles on germination of polymorphic seeds of Atriplex centralasiatica Iljin under saline conditions. Seed Sci Technol 36:325–338

    Google Scholar 

  • Li WQ, Liu XJ, Khan MA, Yamaguchi S (2005) The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. J Plant Res 118:207–214

    Article  CAS  PubMed  Google Scholar 

  • Libourel IGL, Bethke PC, De Michele R, Jones RL (2006) Nitric oxide gas stimulates germination of dormant Arabidopsis seeds: use of a flow-through apparatus for delivery of nitric oxide. Planta 223:813–820

    Article  CAS  PubMed  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  CAS  PubMed  Google Scholar 

  • Martre P, Morillon R, Barrieu F, North GB, Nobel PS, Chrispeels MJ (2002) Plasma membrane aquaporins play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman D, Goldman SL (2004) ***Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366

    Article  CAS  PubMed  Google Scholar 

  • Peng Z, Wang MC, Li F, Lv HJ, Li CL, Xia GM (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics 8:2676–2686

    Article  CAS  PubMed  Google Scholar 

  • Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant-Microbe In 16:1094–1105

    Article  CAS  Google Scholar 

  • Qiu N, Lu C (2003) Enhanced tolerance of photosynthesis against high temperature damage in slatadapted halophyte Atriplex centralasiatica plants. Plant Cell Environ 26:1137–1145

    Article  Google Scholar 

  • Ranieri A, Castagna A, Pacini J, Baldan B, Mensuali Sodi A, Solditini GF (2003) Early production and scavenging of hydrogen peroxide in the apoplast of sunflower plants exposed to ozone. J Exp Bot 54:2529–2540

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM, Testillano PS, Risueño MC, del Río LA, Sandalio LM (2009) Cellular response of pea plants to cadmium toxicity: cross-talk between reactive oxygen species, nitric oxide and calcium. Plant Physiol 150:229–243

    Article  PubMed Central  PubMed  Google Scholar 

  • Shi YH, Zhu SW, Mao XZ, Feng JX, Qin YM, Zhang L, Cheng J, Wei LP, Wang ZY, Zhu YX (2006) Transcriptome profiling, molecular biological, and physiological studies reveal a major role for ethylene in cotton fiber cell elongation. Plant Cell 18:651–664

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sulmon C, Gouesbet G, Binet F, Martin-Laurent F, El Amrani A, Couee I (2007) Sucrose amendment enhances phytoaccumulation of the herbicide atrazine in Arabidopsis thaliana. Environ Pollut 145:507–515

    Article  CAS  PubMed  Google Scholar 

  • Tewari RK, Kim SY, Hahn EJ, Paek KY (2008) Involvement of nitric oxide-induced NADPH oxidase in adventitious root growth and antioxidant defense in Panax ginseng. Plant Biotechnol Rep 2:113–122

    Article  Google Scholar 

  • Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522

    Article  CAS  PubMed  Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant system in acid rain treated bean plants: protective role of exogenous polyammines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Wang L, Huang ZY, Baskin JM, Dong M (2008) Germination of dimorphic seeds of the desert annual halophyte Suaeda aralocaspica (Chenopodiaceae), a C4 plant without Kranz anatomy. Ann Bot 102:757–769

    Article  PubMed  Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923

    Article  CAS  PubMed  Google Scholar 

  • Wink DA, Mitchell JB (1998) Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radical Biol Med 25:434–456

    Article  CAS  Google Scholar 

  • Xu J, Wang WY, Yin HX, Liu XJ, Sun H, Mi Q (2010a) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330

    Article  CAS  Google Scholar 

  • Xu J, Yin HX, Liu XJ, Li X (2010b) Salt affects plant Cd-stress responses by modulating growth and Cd accumulation. Planta 231:449–459

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Yin HX, Li YL, Liu XJ (2010c) Nitric Oxide Is Associated with Long-Term Zinc Tolerance in Solanum nigrum. Plant Physiol 154:1319–1334

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang LP, Mehta SK, Liu ZP, Yang ZM (2008) Copper-induced proline synthesis is associated with nitric oxide generation in Chlamydomonas reinhardtii. Plant Cell Physiol 49:411–419

    Article  CAS  PubMed  Google Scholar 

  • Zhang YY, Wang LL, Liu YL, Zhang Q, Wei QP, Zhang W-H (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555

    Article  CAS  PubMed  Google Scholar 

  • Zhao LQ, Zhang F, Guo JK, Yang YL, Li BB, Zhang LX (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849–857

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr Weiqiang Li for helpful discussions. This work was supported by the National Major Special Project on New Varieties Cultivation for Transgenic Organisms (2009ZX08009-130B), the National Basic Research Program of China (2009CB118305), the National Key Technologies R&D Program of China (2009BADA3B04) and the Knowledge Innovation Program of the Chinese Academy of Sciences (KZCX2-YW-447).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaojing Liu.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, J., Yin, H., Yang, L. et al. Differential salt tolerance in seedlings derived from dimorphic seeds of Atriplex centralasiatica: from physiology to molecular analysis. Planta 233, 859–871 (2011). https://doi.org/10.1007/s00425-010-1347-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1347-y

Keywords

Navigation