Journal of Plant Research

, Volume 125, Issue 1, pp 155–164

Drought-induced proline accumulation is uninvolved with increased nitric oxide, which alleviates drought stress by decreasing transpiration in rice

Regular Paper

Abstract

Accumulation of proline is trusted to be an adaptive response of plants against drought stress, and exogenous application of nitric oxide (NO) enhances proline accumulation in Cu-treated algae. In order to investigate whether NO works as a necessary signaling molecule in drought-induced proline accumulation in rice leaves, effects of drought stress on endogenous NO content and proline accumulation were studied in rice leaves, using sodium nitroprusside (SNP, a NO donor) and 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO, a NO scavenger). The results showed that drought treatment increased both endogenous NO and proline contents in rice leaves, while foliar spray of various concentrations of SNP failed to induce proline accumulation in the leaves of well-watered rice and foliar spray of cPTIO failed to inhibit proline accumulation in the leaves of drought-stressed rice. These results indicate that increase of endogenous NO is dispensable for proline accumulation in the leaves of rice under drought stress. Further studies indicate that exogenous application of NO alleviates drought-induced water loss and ion leakage by decreasing transpiration rate of rice leaves.

Keywords

Abscisic acid Oryza Sodium nitroprusside Transpiration rate Water stress 

Abbreviations

ABA

Abscisic acid

CEC

Cation exchange capacity

cPTIO

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

DAF-FM DA

4-Amino-5-methylamino-2′,7′-difluorofluorescein diacetate

DW

Dry weight

FW

Fresh weight

NO

Nitric oxide

P5CS

Δ1-Pyrroline-5-carboxylate synthetase

PPED

Photosynthetic photo flux density

SNP

Sodium nitroprusside

SW

Saturated weight

ROS

Reactive oxygen species

RWC

Relative water content

References

  1. Ábrahám E, Rigó G, Székely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372PubMedCrossRefGoogle Scholar
  2. Alia MP, Matysik J (2001) Effect of proline on the production of singlet oxygen. Amino Acids 21:191–203Google Scholar
  3. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubiś J (2009) Involvement of nitric oxide in water stress-induced responses of cucumber roots. Plant Sci 177:682–690CrossRefGoogle Scholar
  4. Bates LS, Waldren RP, Tear ID (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  5. Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou J, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315PubMedCrossRefGoogle Scholar
  6. Crawford NM, Guo FQ (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200PubMedCrossRefGoogle Scholar
  7. Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. PNAS 99:16314–16318PubMedCrossRefGoogle Scholar
  8. Farooq M, Basra SMA, Wahid A, Rehman H (2009) Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agron Crop Sci 195:254–261CrossRefGoogle Scholar
  9. Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Exp Bot 45:105–114PubMedCrossRefGoogle Scholar
  10. García-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204PubMedCrossRefGoogle Scholar
  11. Hao G, Xing Y, Zhang J (2008) Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signaling of maize seedling. J Integr Plant Biol 50:435–442PubMedCrossRefGoogle Scholar
  12. Hare PD, Cress WA, van Staden J (1999) Proline synthesis and degradation: a model for elucidating stress-related signal transduction. J Exp Bot 50:413–434CrossRefGoogle Scholar
  13. Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Nitrate oxide: the versatility of an extensive signal molecule. Ann Rev Plant Biol 54:109–136CrossRefGoogle Scholar
  14. Lei Y, Yin C, Ren J, Li C (2007) Effect of osmotic stress and sodium nitroprusside pretreatment on proline metabolism of wheat seedlings. Biol Plant 51:386–390CrossRefGoogle Scholar
  15. Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F (1999) Antioxidant defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physio 119:1091–1099CrossRefGoogle Scholar
  16. López-Carrión AI, Castellano R, Rosales MA, Ruiz JM, Romero L (2008) Role of nitric oxide under saline stress: implications on proline metabolism. Biol Plant 52:587–591CrossRefGoogle Scholar
  17. Luna CM, Pastori GM, Driscoll S, Groten K, Bernard S, Foyer CH (2005) Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. J Exp Bot 56:417–423PubMedCrossRefGoogle Scholar
  18. Ma XL, Wei XH, Long RJ, Cui WJ, Wan YL (2005) Studies on mechanism of enhancing the chilling resistance of annual ryegrass by exogenous nitric oxide. Acta Ecol Sin 25:1269–1274Google Scholar
  19. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefGoogle Scholar
  20. Qiao W, Fan L (2008) Nitric oxide signaling in plant responses to abiotic stresses. J Integr Plant Biol 50:1238–1246PubMedCrossRefGoogle Scholar
  21. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417PubMedCrossRefGoogle Scholar
  22. Siripornadulsil S, Traina S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847PubMedCrossRefGoogle Scholar
  23. Tan J, Zhao H, Hong J, Han Y, Li H, Zhao W (2008) Effects of exogenous nitric oxide on photosynthesis, antioxidant capacity and proline accumulation in wheat seedlings subjected to osmotic stress. World J Agri Sci 4:307–313Google Scholar
  24. Taylor GB (1996) Proline and water deficit. Ups, downs, ins and outs. Plant Cell 8:1221–1224CrossRefGoogle Scholar
  25. Tian X, Lei Y (2006) Nitric oxide treatment alleviates drought stress in wheat seedlings. Biol Plant 50:775–778CrossRefGoogle Scholar
  26. Xiong L, Ishitani M, Lee H, Zhu JK (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress and osmotic stress responsive gene expression. Plant Cell 13:2063–2083PubMedCrossRefGoogle Scholar
  27. Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755–765PubMedCrossRefGoogle Scholar
  28. Xiong J, Fu G, Tao L, Zhu C (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13–20PubMedCrossRefGoogle Scholar
  29. Zhang J, Kirkham MB (1994) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791Google Scholar
  30. 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 49:411–419PubMedCrossRefGoogle Scholar
  31. Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767PubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer 2011

Authors and Affiliations

  1. 1.State Key Laboratory of Rice BiologyChina National Rice Research InstituteHangzhouPeople’s Republic of China
  2. 2.State Key Laboratory of Plant Physiology and Biochemistry, College of Life SciencesZhejiang UniversityHangzhouPeople’s Republic of China
  3. 3.College of Life SciencesChina Jiliang UniversityHangzhouPeople’s Republic of China

Personalised recommendations