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Photosynthetica

, Volume 56, Issue 4, pp 1370–1377 | Cite as

Salicylic acid-induced photosynthetic adaptability of Zea mays L. to polyethylene glycol-simulated water deficit is associated with nitric oxide signaling

  • R. X. Shao
  • L. F. Xin
  • J. M. Guo
  • H. F. Zheng
  • J. Mao
  • X.P. Han
  • L. Jia
  • S. J. Jia
  • C. G. Du
  • R. Song
  • Q. H. Yang
  • R. W. Elmore
Original paper
  • 46 Downloads

Abstract

Salicylic acid (SA) and nitric oxide (NO) form a new group of plant growth substances that cooperatively interact to promote plant growth and productivity. Water deficit (WD) stress is a major limiting factor for photosynthesis, which in turn limits crop yield. However, the mechanism of SA and NO in stimulating photosynthesis has not yet been elucidated. Therefore, in this study, we investigated the SA- and NO-mediated photosynthetic adaptability of maize seedlings to WD in terms of photosynthetic parameters, activities and mRNA levels of CO2 assimilation enzymes. Our results showed that SA alleviated the WD-induced reduction of photosynthetic performance. The activities of Rubisco and Rubisco activase enzymes increased significantly due to SA pretreatment. Moreover, higher transcription rates of Rbc L, ZmRCAα and ZmRCAβ mRNA further confirmed the effects of SA on CO2 assimilation. WD or SA-induced decreases or increases of CO2 assimilation ability were further decreased after c-PTIO addition.

Additional key words

chlorophyll fluorescence transients gene expression nitric oxide scavenger photosynthetic characteristics 

Abbreviations

cGMP

cyclic guanosine monophosphate

Chl

chlorophyll

c-PTIO

2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide

Ci

intercellular CO2 concentration

Fv/Fm

maximum photochemical efficiency of PSII

gs

stomatal conductance

LA

leaf area

MAPK

mitogen-activated kinases

NO

nitric oxide

PEG

polyethylene glycol

PIABS

photosynthesis performance in PSII electron transport

PN

photosynthetic assimilation rate

RCA

Rubisco activase

RCs

per active reaction centers

RWC

relative water content

SA

salicylic acid

WD

water deficit

WUEi

intrinsic water-use efficiency

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References

  1. Ashraf M., Harris P.J.C.: Photosynthesis under stressful environments: an overview.–Photosynthetica 51: 163–190, 2013.CrossRefGoogle Scholar
  2. Bajguz A.: Nitric oxide: role in plants under abiotic stress.–In: Parvaiz A., Mohd R.W. (ed.): Biomedical and Life Sciences: Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment. Pp. 137–159. Springer, New York 2013.Google Scholar
  3. Boex-Fontvieille E., Daventure M., Jossier M. et al.: Phosphorylation pattern of Rubisco activase in Arabidopsis leaves.–Plant Biol. 16: 550–557, 2014.CrossRefPubMedGoogle Scholar
  4. Carmo-Silva A.E., Salvucci M.E.: The regulatory properties of rubisco activase differ among species and affect photosynthetic induction during light transitions.–Plant Physiol. 161: 1645–1655, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chen P., Li X., Huo K. et al.: Promotion of photosynthesis in transgenic rice over-expressing of maize C4 phosphoenolpyruvate carboxylase gene by nitric oxide donors.–J. Plant Physiol. 171: 458–466, 2014a.CrossRefPubMedGoogle Scholar
  6. Chen Y., Jin J.H., Jiang Q.S. et al.: Sodium bisulfite enhances photosynthesis in rice by inducing Rubisco activase gene expression.–Photosynthetica 52: 475–478, 2014b.CrossRefGoogle Scholar
  7. Cheng T., Chen J., Ef A.A. et al.: Quantitative proteomics analysis reveals that S-nitrosoglutathione reductase (GSNOR) and nitric oxide signaling enhance poplar defense against chilling stress.–Planta 242: 1361–1390, 2015.CrossRefPubMedGoogle Scholar
  8. Corpas F.J., Leterrier M., Valderrama R. et al.: Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress.–Plant Sci. 181: 604–611, 2011.CrossRefPubMedGoogle Scholar
  9. Cui J.X., Zhou Y.H., Ding J.G. et al.: Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumberpce.–Plant Cell Environ. 34: 347–358, 2011.CrossRefPubMedGoogle Scholar
  10. Dias M.C., Brüggemann W.: Limitations of photosynthesis in phaseolus vulgaris under drought stress: gas exchange, chlorophyll fluorescence and Calvin cycle enzymes.–Photosynthetica 48: 96–102, 2010.CrossRefGoogle Scholar
  11. Elings A.: Estimation of leaf area in tropical maize.–Agron. J. 92: 436–444, 2000.CrossRefGoogle Scholar
  12. FAOSTAT: Food and agricultural commodities production. https://doi.org/faostat.fao.org/site/339/default.aspx, 2010.
  13. Gondor O. K., Janda T., Soós V. et al.: Salicylic acid induction of flavonoid biosynthesis pathways in wheat varies by treatment.–Front. Plant Sci. 7: 1447, 2016.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hancock J.T.: NO synthase? Generation of nitric oxide in plants.–Period. Biol. 114: 19–24, 2012.Google Scholar
  15. Iqbal N., Umar S., Khan N.A. et al.: A new perspective of phytohormones in salinity tolerance: Regulation of proline metabolism.–Environ. Exp. Bot. 100: 34–42, 2014.CrossRefGoogle Scholar
  16. Jasid S., Simontacchi M., Bartoli C.G. et al.: Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins.–Plant Physiol. 142: 1246–1255, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Jiang Y.P., Cheng F., Zhou Y.H. et al.: Cellular glutathione redox homeostasis plays an important role in the brassinosteroidinduced increase in CO2 assimilation in Cucumis sativus.–New Phytol. 194: 932–943, 2012.CrossRefPubMedGoogle Scholar
  18. Kausar F., Shahbaz M.: Interactive effect of foliar application of nitric oxide (NO) and salinity on wheat (Triticum aestivum L.).–Pak. J. Bot. 45: 67–73, 2013.Google Scholar
  19. Kovacs I., Lindermayr C.: Nitric oxide-based protein modification: formation and site-specificity of protein S-nitrosylation.–Front. Plant Sci. 4: 137, 2013.PubMedPubMedCentralGoogle Scholar
  20. Liao W.B., Huang G.B., Yu J.H. et al.: Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development.–Plant Physiol. Bioch. 58: 6–15, 2012.CrossRefGoogle Scholar
  21. Livak K.J., Schmittgen T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2 -ΔΔCT method. -Methods 25: 402–408, 2001.CrossRefPubMedGoogle Scholar
  22. Liu S., Dong Y., Xu L. et al.: Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings.–Plant Growth Regul. 73: 67–78, 2014.CrossRefGoogle Scholar
  23. Mostofa M.G., Fujita M., Tran L.S.P.: Nitric oxide mediates hydrogen peroxide-and salicylic acid-induced salt tolerance in rice (Oryza sativa L.) seedlings.–Plant Growth Regul. 77: 265–277, 2015.CrossRefGoogle Scholar
  24. Parry M.A.J., Andralojc P.J., Scales J.C.: Rubisco activity and regulation as targets for crop improvement.–J. Exp. Bot. 64: 717–730, 2013.CrossRefPubMedGoogle Scholar
  25. Procházková D., Haisel D., Wilhelmová N. et al.: Effects of exogenous nitric oxide on photosynthesis.–Photosynthetica 51: 483–489, 2013.CrossRefGoogle Scholar
  26. Qiao W., Li C., Fan L.M.: Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses.–Environ. Exp. Bot. 100: 84–93, 2014.CrossRefGoogle Scholar
  27. Serraj R., McNally K.L., Slamet-Loedin I. et al.: Drought resistance improvement in rice: an integrated genetic and resource management strategy.–Plant Prod. Sci. 14: 1–14, 2011.CrossRefGoogle Scholar
  28. Shao R., Wang K., Shangguan Z.P.: Cytokinin-induced photosynthetic adaptability of Zea mays L. to drought stress associated with nitric oxide signal: probed by ESR spectroscopy and fast OJIP fluorescence rise.–J. Plant Physiol. 167: 472–479, 2010.CrossRefPubMedGoogle Scholar
  29. Shao R.X., Chen J.H., Miao F. et al.: Photosynthetic performance of Triticum aestivum L. in response to water and nitrogen deficit.–J. Food Agric. Environ. 11: 1252–1256, 2013.Google Scholar
  30. Siddiqui M.H., Al-Whaibi M.H., Ali H.M. et al.: Mitigation of nickel stress by the exogenous application of salicylic acid and nitric oxide in wheat.–Aust. J. Crop Sci. 7: 1780–1788, 2013.Google Scholar
  31. Sikder S., Foulkes J., West H. et al.: Evaluation of photosynthetic potential of wheat genotypes under drought condition.–Photosynthetica 53: 47–54, 2015.CrossRefGoogle Scholar
  32. Simaei M., Khavarinejad R.A., Saadatmand S. et al.: Interactive effects of salicylic acid and nitric oxide on soybean plants under NaCl salinity.–Russ. J. Plant Physl+ 58: 783–790, 2011.CrossRefGoogle Scholar
  33. Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples.–In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445–483. Taylor and Francis, London 2000.Google Scholar
  34. Suzuki Y., Makino A.: Translational downregulation of RBCL is operative in the coordinated expression of Rubisco genes in senescent leaves in rice.–J. Exp. Bot. 64: 1145–1152, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Tatar O., Brück H., Asch F.: Photosynthesis and remobilization of dry matter in wheat as affected by progressive drought stress at stem elongation stage.–J. Agro. Crop Sci. 202: 292–299, 2016.CrossRefGoogle Scholar
  36. Tossi V., Cassia R., Bruzzone S. et al.: ABA says NO to UV-B: a universal response?–Trends Plant Sci. 17: 510–517, 2012.CrossRefPubMedGoogle Scholar
  37. Vanlerberghe G.C., Martyn G.D., Dahal K.: Alternative oxidase: a respiratory electron transport chain pathway essential for maintaining photosynthetic performance during drought stress.–Physiol. Plantarum 157: 322–337, 2016.CrossRefGoogle Scholar
  38. Wang G.P., Hui Z., Li F. et al.: Improvement of heat and drought photosynthetic tolerance in wheat by over accumulation of glycinebetaine.–Plant Biotechnol. Rep. 4: 213–222, 2010.CrossRefGoogle Scholar
  39. Wang Y., Suo B., Zhao T. et al.: Effect of nitric oxide treatment on antioxidant responses and psbA gene expression in two wheat cultivars during grain filling stage under drought stress and rewatering.–Acta Physiol. Plant. 33: 1923, 2011.CrossRefGoogle Scholar
  40. Wang Q., Liang X., Dong Y. et al.: Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of perennial ryegrass under cadmium stress.–J. Plant Growth Regul. 32: 721–731, 2013.CrossRefGoogle Scholar
  41. Wu Q.S., Xia R.X.: Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions.–J. Plant Physiol. 163: 417–425, 2006.CrossRefPubMedGoogle Scholar
  42. Xu L., Yu J., Han L. et al.: Photosynthetic enzyme activities and gene expression associated with drought tolerance and postdrought recovery in Kentucky bluegrass.–Environ. Exp. Bot. 89: 28–35, 2013.CrossRefGoogle Scholar
  43. Xu L.L., Fan Z.Y., Dong Y.J. et al.: Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of two peanut cultivars under cadmium stress.–Biol. Plantarum 59: 171–182, 2015CrossRefGoogle Scholar
  44. Yin Z.T., Zhang Z.L., Deng D.X. et al.: Characterization of rubisco activase genes in maize: an a-isoform gene functions alongside a β-isoform gene.–Plant Physiol. 164: 2096–2106, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Zhao G.W., Xu H.L., Zhang P.J. et al.: Effects of 2,4-epibrassinolide on photosynthesis and Rubisco activase gene expression in Triticum aestivum L. seedlings under a combination of drought and heat stress.–Plant Growth Regul. 81: 377–384, 2017.CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • R. X. Shao
    • 1
  • L. F. Xin
    • 1
  • J. M. Guo
    • 1
  • H. F. Zheng
    • 1
  • J. Mao
    • 1
  • X.P. Han
    • 1
  • L. Jia
    • 1
  • S. J. Jia
    • 1
  • C. G. Du
    • 1
    • 2
  • R. Song
    • 1
  • Q. H. Yang
    • 1
  • R. W. Elmore
    • 3
  1. 1.Collaborative Innovation Center of Henan Grain Crops and State Key Laboratory of Wheat and Maize Crop Science/College of AgronomyHenan Agricultural UniversityZhengzhouChina
  2. 2.Department of BiologyMontclair State UniversityMontclairUSA
  3. 3.Department of Agronomy and HorticultureUniversity of Nebraska-LincolnLincolnUSA

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