Skip to main content
SpringerLink
Log in

The positive roles of exogenous putrescine on chlorophyll metabolism and xanthophyll cycle in salt-stressed cucumber seedlings

  • Original paper
  • Published:
Photosynthetica

Abstract

The effects of foliar spray of putrescine (Put; 8 mM) on chlorophyll (Chl) metabolism and xanthophyll cycle in cucumber seedlings were investigated under saline conditions of 75 mM NaCl. Exogenous Put promoted the conversion of uroporhyrinogen III to protoporphyrin IX and alleviated decreases in Chl contents and in a size of the xanthophyll cycle pool under salt stress. Moreover, the Put treatment reduced the activities of uroporphyrinogen III synthase, chlorophyllase, and Mg-dechelatase and downregulated the transcriptional levels of glutamyl-tRNA reductase, 5-aminolevulinate dehydratase, uroporphyrinogen III synthase, uroporphyrinogen III decarboxylase, and chlorophyllide a oxygenase, but significantly increased the expression levels of non-yellow coloring 1-like, pheide a oxygenase, red chlorophyll catabolite reductase, and violaxanthin de-epoxidase. Taken together, these results suggest that Put might improve Chl metabolism and xanthophyll cycle by regulating enzyme activities and mRNA transcription levels in a way that improved the salt tolerance of cucumber plants.

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

Similar content being viewed by others

Abbreviations

A:

antheraxanthin

ALA:

δ-aminolevulinic acid

ALAD:

5-aminolevulinate dehydratase

Car:

carotenoids

CAO:

chlorophyllide a oxygenase

Chl:

chlorophyll

CBR:

chlorophyll b reductase

Chlase:

chlorophyllase

CHLH:

Mg chelatase H subunit

DEPS:

de-epoxidation of the xanthophyll cycle

DOE:

days of experiment

FM:

fresh mass

HEMA1:

glutamyl-tRNA reductase

MDCase:

Mg dechelatase

Mg-Proto IX:

Mg proporphyrin IX

NOL:

NYC1-like

NPQ:

nonphotochemical quenching

NYC1:

non-yellow coloring 1

PAO:

pheide a oxygenase

PAs:

polyamines

PBG:

porphobilinogen

PBGD:

porphobilinogen deaminase

PChl:

protochlorophyllide

PPH:

pheophytinase

PPO:

protoporphyrinogen IX oxidase

ProtoIX:

protoporphyrin IX

Put:

putrescine

RCCR:

red chlorophyll catabolite reductase

Spd:

spermidine

Spm:

spermine

UroIII:

uroporhyrinogen III

UROD:

uroporphyrinogen III decarboxylase

UROS:

uroporphyrinogen III synthase

V:

violaxanthin

VAZ:

xanthophyll cycle pool

VDE:

violaxanthin de-epoxidase

Z:

zeaxanthin.

References

  • Alawady A.E., Grimm B.: Tobacco Mg protoporphyrin IX methyltransferase is involved in inverse activation of Mg porphyrin and protoheme synthesis. — Plant J. 41: 282–290, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Bagni N., Tassoni A.: Biosynthesis, oxidation and conjugation of aliphatic polyamines in higher plants. — Amino Acids 20: 301–317, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Bogorad L.: Porphyrin synthesis. — Methods Enzymol. 5: 885–895, 1962.

    Article  CAS  Google Scholar 

  • Caffarri S., Croce R., Breton J. et al.: The major antenna complex of photosystem II has a xanthophyll binding site not involved in light harvesting. — J. Biol. Chem. 276: 35924–35933, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Costa M.L., Civello P.M., Chaves A.R. et al.: Effect of ethephon and 6-benzylaminopurine on chlorophyll degrading enzymes and a peroxidase-linked chlorophyll bleaching during postharvest senescence of broccoli (Brassica oleracea L.) at 20 C. — Postharvest Biol. Tec. 35: 191–199, 2005.

    Article  CAS  Google Scholar 

  • Dei M.: Benzyladenine-induced stimulation of 5-aminolevulinic acid accumulation under various light intensities in levulinic acid-treated cotyledons of etiolated cucumber. — Physiol. Plantarum 64: 153–160, 1985.

    Article  CAS  Google Scholar 

  • García-Plazaola J.I., Becerril J.M.: A rapid high-performance liquid chromatography method to measure lipophilic antioxidants in stressed plants: simultaneous determination of carotenoids and tocopherols. — Phytochem. Analysis 10: 307–313, 1999.

    Article  Google Scholar 

  • Havaux M., DallOsto L., Cuiné S. et al.: The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. — J. Biol. Chem. 279: 13878–13888, 2004.

    Article  CAS  PubMed  Google Scholar 

  • Hieber A.D., Bugos R.C., Yamamoto Y.: Plant lipocalins: violaxanthin de-epoxidase and zeaxanthin epoxidase. — BBAProtein Struct. M. 1482: 84–91, 2000.

    CAS  Google Scholar 

  • Hodgins R.R., van Huystee R.B.: Rapid simultaneous estimation of protoporphyrin and Mg-porphyrins in higher plants. — J. Plant Physiol. 125: 311–323, 1986.

    Article  CAS  Google Scholar 

  • Horn R., Grundmann G., Paulsen H.: Consecutive binding of chlorophylls a and b during the assembly in vitro of light harvesting chlorophyll a/b protein (LHCII b). — J. Mol. Biol. 366: 1045–1054, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Hörtensteiner S.: Update on the biochemistry of chlorophyll breakdown. — Plant Mol. Biol. 82: 505–517, 2013.

    Article  PubMed  Google Scholar 

  • Horton P., Ruban A.: Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. — J. Exp. Bot. 56: 365–373, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Hu X., Zhang Y., Shi Y. et al.: Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity-alkalinity mixed stress. — Plant Physiol. Bioch. 57: 200–209, 2012.

    Article  CAS  Google Scholar 

  • Ioannidis N.E., Kotzabasis K.: Effects of polyamines on the functionality of photosynthetic membrane in vivo and in vitro. — BBA-Bioenergetics 1767: 1372–1382, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Jennings R.C., Bassi R., Garlaschi F.M. et al.: Distribution of the chlorophyll spectral forms in the chlorophyll-protein complexes of photosystem II antenna. — Biochemistry-US 32: 3203–3210, 2015.

    Article  Google Scholar 

  • Jia T., Ito H., Tanaka A.: The chlorophyll b reductase NOL participates in regulating the antenna size of photosystem II in Arabidopsis thaliana. — Procedia Chem. 14: 422–427, 2015.

    Article  CAS  Google Scholar 

  • Johnson M.P., Havaux M., Triantaphylidès et al.: Elevated zeaxanthin bound to oligomeric LHCII enhances the resistance of Arabidopsis to photooxidative stress by a lipid-protective, antioxidant mechanism. — J. Biol. Chem. 282: 22605–22618, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Li J., Hu L., Zhang L. et al.: Exogenous spermidine is enhancing tomato tolerance to salinity. — alkalinity stress by regulating chloroplast antioxidant system and chlorophyll metabolism. — BMC Plant Biol. 15: 1–17, 2015.

    Article  Google Scholar 

  • Li X., Zhao W., Sun X. et al.: Molecular cloning and characterization of violaxanthin de-epoxidase (CsVDE) in cucumber. — PLoS ONE 8: 64383, 2013.

    Article  Google Scholar 

  • Li X.G., Meng Q.W., Jiang G.Q. et al.: The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. — Photosynthetica 41: 259–265, 2003.

    Article  CAS  Google Scholar 

  • Masuda T., Tanaka A., Melis A.: Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. — Plant Mol. Biol. 51: 757–771, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Moran R.: Formulae for determination of chlorophyllous pigments extracted with N,N-dimethylformamide. — Plant Physiol. 69:1376–1381, 1982.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parihar P., Singh S., Singh R. et al.: Effect of salinity stress on plants and its tolerance strategies: a review. — Environ. Sci. Pollut. R. 22: 4056–4075, 2015.

    Article  CAS  Google Scholar 

  • Porra R.J.: Recent progress in porphyrin and chlorophyll biosynthesis. — Photochem. Photobiol. 65: 492–516, 1997.

    Article  CAS  Google Scholar 

  • Pružinská A., Anders I., Aubry S. et al.: In vivo participation of red chlorophyll catabolite reductase in chlorophyll breakdown. — Plant Cell 19: 369–387, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rimington C.: Spectral-absorption coefficients of some porphyrins in the Soret-band region. — Biochem. J. 75: 620–623, 1960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sáez P.L., Bravo L.A., Latsague M.I.: Light energy management in micropropagated plants of Castanea sativa, effects of photoinhibition. — Plant Sci. 201: 12–24, 2013.

    Article  PubMed  Google Scholar 

  • Sato R., Ito H., Tanaka A.: Chlorophyll b degradation by chlorophyll b reductase under high-light conditions. — Photosynth. Res. 126: 249–259, 2015.

    Article  CAS  PubMed  Google Scholar 

  • Sato Y., Morita R., Katsuma S. et al.: Two short-chain dehydrogenase/reductases, NON-YELLOW COLORING 1 and NYC1-LIKE, are required for chlorophyll b and lightharvesting complex II degradation during senescence in rice. — Plant J. 57: 120–131, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Shu S., Yuan L.Y., Guo S.R. et al.: Effects of exogenous spermidine on photosynthesis, xanthophyll cycle and endogenous polyamines in cucumber seedlings exposed to salinity. — Afr. J. Biotechnol. 11: 6064–6074, 2012.

    CAS  Google Scholar 

  • Tanaka A., Tanaka R.: Chlorophyll metabolism. — Curr. Opin. Plant Biol. 9: 248–255,2006.

    Article  CAS  PubMed  Google Scholar 

  • Wang H.Y., Tang X.L., Wang H.L. et al.: Physiological responses of Kosteletzkya virginica to coastal wetland soil. — Sci. World J. 2015: 1–9, 2015.

    Google Scholar 

  • Yao N., Greenberg J.T.: Arabidopsis ACCELERATED CELL DEATH 2 modulates programmed cell death. — Plant Cell 18: 397–411, 2006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan Y.H., Zhong M., Shu S. et al.: Effects of exogenous putrescine on leaf anatomy and carbohydrate metabolism in cucumber (Cucumis sativus L.) under salt stress. — J. Plant Growth Regul. 34: 451–464, 2015.

    Article  CAS  Google Scholar 

  • Zhong M., Yuan Y.H., Shu S. et al.: Effects of exogenous putrescine on glycolysis and Krebs cycle metabolism in cucumber leaves subjected to salt stress. — Plant Growth Regul. 79: 319–330, 2016.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    R. N. Yuan, S. Shu, S. R. Guo, J. Sun & J. Q. Wu

  2. Nanjing Agricultural University (Suqian) Academy of Protected Horticulture, Suqian, 223800, China

    S. R. Guo & J. Sun

Authors
  1. R. N. Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. R. Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Q. Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. R. Guo.

Additional information

Acknowledgements: This work was funded by the National Natural Science Foundation of China (No. 31471869, No. 31672199 and No. 31401919) and the Jiangsu Province Scientific and Technological Achievements into Special Fund (BA2014147) and was sponsored by the China Agriculture Research System (CARS-25-C-03).

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yuan, R.N., Shu, S., Guo, S.R. et al. The positive roles of exogenous putrescine on chlorophyll metabolism and xanthophyll cycle in salt-stressed cucumber seedlings. Photosynthetica 56, 557–566 (2018). https://doi.org/10.1007/s11099-017-0712-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-017-0712-5

Additional key words

Search

Navigation