Skip to main content
SpringerLink
Log in

Differential blockage of photosynthetic electron flow in young and mature leaves of Arabidopsis thaliana by exogenous proline

  • Original Papers
  • Published:
Photosynthetica

Abstract

Responses of the photosynthetic electron transport system of chloroplasts to exogenous proline application were evaluated in young and mature leaves of Arabidopsis thaliana plants under optimal growth conditions. Exogenous proline application (10 mM) during the 4th week of growth increased proline accumulation in young leaves more than in mature leaves, and possibly due to its degradation producing NADPH, decreased significantly the ratio of NADP+/NADPH in both leaf types compared with controls (without proline). However, the ratio of NADP+/NADPH remained significantly higher in the young leaves, suggesting lower proline degradation which resulted in less reduced plastoquinone pool than that in the mature leaves, under both low light [130 μmol(photon) m−2 s−1] and high light [1,200 μmol(photon) m−2 s−1] treatments. The young leaves seemed to adjust nonphotochemical fluorescence quenching in order to maintain a better PSII quantum yield. We concluded that under optimal growth conditions exogenous proline results in overreduction of the plastoquinone pool and blockage of photosynthetic electron flow due to accumulation of NADPH. We suggest that optimum concentrations of proline are required for optimal PSII photochemistry.

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

AL:

actinic light

AOI:

area of interest

Chl:

chlorophyll

ETR:

electron transport rate

F0, Fm :

minimal and maximal chlorophyll a fluorescence of the dark-adapted state

F0′, Fm′:

minimal and maximal chlorophyll a fluorescence of the light-adapted state

Fs :

steady-state photosynthesis at a given actinic light

Fv/Fm :

potential (maximal) quantum yield of PSII photochemistry

HL:

high light

LL:

low light

ML:

mature leaves

NPQ:

nonphotochemical quenching

P5C:

Δ1-pyrroline-5-carboxylate

P5CDH:

Δ1-pyrroline-5-carboxylate dehydrogenase

P5CR:

Δ1-pyrroline-5-carboxylate reductase

P5CS:

Δ1-pyrroline-5-carboxylate synthase

PDH:

proline dehydrogenase

PQ:

plastoquinone

Pro:

proline

qP :

photochemical quenching coefficient

ROS:

reactive oxygen species

YL:

young leaves

ΦPSII :

actual (effective) quantum yield of PSII photochemistry

References

  • Ashraf M., Foolad M.R.: Roles of glycine betaine and proline in improving plant abiotic stress resistance. — Environ. Exp. Bot. 59: 206–216, 2007.

    Article  CAS  Google Scholar 

  • Bates L.S., Waldren R.P., Teare I.D.: Rapid determination of free proline for water stress studies. — Plant Soil 39: 205–207, 1973.

    Article  CAS  Google Scholar 

  • Bukhov N., Egorova E., Carpentier R.: Electron flow to photosystem I from stromal reductants in vivo: the size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units. — Planta 215: 812–820, 2002.

    Article  CAS  PubMed  Google Scholar 

  • Chen T.H., Murata N.: Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. — Curr. Opin. Plant Biol. 5: 250–257, 2002.

    Article  CAS  PubMed  Google Scholar 

  • De Ronde J.A., Cress W.A., Krüger G.H.J. et al.: Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. — J. Plant Physiol. 161: 1211–1224, 2004.

    Article  PubMed  Google Scholar 

  • Deuschle K., Funck D., Hellmann H. et al.: A nuclear gene encoding mitochondrial Δ1-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. — Plant J. 27: 345–356, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Deuschle K., Funck D., Forlani G. et al.: The role of Δ1-pyrroline-5-carboxylate dehydrogenase in proline degradation. — Plant Cell 16: 3413–3425, 2004.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dietz K.J., Pfannschmidt T.: Novel regulators in photosynthetic redox control of plant metabolism and gene expression. — Plant Physiol. 155: 1477–1485, 2011.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Endo T., Schreiber U., Asada K.: Suppression of quantum yield of photosystem II by hyperosmotic stress in Chlamydomonas reinhardtii. — Plant Cell Physiol. 36: 1253–1258, 1995.

    CAS  Google Scholar 

  • Foyer C.H., Neukermans J., Queval G. et al.: Photosynthetic control of electron transport and the regulation of gene expression. — J. Exp. Bot. 63:1637–1661, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Funck D., Eckard S., Müller G.: Non-redundant functions of two proline dehydrogenase isoforms in Arabidopsis. — BMC Plant Biol. 10: 70, 2010.

    Article  PubMed Central  PubMed  Google Scholar 

  • Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. — Biochim. Biophys. Acta 990: 87–92, 1989.

    Article  CAS  Google Scholar 

  • Gorbe E., Calatayud A.: Applications of chlorophyll fluorescence imaging technique in horticultural research: a review. — Sci. Hortic.-Amsterdam 138: 24–35, 2012.

    Article  CAS  Google Scholar 

  • Guidi L., Calatayud A.: Non-invasive tools to estimate stressinduced changes in photosynthetic performance in plants inhabiting Mediterranean areas. — Environ. Exp. Bot. 103: 42–52, 2014.

    Article  CAS  Google Scholar 

  • Hald S., Nandha B., Gallois P. et al.: Feedback regulation of photosynthetic electron transport by NADP(H) redox poise. — Biochim. Biophys. Acta 1777: 433–440, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Hanachi S., Van Labeke M.C., Mehouachi T.: Application of chlorophyll fluorescence to screen eggplant (Solanum melongena L.) cultivars for salt tolerance. — Photosynthetica 52: 57–62, 2014.

  • Hare P.D., Cress W.A.: Metabolic implications of stress-induced proline accumulation in plants. — Plant Growth Regul. 21: 79–102, 1997.

    Article  CAS  Google Scholar 

  • Hare P.D., Cress W.A., Van Staden J.: Dissecting the roles of osmolyte accumulation during stress. — Plant Cell Environ. 21: 535–553, 1998.

    Article  CAS  Google Scholar 

  • Hare P.D., Cress W.A., Van Staden J.: Disruptive effects of exogenous proline on chloroplast and mitochondrial ultrastructure in Arabidopsis leaves. — S. Afr. J. Bot. 68: 393–396, 2002.

    Article  CAS  Google Scholar 

  • Havaux M.: Short-term responses of photosystem I to heat stress. — Photosynth. Res. 47: 85–97, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Havaux M., Dall’Osto L., Bassi R.: Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae. — Plant Physiol. 145: 1506–1520, 2007.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hellmann H., Funck D., Rentsch D. et al.: Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. — Plant Physiol. 123: 779–789, 2000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hong Z.L., Lakkineni K., Zhang Z.M. et al.: Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. — Plant Physiol. 122: 1129–1136, 2000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Khayyat M., Tehranifar A., Davarynejad G.H. et al.: Vegetative growth, compatible solute accumulation, ion partitioning and chlorophyll fluorescence of ‘Malas-e-Saveh’ and ’shishe-Kab’ pomegranates in response to salinity stress. — Photosynthetica 52: 301–312, 2014.

  • Krause G.H., Weis E.: Chlorophyll fluorescence and photosynthesis: the basics. — Annu. Rev. Plant Phys. 42: 313–349, 1991.

    Article  CAS  Google Scholar 

  • Mani S., Van de Cotte B., Van Montagu M. et al.: Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. — Plant Physiol. 128: 73–83, 2002.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marutani Y., Yamauchi Y., Kimura Y. et al.: Damage to photosystem II due to heat stress without light-driven electron flow: involvement of enhanced introduction of reducing power into thylakoid membranes. — Planta 236: 753–761, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Morales F., Moise N., Quílez R. et al.: Iron deficiency interrupts energy transfer from a disconnected part of the antenna to the rest of Photosystem II. — Photosynth. Res. 70: 207–220, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Moustakas M., Sperdouli I., Kouna T. et al.: Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem II functioning of Arabidopsis thaliana leaves. — Plant Growth Regul. 65: 315–325, 2011.

    Article  CAS  Google Scholar 

  • Murchie E.H., Lawson T.: Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. — J. Exp. Bot. 64: 3983–3998, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K., Satoh R., Kiyosue T. et al.: A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis. — Plant Physiol. 118: 1233–1241, 1998.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nanjo T., Fujita M., Seki M. et al.: Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. — Plant Cell Physiol. 44: 541–548, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Ögren E.: Evaluation of chlorophyll fluorescence as a probe for drought stress in willow leaves. — Plant Physiol. 93: 1280–1285, 1990.

    Article  PubMed Central  PubMed  Google Scholar 

  • Osório M.L., Osório J., Romano A.: Photosynthesis, energy partitioning, and metabolic adjustments of the endangered Cistaceae species Tuberaria major under high temperature and drought — Photosynthetica 51: 75–84, 2013.

    Article  Google Scholar 

  • Osório J., Osório M.L., Correia P.J. et al.: Chlorophyll fluorescence imaging as a tool to understand the impact of iron deficiency and resupply on photosynthetic performance of strawberry plants. — Sci. Hortic.-Amsterdam 165: 148–155, 2014.

    Article  Google Scholar 

  • Peng Z., Lu Q., Verma D.P.S.: Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. — Mol. Gen. Genet. 253: 334–341, 1996.

    CAS  PubMed  Google Scholar 

  • Petrillo E., Godoy Herz M.A., Fuchs A. et al.: A chloroplast retrograde signal regulates nuclear alternative splicing. — Science 344: 427–430, 2014.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Poulson M.E., Boeger M.R.T., Donahue R.A.: Response of photosynthesis to high light and drought for Arabidopsis thaliana grown under a UV-B enhanced light regime. — Photosynth. Res. 90: 79–90, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Rius S.P., Casati P., Iglesias A.A. et al.: Characterization of an Arabidopsis thaliana mutant lacking a cytosolic nonphosphorylating glyceraldehyde-3-phosphate dehydrogenase. — Plant Mol. Biol. 61: 945–957, 2006.

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U., Bilger W., Neubauer C.: Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. — In: Schulze E.D., Caldwell M.M. (ed.): Ecophysiology of Photosynthesis. Ecological Studies, vol. 100. Pp. 49–70. Springer, Berlin 1994.

    Google Scholar 

  • Sperdouli I., Moustakas M.: Spatio-temporal heterogeneity in Arabidopsis thaliana leaves under drought stress. — Plant Biol. 14: 118–128, 2012a.

    CAS  PubMed  Google Scholar 

  • Sperdouli I., Moustakas M.: Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. — J. Plant Physiol. 169: 577–585, 2012b.

    Article  CAS  PubMed  Google Scholar 

  • Sperdouli I., Moustakas M.: A better energy allocation of absorbed light in photosystem II and less photooxidative damage contribute to acclimation of Arabidopsis thaliana young leaves to water deficit. — J. Plant Physiol. 171: 587–593, 2014a.

    Article  CAS  PubMed  Google Scholar 

  • Sperdouli I., Moustakas M.: Leaf developmental stage modulates metabolite accumulation and photosynthesis contributing to acclimation of Arabidopsis thaliana to water deficit. — J. Plant Res. 127: 481–489, 2014b.

    Article  CAS  PubMed  Google Scholar 

  • Szabados L., Savouré A.: Proline: a multifunctional amino acid. — Trends Plant Sci. 15: 89–97, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Székely G., Ábrahám E., Cséplő Á. et al.: Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. — Plant J. 53: 11–28, 2008.

    Article  PubMed  Google Scholar 

  • Triantaphylidès C., Krischke M., Hoeberichts F.A. et al.: Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. — Plant Physiol. 148: 960–968, 2008.

    Article  PubMed Central  PubMed  Google Scholar 

  • Verbruggen N., Hermans C.: Proline accumulation in plants: a review. — Amino Acids 35: 753–759, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto Y., Aminaka R., Yoshioka M. et al.: Quality control of photosystem II: impact of light and heat stresses. — Photosynth. Res. 98: 589–608, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z., Yu J., Stanton R.: A method for determination of pyridine nucleotides using a single extract. — Anal. Biochem. 285: 163–167, 2000.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botany, School of Biology, Aristotle University of Thessaloniki, University Campus, 54124, Thessaloniki, Greece

    I. Sperdouli & M. Moustakas

Authors
  1. I. Sperdouli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Moustakas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Moustakas.

Additional information

Acknowledgements: This work was supported by funds of the Aristotle University of Thessaloniki.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sperdouli, I., Moustakas, M. Differential blockage of photosynthetic electron flow in young and mature leaves of Arabidopsis thaliana by exogenous proline. Photosynthetica 53, 471–477 (2015). https://doi.org/10.1007/s11099-015-0116-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-015-0116-3

Additional key words

Search

Navigation