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Different responses of photosystem I and photosystem II in three tropical oilseed crops exposed to chilling stress and subsequent recovery

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Different responses of photosystem I and II to chilling.

Abstract

Tropical crops are sensitive to chilling stress, but the underlying physiological mechanisms are unclear. We investigated the maximum quantum yield of PSII (F v/F m), the maximum photo-oxidizable P700 (P m), the energy distribution in PSII, and the redox state of P700 in leaves of seedlings of three promising oilseed crops originating from tropical regions, Plukenetia volubilis, Jatropha curcas and Ricinus communis, during chilling treatment and subsequent recovery under a photon flux density of 450 μmol m−2 s−1. Our results showed that F v/F m decreased progressively and significantly to about 44.7, 62.2 and 77.0 % of the control after chilling treatment for 3 days in P. volubilis, J. curcas and R. communis, respectively, mainly due to the decrease in F m (maximum fluorescence of PSII). After recovery under 18 °C for 6 days, F v/F m recovered to 81.4 and 94.9 % of the control in J. curcas and R. communis, but only to 26.3 % in P. volubilis. Under chilling stress and subsequent recovery, P m remained stable in J. curcas and R. communis, whereas it decreased slightly in P. volubilis. These results indicated that PSII was more sensitive to chilling stress than PSI under moderate light for all three species, and that P. volubilis was the most susceptible. Cyclic electron flow around PSI and effective quantum yield of photosystem II [Y (CEF)/Y (II)] ratio were stimulated much more in J. curcas and R. communis compared with that in P. volubilis under chilling conditions, resulting in more severe injury as indicated by higher accumulation of hydrogen peroxide and malondialdehyde. There was a significantly negative relationship between F v/F m and Y (CEF)/Y (II), suggesting that stimulation of Y (CEF)/Y (II) plays a pivotal role in protecting PSI and PSII from photoinhibition caused by chilling stress.

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Abbreviations

A growth :

Actual photosynthetic rate under growth condition (μmol m−2 s−1)

A max :

Light-saturated photosynthetic rate (μmol m−2 s−1)

CEF:

Cyclic electron flow

G s and G smax :

Stomatal conductance under growth and light-saturated light, respectively (mol m−2 s−1)

H2O2 :

Hydrogen peroxide (μmol g−1)

F v/F m :

The maximum quantum yield of PSII

LEF:

Linear electron flow

MDA:

Malondialdehyde (nmol g−1)

NPQ:

Non-photochemical quenching

PSI:

Photosystem I

PSII:

Photosystem II

ROS:

Reactive oxygen species

Y (I) :

Effective quantum yield of photosystem I

Y (II) :

Effective quantum yield of photosystem II

Y (NA) :

Fraction of overall PSI reaction center P700 that cannot be oxidized in a given state

Y (ND) :

Fraction of overall PSI reaction center P700 that is oxidized in a given state

Y (NO) :

Fraction of energy that is passively dissipated in form of heat and fluorescence

Y (NPQ) :

Fraction of energy dissipated in form of heat via the regulated non-photochemical quenching mechanism

References

  • Achten WMJ, Verchot L, Franken YJ, Mathijs E, Singh VP, Aerts R, Muys B (2008) Jatropha bio-diesel production and use. Biomass Bioenerg 32:1063–1084

    Article  CAS  Google Scholar 

  • Allen DJ, Ort DR (2011) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–42

    Article  Google Scholar 

  • Almoguera C, Prieto-Dapena P, Personat J-M, Tejedor-Cano J, Lindahl M, Diaz-Espejo A, Jordano J (2012) Protection of the photosynthetic apparatus from extreme dehydration and oxidative stress in seedlings of transgenic tobacco. PLoS One 7:e51443

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brennan T, Frenkel C (1977) Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiol 59:411–416

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Briantais JM, Dacosta J, Goulas Y, Ducruet JM, Moya I (1996) Heat stress induces in leaves an increase of the minimum level of chlorophyll fluorescence, F o: a time-resolved analysis. Photosynth Res 48:189–196

    Article  CAS  PubMed  Google Scholar 

  • Cai ZQ (2011) Shade delayed flowering and decreased photosynthesis, growth and yield of Sacha Inchi (Plukenetia volubilis) plants. Ind Crop Prod 34:1235–1237

    Article  Google Scholar 

  • Cai ZQ, Jiao DY, Tang SX, Dao XS, Lei YB, Cai CT (2012) Leaf photosynthesis, growth and seed chemicals of Sacha Inchi (Plukenetia volubilis) plants cultivated along an altitude gradient. Crop Sci 52:1859–1867

    Article  CAS  Google Scholar 

  • Danon A (2012) Environmentally-induced oxidative stress and its signaling. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Advances in photosynthesis and respiration (Govindjee and Sharkey TD, Series eds), vol 34. Springer, Dordrecht, pp 319–330

    Chapter  Google Scholar 

  • Glover JD, Reganold JP, Bell LW, Borevitz J, Brummer EC, Buckler ES, Cox CM, Cox TS, Crews TE, Culman SW, DeHaan LR, Eriksson D, Gill BS, Holland J, Hu F, Hulke BS, Ibrahim AMH, Jackson W, Jones SS, Murray SC, Paterson AH, Ploschuk E, Sacks EJ, Snapp S, Tao D, van Tassel DL, Wade LJ, Wyse DL, Xu Y (2010) Increased food and ecosystem security via perennial grains. Science 25:1638–1639

    Article  Google Scholar 

  • Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107–114

    Article  CAS  PubMed  Google Scholar 

  • Govindachary S, Bukhov NG, Joly D, Carpentier R (2004) Photosystem II inhibition by moderate light under low temperature in intact leaves of chilling-sensitive and -tolerant plants. Physiol Plant 121:322–333

    Article  CAS  PubMed  Google Scholar 

  • Gui MM, Lee KT, Bahatia S (2008) Feasibility of edible oil vs. non-edible oil vs. waste edible oil as biodiesel feedstock. Energy 33:1646–1653

    Article  CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2010) The different effects of chilling stress under moderate light intensity on photosystem II compared with photosystem I and subsequent recovery in tropical tree species. Photosynth Res 103:173–182

    Article  Google Scholar 

  • Huang W, Zhang SB, Cao KF (2011) Cyclic electron flow plays an important role in photoprotection of tropical trees illuminated at temporal chilling temperature. Plant Cell Physiol 52:297–305

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Yang SJ, Zhang SB, Zhang JL, Cao KF (2012) Cyclic electron flow plays an important role in photoprotection for the resurrection plant Paraboea rufescens under drought stress. Planta 235:819–828

    Article  CAS  PubMed  Google Scholar 

  • Ivanov AG, Morgan RM, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292

    Article  CAS  PubMed  Google Scholar 

  • Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 180:384–389

    Article  Google Scholar 

  • Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proc Natl Acad Sci USA 108:13317–13322

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaniuga Z (2008) Chilling response of plants: importance of galactolipase, free fatty acids and free radicals. Plant Biol 10:171–184

    Article  CAS  PubMed  Google Scholar 

  • Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192:261–268

    Article  CAS  Google Scholar 

  • Kornyeyev D, Logan BA, Allen RD, Holaday AS (2003) Effect of chloroplastic overproduction of ascorbate peroxidase on photosynthesis and photoprotection in cotton leaves subjected to low temperature photoinhibition. Plant Sci 165:1033–1041

    Article  CAS  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Krumova SB, Laptenok SP, Kovacs L, Toth T, van Hoek A, Garab G, van Amerongen H (2010) Digalactosyl-diacylglycerol-deficiency lowers the thermal stability of thylakoid membranes. Photosynth Res 105:229–242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kudoh H, Sonoike K (2002) Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. Planta 215:541–548

    Article  CAS  PubMed  Google Scholar 

  • Laisk A, Talts E, Oja V, Eichelmann H, Peterson RB (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95

    Article  CAS  PubMed  Google Scholar 

  • Madankar CS, Pradhan S, Naik SN (2013) Parametric study of reactive extraction of castor seed (Ricinus communis L.) for methyl ester production and its potential use as bio-lubricant. Ind Crop Prod 43:283–290

    Article  CAS  Google Scholar 

  • Mai J, Herbette S, Vandame M, Kositsup B, Kasemsap P, Cavaloc E, Jelien JL, Ameglio T, Roeckel-Drevet P (2009) Effect of chilling on photosynthesis and antioxidant enzymes in Hevea brasiliensis Muell. Arg. Trees 23:863–874

    Article  CAS  Google Scholar 

  • Millaleo R, Reyes-Diaz M, Alberdi M, Ivanov AG, Krol M, Huner NPA (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Exp Bot 64:343–354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miyake C (2010) Alternative electron flow (water–water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, Tomizawa K (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830

    Article  CAS  PubMed  Google Scholar 

  • Murchie EH, Niyogi KK (2011) Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 155:86–92

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakano R, Ishida H, Kobayashi M, Makino A, Mae T (2010) Biochemical changes associated with in vivo RbcL fragmentation by reactive oxygen species under chilling-light conditions. Plant Biol 12:35–45

    Article  CAS  PubMed  Google Scholar 

  • Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568

    Article  CAS  PubMed  Google Scholar 

  • Nishiyama Y, Allakhverdiev SI, Nurata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749

    Article  CAS  PubMed  Google Scholar 

  • Okegawa Y, Kagawa Y, Kobayashi Y, Shikanai T (2008) Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol 49:825–834

    Article  CAS  PubMed  Google Scholar 

  • Ramalho JC, Campos PS, Quartin VL, Silva MJ, Nunes MA (1999) High irradiance impairments on photosynthetic electron transport, ribulose-1,5-bisphosphate carboxylase/oxygenase and N assimilation as a function of N availability in Coffea arabica L. plants. J Plant Physiol 154:319–326

    Article  CAS  Google Scholar 

  • Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K, Terashima I (1994) Mechanism of the photosystem I photoinhibition in leaves of Cucumis sativus L. Planta 194:287–293

    Article  CAS  Google Scholar 

  • Takahashi H, Clowez S, Wollman FA, Vallon O, Rappaport F (2013) Cyclic electron flow is redox-controlled but impendent of state transition. Nat Commun. doi:10.1038/ncomms2954 (in press)

    Google Scholar 

  • Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306

    Article  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  PubMed  Google Scholar 

  • Tovuu A, Zulfugarov IS, Lee CH (2013) Correlations between the temperature dependence of chlorophyll fluorescence and the fluidity of thylakoid membranes. Physiol Plant 147:409–416

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Chinese Academy of Sciences (Nos. KSCX2EWQ17, KSCX2EWZ15, SDSQB201201), and the National Science Foundation in China (Nos. 31370607, 31370684).

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, 610041, China

    Yan-bao Lei & Bao-li Duan

  2. Key Laboratory of Tropical Plant Resource and Sustainable Use, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, 666303, China

    Yan-bao Lei, Yu-long Zheng & Zhi-quan Cai

  3. Kunming Branch, Chinese Academy of Sciences, Kunming, 650204, China

    Kai-jie Dai

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  1. Yan-bao Lei
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  2. Yu-long Zheng
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Correspondence to Zhi-quan Cai.

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Communicated by W. Bilger.

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Lei, Yb., Zheng, Yl., Dai, Kj. et al. Different responses of photosystem I and photosystem II in three tropical oilseed crops exposed to chilling stress and subsequent recovery. Trees 28, 923–933 (2014). https://doi.org/10.1007/s00468-014-1007-0

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