Effects of low temperature stress on excitation energy partitioning and photoprotection in Zea mays
Leonid V. Savitch A D E , Alexander G. Ivanov B D , Loreta Gudynaite-Savitch B C , Norman P. A. Huner B and John Simmonds AA Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Centre (ECORC), Central Experimental Farm, 960 Carling Avenue, Ottawa, ON K1A 0C6, Canada.
B Department of Biology, University of Western Ontario, London, ON N6A 5B7, Canada.
C Present address: Iogen Corporation, 310 Hunt Club Road East, Ottawa, ON K1V 1C1, Canada.
D These authors contributed equally to the writing of this manuscript.
E Corresponding author. Email: savitchl@agr.gc.ca
Functional Plant Biology 36(1) 37-49 https://doi.org/10.1071/FP08093
Submitted: 21 March 2008 Accepted: 4 October 2008 Published: 7 January 2009
Abstract
Analysis of the partitioning of absorbed light energy within PSII into fractions utilised by PSII photochemistry (ΦPSII), thermally dissipated via ΔpH- and zeaxanthin-dependent energy quenching (ΦNPQ) and constitutive non-photochemical energy losses (Φf,D) was performed in control and cold-stressed maize (Zea mays L.) leaves. The estimated energy partitioning of absorbed light to various pathways indicated that the fraction of ΦPSII was twofold lower, whereas the proportion of thermally dissipated energy through ΦNPQ was only 30% higher, in cold-stressed plants compared with control plants. In contrast, Φf,D, the fraction of absorbed light energy dissipated by additional quenching mechanism(s), was twofold higher in cold-stressed leaves. Thermoluminescence measurements revealed that the changes in energy partitioning were accompanied by narrowing of the temperature gap (ΔTM) between S2/3QB− and S2QA− charge recombinations in cold-stressed leaves to 8°C compared with 14.4°C in control maize plants. These observations suggest an increased probability for an alternative non-radiative P680+QA− radical pair recombination pathway for energy dissipation within the reaction centre of PSII in cold-stressed maize plants. This additional quenching mechanism might play an important role in thermal energy dissipation and photoprotection when the capacity for the primary, photochemical (ΦPSII) and zeaxanthin-dependent non-photochemical quenching (ΦNPQ) pathways are thermodynamically restricted in maize leaves exposed to cold temperatures.
Additional keywords: cold stress, non-photochemical quenching, PSII photochemistry, thermoluminescence.
Acknowledgements
This work was supported by the OCPA/AAFC Matching Investment Initiative, the Canadian Crops Genomics Initiative and NSERC Canada.
Anderson JM,
Woo KC, Bordman NK
(1971) Photochemical system in mesophyll and bundle sheath chloroplasts of C4 plants. Biochimica et Biophysica Acta 245, 398–408.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Andrews JR,
Fryer MJ, Baker NR
(1995) Characterization of chilling effects on photosynthetic performance of maize crops during early season growth using chlorophyll fluorescence. Journal of Experimental Botany 46, 1195–1203.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Aro E-M,
Virgin I, Andersson B
(1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113–134.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Asada K,
Heber U, Schreiber U
(1993) Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as determined in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant & Cell Physiology 34, 39–50.
|
CAS |
Cailly AL,
Rizza F,
Genty B, Harbinson J
(1996) Fate of excitation at PSII in leaves. The non-photochemical side. Plant Physiology and Biochemistry (special issue), 86.
Cao J, Govindjee
(1990) Chlorophyll a fluorescence transients as an indicator of active and inactive Photosystem II in thylakoid membranes. Biochimica et Biophysica Acta 1015, 180–188.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chylla RA, Whitmarsh J
(1989) Inactive photosystem II complexes in leaves. Turnover rate and quantitation. Plant Physiology 90, 765–772.
|
CAS |
Crossref |
PubMed |
Darie CC,
Biniossek ML,
Winter V,
Mutschler B, Haehnel W
(2005) Isolation and structural characterization of the Ndh complex from mesophyll and bundle sheath chloroplasts of Zea mays. FEBS Journal 272, 2705–2716.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Demmig-Adams B, Adams WW
(1992) Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43, 599–626.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Demmig-Adams B,
Adams WW,
Barker DH,
Logan BA,
Bowling RD, Verhoeven AS
(1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiologia Plantarum 98, 253–264.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
DeVault D, Govindjee
(1990) Photosynthetic glow peaks and their relationship with the free-energy changes. Photosynthesis Research 24, 175–181.
|
CAS |
Diaz M,
Ball E, Lüttge U
(1990) Stress-induced accumulation of the xanthophyll rhodoxanthin in leaves of Aloe vera. Plant Physiology and Biochemistry 28, 679–682.
|
CAS |
Ducruet J-M
(2003) Chlorophyll thermoluminescence of leaf discs: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators. Journal of Experimental Botany 54, 2419–2430.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ducruet J-M,
Peeva V, Havaux M
(2007) Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynthesis Research 93, 159–171.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Etienne A-L,
Ducruet J-M,
Ajilani G, Vernotte C
(1990) Comparative studies on electron transfer in photosystem II of herbicide resistant mutants from different organisms. Biochimica et Biophysica Acta 1015, 435–440.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Finazzi G,
Johnson GN,
Dall’Osto L,
Joliot P,
Wollman F-A, Bassi R
(2004) A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proceedings of the National Academy of Sciences of the United States of America 101, 12375–12380.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Foyer CH,
Vanacker H,
Gomez LD, Harbinson J
(2002.) Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures. Plant Physiology and Biochemistry 40, 659–668.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Fracheboud Y,
Haldimann P,
Leipner J, Stamp P
(1999) Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). Journal of Experimental Botany 50, 1533–1540.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Fryer MJ,
Oxborough K,
Martin B,
Ort DR, Baker NR
(1995) Factors associated with depression of photosynthetic quantum efficiency in maize at low growth temperature. Plant Physiology 108, 761–767.
|
CAS |
PubMed |
Fryer MJ,
Andrews JR,
Oxborough K,
Blowers DA, Baker NR
(1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiology 116, 571–580.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Giersch C, Krause GH
(1991) A simple model relating photoinhibitory fluorescence quenching in chloroplasts to a population of altered photosystem II reaction centers. Photosynthesis Research 30, 115–121.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Govindjee
,
Eggenberg P,
Pfister K, Strasser RJ
(1992) Chlorophyll a fluorescence decay in herbicide-resistant D1 mutants of Chlamydomonas reinhardtii and the formate effects. Biochimica et Biophysica Acta 1101, 353–358.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gray GR,
Savitch LV,
Ivanov AG, Hüner NPA
(1996) Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiology 110, 61–71.
|
CAS |
PubMed |
Greer DH, Hardacre AK
(1989) Photoinhibition of photosynthesis and its recovery in two maize hybrids varying in low temperature tolerance. Australian Journal of Plant Physiology 16, 189–198.
| Crossref | GoogleScholarGoogle Scholar |
Haldimann P
(1997) Chilling-induced changes to carotenoid composition, photosynthesis and the maximum quantum yield of photosystem II photochemistry in two maize genotypes differing in tolerance to low temperature. Journal of Plant Physiology 151, 610–619.
|
CAS |
Haldimann P
(1998) Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays genotypes differing in chilling sensitivity. Plant, Cell & Environment 21, 200–208.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Haldimann P,
Fracheboud Y, Stamp P
(1995) Carotenoid composition in Zea mays developed at sub-optimal temperature and different light intensities. Physiologia Plantarum 95, 409–414.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Haldimann P,
Fracheboud Y, Stamp P
(1996) Photosynthetic performance and resistance to photoinhibition of Zea mays L. leaves grown at suboptimal temperature. Plant, Cell & Environment 19, 85–92.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Havaux M
(1987) Effects of chilling on the redox state of the primary electron acceptor QA of photosystem II in chilling-sensitive and resistant plant species. Plant Physiology and Biochemistry 25, 735–743.
Hendrickson L,
Furbank RT, Chow WS
(2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynthesis Research 82, 73–81.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hendrickson L,
Föorster B,
Pogson BJ, Chow WS
(2005) A simple chlorophyll fluorescence parameter that correlates with the rate coefficient of photoinactivation of photosystem II. Photosynthesis Research 84, 43–49.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hikosaka K,
Kato MC, Hirose T
(2004) Photosynthetic rates and partitioning of absorbed light energy in photosynthetic leaves. Physiologia Plantarum 121, 699–708.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Horton P, Hegen A
(1988) Studies on the induction of chlorophyll fluorescence in barley protoplasts. IV. Resolution of non-photochemical quenching. Biochimica et Biophysica Acta 932, 107–115.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Horton P,
Ruban AV, Walters RG
(1996) Regulation of light harvesting in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 655–684.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hovenden MJ, Warren CR
(1998) Photochemistry, energy dissipation and cold-hardening in Eucaliptus nitens and E. pauciflora. Australian Journal of Plant Physiology 25, 581–589.
| Crossref | GoogleScholarGoogle Scholar |
Huner NPA,
Maxwell DP,
Gray GR,
Savitch LV,
Krol M,
Ivanov AG, Falk S
(1996) Sensing environmental change: PSII excitation pressure and redox signalling. Physiologia Plantarum 98, 358–364.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Huner NPA,
Öquist G, Sarhan F
(1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224–230.
| Crossref | GoogleScholarGoogle Scholar |
Ivanov B, Edwards GE
(1997) Electron flow accompanying the ascorbate peroxidase cycle in maize mesophyll chloroplasts and its cooperation with linear electron flow to NADP+ and cyclic electron flow in thylakoid membrane energization. Photosynthesis Research 52, 187–198.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ivanov B, Edwards GE
(2000) Influence of ascorbate and the Mehler peroxidase reaction on non-photochemical quenching of chlorophyll fluorescence in maize mesophyll chloroplasts. Planta 210, 765–774.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ivanov AG,
Krol M,
Maxwell DP, Huner NPA
(1995) Abscisic acid induced protection against photoinhibition of PSII correlates with enhanced activity of the xanthophyll cycle. FEBS Letters 371, 61–64.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ivanov AG,
Morgan RM,
Gray GR,
Velitchkova MY, Huner NPA
(1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Letters 430, 288–292.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ivanov AG,
Sane PV,
Zeinalov Y,
Malmberg G,
Gardeström P,
Huner NPA, Öquist G
(2001) Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L.). Planta 213, 575–585.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ivanov AG,
Sane P,
Hurry V,
Król M,
Sveshnikov D,
Huner NPA, Öquist G
(2003) Low temperature modulation of the redox properties of the acceptor side of photosystem II: photoprotection through reaction centre quenching of excess energy. Physiologia Plantarum 119, 376–383.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ivanov AG,
Krol M,
Sveshnikov D,
Malmberg G,
Gardeström P,
Hurry V,
Öquist G, Huner NPA
(2006a) Characterization of the photosynthetic apparatus in cortical bark chlorenchyma of Scots pine. Planta 223, 1165–1177.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ivanov AG,
Sane PV,
Krol M,
Gray GR,
Balseris A,
Savitch LV,
Öquist G, Hüner NPA
(2006b) Acclimation to temperature and irradiance modulates PSII charge recombination. FEBS Letters 580, 2797–2802.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Janda T,
Szalai G, Paldi E
(2000) Thermoluminescence investigation of low temperature stress in maize. Photosynthetica 38, 635–639.
| Crossref | GoogleScholarGoogle Scholar |
Janda T,
Szalai G,
Papp N,
Pal M, Paldi E
(2004) Effects of freezing on thermoluminescence in various plant species. Photochemistry and Photobiology 80, 525–530.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kingston-Smith AH,
Harbinson J,
Williams J, Foyer CH
(1997) Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiology 114, 1039–1046.
|
CAS |
PubMed |
Kingston-Smith AH,
Harbinson J,
Williams J, Foyer CH
(1999) Acclimation of photsynthesis, H2O2 content and antioxidants in maize (Zea mays) grown at sub-optimal temperatures. Plant, Cell and Environment 22, 1071–1083.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Klughammer C, Schreiber U
(1991) Analysis of light-induced absorbency changes in the near-infrared spectral region. 1. Characterization of various components in isolated chloroplasts. Zeitschrift fur Naturforschung C 46, 233–244.
|
CAS |
Kornyeyev D, Hendrickson L
(2007) Energy partitioning in photosysten II complexes subjected to photoinhibitory treatment. Functional Plant Biology 34, 214–220.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Kornyeyev D,
Logan BA,
Tissue DT,
Allen RD, Holaday AS
(2006) Compensation for PSII photoinactivation by regulated non-photochemical dissipation influences the impact of photoinactivation on electron transport and CO2 assimilation. Plant & Cell Physiology 47, 437–446.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Koscielniak J, Biesaga-Koscielniak J
(2006) Photosynthesis and non-photochemical excitation quenching components of chlorophyll excitation in maize and field bean during chilling at different photon flux density. Photosynthetica 44, 174–180.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Krall JP, Edwards GE
(1991) Environmental effects on the relationship between the quantum yield of carbon assimilation and in vivo PSII electron transport in maize. Australian Journal of Plant Physiology 18, 267–278.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Kramer DM,
Johnson G,
Kiirats O, Edwards GE
(2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynthesis Research 79, 209–218.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Krause GH
(1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiologia Plantarum 74, 566–574.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Krause GH, Weis E
(1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Krol M,
Ivanov AG,
Jansson S,
Kloppstech K, Huner NPA
(1999) Greening under high light or cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the chlorina f2 mutant. Plant Physiology 120, 193–204.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Labate CA,
Adcock MD, Leegood RC
(1990) Effects of temperature on the regulation of photosynthetic carbon assimilation in leaves of maize and barley. Planta 181, 547–554.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Lado C,
Then M,
Varga I,
Szőke É, Szentmihályi K
(2004) Antioxidant property of volatile oils determined by the ferric reducing ability. Zeitschrift für Naturforschung C 59, 354–358.
|
CAS |
Leipner J,
Fracheboud Y, Stamp P
(1997) Acclimation by suboptimal growth temperature diminishes photooxidative damage in maize leaves. Plant, Cell & Environment 20, 366–372.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Leipner J,
Stamp P, Fracheboud Y
(2000) Artificially increased ascorbate content affects zeaxanthin formation but not thermal energy dissipation of degradation of antioxidants during cold-induced photooxidative stress in maize leaves. Planta 210, 964–969.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Losciale P,
Oguchi R,
Hendrickson L,
Hope AB,
Corelli-Grappadelli L, Chow WS
(2008) A rapid, whole-tissue determination of the functional fraction of PSII after photoinhibition of leaves based on flash-induced P700 redox kinetics. Physiologia Plantarum 132, 23–32.
|
CAS |
PubMed |
Massacci A,
Iannelli MA,
Pietrini F, Loreto F
(1995) The effect of growth at low temperature on photosynthetic characteristics and mechanisms of photoprotection of maize leaves. Journal of Experimental Botany 46, 119–127.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Matsubara S, Chow WS
(2004) Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo. Proceedings of the National Academy of Sciences of the United States of America 101, 18234–18239.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Miranda T, Ducruet J-M
(1995) Effects of dark- and light-induced proton gradients in thylakoids on the Q and B thermoluminescence bands. Photosynthesis Research 43, 251–262.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Mohanty N,
Bruce D, Turpin DH
(1991) Dark ammonium assimilation reduces the plastoquinone pool of photosystem II in green alga Selenastum minutum. Plant Physiology 96, 513–517.
|
CAS |
Crossref |
PubMed |
Müller P,
Li XP, Niyogi KK
(2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558–1566.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Neubauer C, Yamamoto HY
(1994) Membrane barriers and Mehler-peroxidase reaction limit the ascorbate availability for violaxanthin de-epoxidase activity in intact chloroplasts. Photosynthesis Research 39, 137–147.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Nie G-Y,
Long SP, Baker NR
(1992) The effect of development at suboptimal temperatures on photosynthetic capacity and susceptibility to chilling-dependent photoinhibition in Zea mays. Physiologia Plantarum 85, 554–560.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Niinemets U, Kull O
(2001) Sensitivity of photosynthetic electron transport to photoinhibition in a temperate deciduous forest canopy: photosystem II center oppenes, non-radiative energy dissipation and excess irradiance under field conditions. Tree Physiology 21, 899–914.
|
CAS |
PubMed |
Niyogi KK
(1999) Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology 50, 333–359.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ohad I,
Adir N,
Koike H,
Kyle DJ, Inoue Y
(1990) Mechanism of photoinhibition in vivo: a reversible light-induced conformational change of reaction center II is related to an irreversible modification of the D1 protein. Journal of Biological Chemistry 265, 1972–1979.
|
CAS |
PubMed |
Ono T,
Noguchi T, Yoshihiro N
(1995) Characteristic changes of function and structure of photosystem II during strong-light photoinhibition under aerobic conditions. Biochimica et Biophysica Acta 1229, 239–248.
| Crossref | GoogleScholarGoogle Scholar |
Ortiz-Lopez A,
Nie G-Y,
Ort DR, Baker NR
(1990) The involvement of the photoinhibition of photosystem II and impaired membrane energization in the reduced quantum yield of carbon assimilation in chilled maize. Planta 181, 78–84.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Pastori G,
Foyer CH, Mullineaux P
(2000) Low temperature-induced changes in the distribution of H2O2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves. Journal of Experimental Botany 51(342), 107–113.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ruban AV, Horton P
(1995) An investigation of the sustained component of nonphotochemical quenching of chlorophyll fluorescence in isolated spinach chloroplasts and leaves of spinach. Plant Physiology 108, 721–726.
|
CAS |
PubMed |
Sane PV,
Ivanov AG,
Sveshnikov D,
Huner NPA, Öquist G
(2002) A transient exchange of the photosystem II reaction center protein D1 : 1 with D1 : 2 during low temperature stress of Synechococcus sp. PCC 7942 in the light lowers the redox potential of QB. Journal of Biological Chemistry 277, 32739–32745.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sane PV,
Ivanov AG,
Hurry V,
Huner NPA, Öquist G
(2003) Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis. Plant Physiology 132, 2144–2151.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Savitch LV,
Massacci A,
Gray GR, Huner NPA
(2000) Acclimation to low temperature or high light mitigate sensitivity to photoinhibition: roles of the Calvin cycle and the Mehler reaction. Australian Journal of Plant Physiology 27, 253–264.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Schreiber U,
Shliwa W, Bilger U
(1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorimeter. Photosynthesis Research 10, 51–62.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sharkey TD,
Savitch LV, Butz ND
(1991) Photometric method for routine determination of kcat and carbamylation of rubisco. Photosynthesis Research 28, 41–48.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sun Z-L,
Lee H-Y,
Matsubara S,
Hope AB,
Pogson BJ,
Hong Y-N, Chow WS
(2006) Photoprotection of residual functional photosystem II units that survive illumination in the absence of repair, and their critical role in subsequent recovery. Physiologia Plantarum 128, 415–424.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Thayer SS, Bjorkman O
(1992) Carotenoid distribution and deepoxidation in thylakoid pigment–protein complexes from cotton leaves and bundle-sheath cells of maize. Photosynthesis Research 33, 213–225.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
van Kooten O, Snel JFH
(1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research 25, 147–150.
| Crossref | GoogleScholarGoogle Scholar |
Vass I, Govindjee
(1996) Thermoluminescence from the photosynthetic apparatus. Photosynthesis Research 48, 117–126.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Walters RG, Horton P
(1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynthesis Research 27, 121–133.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Walters RG, Johnson GN
(1997) The effect of elevated light on photosystem II function: a thermoluminescence study. Photosynthesis Research 54, 169–183.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Woo KC,
Anderson JM,
Boardman NK,
Downton WJS,
Osmond CB, Thorne SW
(1970) Deficient photosystem II in granal bundle sheath chloroplasts of C4 plants. Proceedings of the National Academy of Sciences of the United States of America 67, 18–25.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |