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Mitochondrial electron transport protects floating leaves of long leaf pondweed (Potamogeton nodosus Poir) against photoinhibition: comparison with submerged leaves

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Abstract

Investigations were carried to unravel mechanism(s) for higher tolerance of floating over submerged leaves of long leaf pondweed (Potamogeton nodosus Poir) against photoinhibition. Chloroplasts from floating leaves showed ~5- and ~6.4-fold higher Photosystem (PS) I (reduced dichlorophenol-indophenol → methyl viologen → O2) and PS II (H2O → parabenzoquine) activities over those from submerged leaves. The saturating rate (V max) of PS II activity of chloroplasts from floating and submerged leaves reached at ~600 and ~230 µmol photons m−2 s−1, respectively. Photosynthetic electron transport rate in floating leaves was over 5-fold higher than in submerged leaves. Further, floating leaves, as compared to submerged leaves, showed higher F v/F m (variable to maximum chlorophyll fluorescence, a reflection of PS II efficiency), as well as a higher potential to withstand photoinhibitory damage by high light (1,200 µmol photons m−2 s−1). Cells of floating leaves had not only higher mitochondria to chloroplast ratio, but also showed many mitochondria in close vicinity of chloroplasts. Electron transport (NADH → O2; succinate → O2) in isolated mitochondria of floating leaves was sensitive to both cyanide (CN−) and salicylhydroxamic acid (SHAM), whereas those in submerged leaves were sensitive to CN−, but virtually insensitive to SHAM, revealing the presence of alternative oxidase in mitochondria of floating, but not of submerged, leaves. Further, the potential of floating leaves to withstand photoinhibitory damage was significantly reduced in the presence of CN− and SHAM, individually and in combination. Our experimental results establish that floating leaves possess better photosynthetic efficiency and capacity to withstand photoinhibition compared to submerged leaves; and mitochondria play a pivotal role in protecting photosynthetic machinery of floating leaves against photoinhibition, most likely by oxidation of NAD(P)H and reduction of O2.

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Abbreviations

Chl:

Chlorophyll

CN:

Cyanide

DCMU:

3-(3,4-Dichlorophenyl)-1,1-Dimethylurea

DCPIP:

Dichlorophenol indophenol

ETR:

Electron transport rate

F m :

Maximum chlorophyll a fluorescence

F o :

Initial (minimum) chlorophyll a fluorescence

F v :

Variable (F m–F o) chlorophyll a fluorescence

MV:

Methyl viologen

NAD(P)+ :

Oxidized nicotinamide adenine dinucleotide (phosphate)

NAD(P)H:

Reduced nicotinamide adenine dinucleotide (phosphate)

pBQ:

Parabenzoquinone

PFD:

Photon flux density

PQ:

Plastoquinone

PS I, PS II:

Photosystem I, Photosystem II

Q A :

Oxidized primary plastoquinone electron acceptor of PS II

\(Q_{A^-}\) :

Reduced primary plastoquinone electron acceptor of PS II

SHAM:

Salicylhydroxamic acid

References

  • Adams WW III, Demmig-Adams B, Winter K, Schreiber U (1990) The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77 K, as an indicator of the photon yield of photosynthesis. Planta 180:166–174

    Article  CAS  PubMed  Google Scholar 

  • Alia, Mohanty P, Pardha-Saradhi P (1992) Effect of sodium chloride on primary photochemical activities in cotylendoary leaves of Brassica juncea. Biochem Physiol Pflanzen 188:1–12

  • Anderson JM, Chow WS, Rivas JDL (2008) Dynamic flexibility in the structure and function of photosystem II in higher plant thylakoid membranes: the grana enigma. Photosynth Res 98:575–587

    Article  CAS  PubMed  Google Scholar 

  • Araujo WL, Nunes-Nesi A, Fernie AR (2014) On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions. Photosynth Res 119:141–156

    Article  CAS  PubMed  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958

    Article  CAS  PubMed  Google Scholar 

  • Bartoli CG, Pastori GM, Foyer CH (2000) Ascorbate biosynthesis in mitochondria is linked to the electron transport chain between complexes iii and iv. Plant Physiol 123:335–343

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bartoli CG, Gomez F, Gergoff G, Gulamet JJ, Puntarulo S (2005) Up-regulation of the mitochondrial alternative oxidase pathway enhances photosynthetic electron transport under drought conditions. J Exp Bot 53:1269–1276

    Article  Google Scholar 

  • Berg AP, Krogmann DW (1975) Mechanism of KCN inhibition of photosystem I. J Biol Chem 250:8957–8962

    CAS  PubMed  Google Scholar 

  • Biel KY, Nishio JN (2010) Untangling metabolic and spatial interactions of stress tolerance in plants. 2. Accelerated method for measuring and predicting stress tolerance. can we unravel the mysteries of the interactions between photosynthesis and respiration? Protoplasma 245:29–48

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of dye-binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220

    Article  CAS  PubMed  Google Scholar 

  • Chen S, Yina C, Strasser RJ, Govindjee, Yang C, Qiang S (2012) Reactive oxygen species from chloroplasts contribute to 3-acetyl-5-isopropyltetramic acid-induced leaf necrosis of Arabidopsis thaliana. Plant Physiol Biochem 52:38–51

    Article  CAS  PubMed  Google Scholar 

  • Cramer WA, Knaff DB (1991) Energy transduction in biological membranes: a textbook of bioenergetics. Springer-Verlag, New York

    Google Scholar 

  • Croce R, Amerongen Van (2014) Natural strategies for photosynthetic light harvesting. Nat Chem Biol 10:492–501

    Article  CAS  PubMed  Google Scholar 

  • David GFX, Herbert J, Wright CDS (1973) The ultrastructure of the pineal ganglion in the ferret. J Anat 115:79–97

    CAS  PubMed Central  PubMed  Google Scholar 

  • Demmig B, Björkman O (1987) Comparison of the effect of excessive light on chlorophyll fluorescence (77 K) and photon yield of O2 evolution in leaves of higher plants. Planta 171:171–184

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW III, Autar AK (2006) Photoprotection, photoinhibition, gene regulation, and environment. Advances in photosynthesis and respiration. Springer, Dordrecht

    Book  Google Scholar 

  • Duncan DB (1955) Multiple range and multiple F tests. Biometrics 39:205–207

    Google Scholar 

  • Elthon TE, Mcintosh L (1987) Identification of the alternative terminal oxidase of higher plant mitochondria. Proc Natl Acad Sci USA 84:8399–8403

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2002) Photosynthetic nitrogen assimilation and associated carbon and respiratory metabolism. Advances in photosynthesis and respiration. Springer, Dordrecht

    Google Scholar 

  • Foyer CH, Noctor G (2012) Managing the cellular redox hub in photosynthetic organisms. Plant, Cell Environ 35:199–201

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Govindjee (2004) Chlorophyll a fluorescence: a bit of basics and history. In: Papageorgiou G, Govindjee (eds) Chlorophyll a fluorescence: a probe of photosynthesis. Kluwer Academic Publishers, Amsterdam, pp 2–42

    Google Scholar 

  • Hell R, Dahl C, Knaff D and Leustek T (eds) (2008) Sulfur metabolism in phototrophic organisms. Advances in photosynthesis and respiration, vol 27. Springer, Dordrecht

  • Hussner A, Hoelkena HP, Jahns P (2010) Low light acclimated submerged freshwater plants show a pronounced sensitivity to increasing irradiances. Aquatic Bot 93:17–24

    Article  Google Scholar 

  • Jana S, Choudhari MA (1980) Characterization of hill activity of a submersed aquatic angiosperm (Sago Pondweed). J Aquat Plant Manag 18:30–34

    Google Scholar 

  • Kangasjarvi S, Neukermans J, Li S, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63:1619–1636

    Article  PubMed  Google Scholar 

  • Kolloffel C (1967) Respiration rate and mitochondrial activity in the cotyledons of P. sativum L. during germination. Acta Bot Neerl 16:111–112

    Article  Google Scholar 

  • Kordyum E, Klimenko E (2013) Chloroplast ultrastructure and chlorophyll performance in the leaves of heterophyllous Nuphar lutea (L.) Smith. plants. Aquatic Bot 110:84–91

    Article  CAS  Google Scholar 

  • Kramer DM, Avenson TJ, Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Burkart S (1999) Photosynthesis and high light stress. Bulg J Plant Physiol 25:3–16

    CAS  Google Scholar 

  • Ligeza A, Wisniewska A, Subczynski WK, Tikhonov AN (1994) Oxygen production and consumption by chloroplasts in situ and in vitro as studied with microscopic spin label probes. Biochim Biophys Acta 1186:201–208

    Article  CAS  PubMed  Google Scholar 

  • Ligeza A, Tikhonov AN, Subszynski WK (1997) In situ measurements of oxygen production using paramagnetic fusinate particles injected into a bean leaf. Biochim Biophys Acta 1319:133–137

    Article  CAS  Google Scholar 

  • Ligeza A, Tikhonov AN, Hyde JS, Subczynski WK (1998) Oxygen permeability of thylakoid membranes: EPR spin labeling study. Biochim Biophys Acta 1365:453–463

    Article  CAS  PubMed  Google Scholar 

  • Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annu Rev Plant Biol 62:79–104

    Article  CAS  PubMed  Google Scholar 

  • Møller IM, Sweetlove LJ (2010) ROS signalling-specificity is required. Trends Plant Sci 15:370–374

    Article  PubMed  Google Scholar 

  • Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

    Article  PubMed  Google Scholar 

  • Munday JC Jr, Govindjee (1969a) Light-induced changes in the fluorescence yield of chlorophyll a in vivo III. The dip and the peak in the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:1–21

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Munday JC Jr, Govindjee (1969b) Light-induced changes in the fluorescence yield of chlorophyll a in vivo. IV. The effect of preillumination on the fluorescence transient of Chlorella pyrenoidosa. Biophysic J 9:22–35

  • Nishiyama Y, Allakhverdiev SI, Murata N (2011) Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. Physiol Plant 142:35–46

    Article  CAS  PubMed  Google Scholar 

  • Noctor G (2006) Metabolic signaling in defence and stress: the central roles of redox couples. Plant, Cell Environ 29:409–425

    Article  CAS  Google Scholar 

  • Oquist G, Anderson JM, McCaffery S, Chow WS (1992) Mechanistic differences in photoinhibition of sun and shade plants. Planta 188:422–431

    Article  CAS  PubMed  Google Scholar 

  • Ort D, Izawa S, Good NE, Krogmann DW (1973) Effects of the plastocyanin antagonists KCN and poly-l-lysine on partial reaction in isolated chloroplasts. FEBS Lett 31:119–122

    Article  CAS  PubMed  Google Scholar 

  • Papageorgiou GC, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht

  • Pardha-Saradhi P, Suzuki I, Katoh A, Sakamoto A, Sharmila P, Shi D-J, Murata N (2000) Protection of photosysytem II complex by abscisic acid against photoinduced-inactivation. Plant, Cell Environ 23:711–718

    Article  Google Scholar 

  • Poolman MG, Kundu S, Shaw R, Fell DA (2013) Responses to light intensity in a genome-scale model of rice metabolism. Plant Physiol 162:1060–1072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Potters G, Horemans N, Jansen AK (2010) The cellular redox state in plant stress biology: a charging concept. Plant Physiol Biochem 48:292–300

    Article  CAS  PubMed  Google Scholar 

  • Prasad KVSK, Pardha-Saradhi P (2004) Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts. Plant Sci 166:1197–1212

    Article  CAS  Google Scholar 

  • Puthur JT, Pardha-Saradhi P (2004) Developing embryos of Sesbania sesban have unique potential to photosynthesize under high osmotic environment. J Plant Physiol 161:1107–1118

    Article  CAS  PubMed  Google Scholar 

  • Puthur JT, Shackira AM, Pardha-Saradhi P, Bartels D (2013) Chloroembryos: a unique photosynthesis system. J Plant Physiol 170:1131–1138

    Article  CAS  PubMed  Google Scholar 

  • Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8:546–563

    Article  CAS  PubMed  Google Scholar 

  • Ryan FJ (1985) Isolation and characterization of photosynthetically active cells from submersed and floating leaves of the aquatic macrophyte Potamogeton nodosus Poir. Plant Cell Physiol 26:309–315

    CAS  Google Scholar 

  • Scheibe R, Dietz K-J (2012) Reduction-oxidation network for flexible adjustment of cellular metabolism in photoautotrophic cells. Plant, Cell Environ 35:202–216

    Article  CAS  Google Scholar 

  • Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK, Los DA, Kuznetsov VV, Allakhverdiev SI (2014) Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signaling in phototrophic organisms. Biochim Biophys Acta 1837:835–848

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U, Bilger W, Hormann H, Neubauer C (1998) Chlorophyll fluorescence as a diagnostic tool: basics and some aspects of practical relevance. Raghavendra AS(ed) Photosynthesis: a comprehensive treatise. Cambridge university press, Cambridge, pp 320–336

    Google Scholar 

  • Shabnam N, Pardha-Saradhi P (2013) Photosynthetic electron transport system promotes synthesis of Au-nanoparticles. PLoS ONE 8:e71123

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sharmila P, Anwar F, Sharma KR, Pardha-Saradhi P (2008) Management of abiotic stresses in grain legumes through manipulation of genes for compatible solutes. In: Kirti PB (ed) Handbook of new technologies for genetic improvement of legumes. CRC Press, Boca Raton, pp 577–603

    Google Scholar 

  • Sharmila P, Phanindra MLV, Anwar F, Singh K, Gupta S, Pardha-Saradhi P (2009) Targeting prokaryotic choline oxidase into chloroplasts enhance the potential of photosynthetic machinery of plants to withstand oxidative damage. Plant Physiol Biochem 47:391–396

    Article  CAS  PubMed  Google Scholar 

  • Stirbet A, Govindjee (2011) On the relation between Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescent transient. J Photochem Photobiol B: Biol. 104:236–257

    Article  CAS  Google Scholar 

  • Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15–61

    Article  CAS  PubMed  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer Academic Publishers, Amsterdam, pp 977–980

    Google Scholar 

  • Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic Chl a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32–42

    Article  CAS  Google Scholar 

  • Strauss AJ, Kruger GHJ, Strasser RJ, Van Heerden PDR (2006) Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. Environ Exp Bot 56:147–157

    Article  CAS  Google Scholar 

  • Suzuki N, Koussevitzk K, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant, Cell Environ 35:259–270

    Article  CAS  Google Scholar 

  • Taniguchi M, Miyake H (2012) Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Curr Opin Plant Biol 15:252–260

    Article  CAS  PubMed  Google Scholar 

  • Toth S, Schansker G, Strasser RJ (2007) A non-invasive assay of the pastoquinone pool redox state based on the OJIP transient. Photosynth Res 93:193–203

    Article  CAS  PubMed  Google Scholar 

  • Wientjes E, Van Amerongen H, Croce R (2013) Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation. J Phys Chem B 117:11200–11208

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Terashima I, Noguchi K (2006) Distinct roles of the cytochrome pathway and alternative oxidase in leaf photosynthesis. Plant Cell Physiol 47:22–31

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Watanabe C, Kato Y, Sakamoto W, Noguchi K (2008) Influence of chloroplastic photo-oxidative stress on mitochondrial alternative oxidase capacity and respiratory properties: a case study with Arabidopsis yellow variegated 2. Plant Cell Physiol 49:592–603

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Watanabe CK, Terashima I, Noguchi K (2011a) Physiological impact of mitochondrial alternative oxidase on photosynthesis and growth in Arabidopsis thaliana. Plant, Cell Environ 34:1890–1899

    Article  CAS  Google Scholar 

  • Yoshida K, Watanabe CK, Hachiya T, Tholen D, Shibata MI, Noguchi K (2011b) Distinct responses of the mitochondrial respiratory chain to long- and short-term high-light environments in Arabidopsis thaliana. Plant, Cell Environ 34:618–628

    Article  CAS  Google Scholar 

  • Zhang LT, Gao HY, Zhang ZS, Xue ZC, Meng QW (2012) The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. BMC Plant Biol 12:1–18

    Article  Google Scholar 

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Acknowledgments

This work was supported by funds from the Swiss Agency for Development and Cooperation, Government of Switzerland and the Department of Biotechnology (Government of India) under the Indo-Swiss Collaboration in Biotechnology; and the Department of Biotechnology (Government of India) under Bio-CARe Women Scientist Scheme. NS is thankful to the University Grants Commission (of India) for providing her a fellowship. Govindjee is thankful to Ravenshaw University for a visiting professorship (January 5–March 5, 2014) in the Department of Botany; it was during this period the final draft of this paper was written. We also acknowledge the help received from Electron Microscope facility, All India Institute of Medical Sciences (New Delhi) for the ultrastructural studies. We are thankful to Prof. K.S. Rao, Department of Botany, University of Delhi, for the use of LICOR 6400.

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Authors and Affiliations

  1. Department of Environmental Studies, University of Delhi, Delhi, 110007, India

    Nisha Shabnam & P. Pardha-Saradhi

  2. Department of Chemistry, Indian Institute of Technology Delhi, New Delhi, 110016, India

    P. Sharmila

  3. Department of Botany, Hindu College, University of Delhi, Delhi, 110007, India

    Anuradha Sharma

  4. Bioenergetics Laboratory, University of Geneva, 1254, Jussy/Geneva, Switzerland

    Reto J. Strasser

  5. Department of Biology, North West University, Potchefstroom, South Africa

    Reto J. Strasser

  6. Laboratory for Weed Research, Nanjing Agricultural University, Nanjing, China

    Reto J. Strasser

  7. Department of Plant Biology, Department of Biochemistry, and Center of Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801-3707, USA

    Govindjee

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  1. Nisha Shabnam
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Shabnam, N., Sharmila, P., Sharma, A. et al. Mitochondrial electron transport protects floating leaves of long leaf pondweed (Potamogeton nodosus Poir) against photoinhibition: comparison with submerged leaves. Photosynth Res 125, 305–319 (2015). https://doi.org/10.1007/s11120-014-0051-3

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