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Potamogeton Nodosus Poir) Against Photoinhibition: Comparison with Submerged Leaves

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Potamogeton Nodosus Poir) Against Photoinhibition: Comparison with Submerged Leaves Photosynth Res DOI 10.1007/s11120-014-0051-3 REGULAR PAPER Mitochondrial electron transport protects floating leaves of long leaf pondweed (Potamogeton nodosus Poir) against photoinhibition: comparison with submerged leaves Nisha Shabnam • P. Sharmila • Anuradha Sharma • Reto J. Strasser • Govindjee • P. Pardha-Saradhi Received: 17 September 2014 / Accepted: 16 October 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract Investigations were carried to unravel mecha- leaves reached at *600 and *230 lmol photons m-2 s-1, nism(s) for higher tolerance of floating over submerged respectively. Photosynthetic electron transport rate in float- leaves of long leaf pondweed (Potamogeton nodosus Poir) ing leaves was over 5-fold higher than in submerged leaves. against photoinhibition. Chloroplasts from floating leaves Further, floating leaves, as compared to submerged leaves, showed *5- and *6.4-fold higher Photosystem (PS) I showed higher Fv/Fm (variable to maximum chlorophyll (reduced dichlorophenol-indophenol ? methyl violo- fluorescence, a reflection of PS II efficiency), as well as a gen ? O2) and PS II (H2O ? parabenzoquine) activities higher potential to withstand photoinhibitory damage by -2 -1 over those from submerged leaves. The saturating rate (Vmax) high light (1,200 lmol photons m s ). Cells of floating of PS II activity of chloroplasts from floating and submerged leaves had not only higher mitochondria to chloroplast ratio, but also showed many mitochondria in close vicinity of chloroplasts. Electron transport (NADH ? O2; succi- N. Shabnam P. Pardha-Saradhi (&) Á nate ? O2) in isolated mitochondria of floating leaves was Department of Environmental Studies, University of Delhi, sensitive to both cyanide (CN-) and salicylhydroxamic acid Delhi 110007, India e-mail: [email protected] (SHAM), whereas those in submerged leaves were sensitive to CN-, but virtually insensitive to SHAM, revealing the P. Sharmila presence of alternative oxidase in mitochondria of floating, Department of Chemistry, Indian Institute of Technology Delhi, but not of submerged, leaves. Further, the potential of New Delhi 110016, India floating leaves to withstand photoinhibitory damage was - A. Sharma significantly reduced in the presence of CN and SHAM, Department of Botany, Hindu College, University of Delhi, individually and in combination. Our experimental results Delhi 110007, India establish that floating leaves possess better photosynthetic R. J. Strasser efficiency and capacity to withstand photoinhibition com- Bioenergetics Laboratory, University of Geneva, pared to submerged leaves; and mitochondria play a pivotal 1254 Jussy/Geneva, Switzerland role in protecting photosynthetic machinery of floating leaves against photoinhibition, most likely by oxidation of R. J. Strasser Department of Biology, North West University, Potchefstroom, NAD(P)H and reduction of O2. South Africa Keywords Chlorophyll a fluorescence Á CN-resistant R. J. Strasser alternative oxidase pathway Á CN-sensitive cytochrome Laboratory for Weed Research, Nanjing Agricultural University, Nanjing, China oxidase pathway Á Chloroplast-mitochondria interaction Á Photoinhibition Á Potamogeton nodosus Govindjee (&) Department of Plant Biology, Department of Biochemistry, and Abbreviations Center of Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801-3707, USA Chl Chlorophyll e-mail: [email protected] CN Cyanide 123 Photosynth Res DCMU 3-(3,4-Dichlorophenyl)-1,1-Dimethylurea proteins, nucleic acids, and lipids resulting in disruption of DCPIP Dichlorophenol indophenol overall cellular metabolism (Demmig-Adams et al. 2006; ETR Electron transport rate Møller et al. 2007; Møller and Sweetlove 2010; Chen et al. Fm Maximum chlorophyll a fluorescence 2012; Suzuki et al. 2012). Thus, cellular capacity to ? Fo Initial (minimum) chlorophyll a fluorescence modulate the NAD(P)H/NAD(P) ratio is critical not only Fv Variable (Fm–Fo) chlorophyll a fluorescence for the redox control of metabolism, but also for restraining MV Methyl viologen oxidative stress (Bartoli et al. 2005; Buchanan and Balmer NAD(P)? Oxidized nicotinamide adenine dinucleotide 2005; Noctor 2006; Møller et al. 2007; Yoshida et al. 2006, (phosphate) 2008; Foyer and Noctor 2002, 2012). NAD(P)H Reduced nicotinamide adenine dinucleotide Although photosynthesis is an autonomous metabolic (phosphate) process that takes place in chloroplasts, its efficiency is pBQ Parabenzoquinone strongly linked to mitochondrial activity (Raghavendra and PFD Photon flux density Padmasree 2003; Yoshida et al. 2006; 2008; Poolman et al. PQ Plastoquinone 2013; Araujo et al. 2014). It is known that mitochondrial PS I, PS II Photosystem I, Photosystem II electron transport, mediated by both cyanide (CN)-sensi- QA Oxidized primary plastoquinone electron tive cytochrome c oxidase, and CN-resistant alternative acceptor of PS II oxidase pathways, optimizes photosynthetic activity at QAÀ Reduced primary plastoquinone electron saturating light intensity by modulating reducing equiva- acceptor of PS II lents and ensuring the rapid availability of NADP? (ter- SHAM Salicylhydroxamic acid minal acceptor of photosynthetic electron transport) (Bartoli et al. 2005; Yoshida et al. 2006, 2011a, 2011b; Suzuki et al. 2012; Araujo et al. 2014). In fact, inhibition of either of the above-mentioned pathways leads to a decrease Introduction in the steady state level of photosynthetic O2 evolution, as well as in the quantum yield of PS II (Raghavendra and Bioenergetics of plants involves chloroplasts, where pho- Padmasree 2003; Yoshida et al. 2006; Møller et al. 2007; tosynthesis takes place, as well as mitochondria, where Zhang et al. 2012). respiration takes place (Cramer and Knaff 1991). These Potamogeton nodosus Poir (long leaf pondweed) is a two organelles together maintain cellular redox status lar- heterophyllous monocotyledonous aquatic plant with two gely by regulating the balance of oxidized and reduced distinct types of leaves: floating and submerged (Ryan 1985; forms of nicotinamide dinucleotide (phosphate), NAD(P)?, also see http://plants.usda.gov/core/profile?symbol=pono2). and NAD(P)H. Normally, the rate of light-driven NADP? Submerged leaves are thin, translucent with little or no reduction is balanced with simultaneous oxidation of cuticle. In contrast, floating leaves are thick, opaque with NADPH through carbon assimilation (i.e., through Calvin– shining thick cuticle. Ryan (1985) had recorded superior Benson cycle) and other assimilatory pathways such as that CO2 fixation in cells isolated from floating leaves compared of nitrogen and sulfur (Foyer and Noctor 2002; Kramer to those from submerged leaves of P. nodosus. Kordyum and et al. 2004; Hell et al. 2008; Scheibe and Dietz 2012; Klimenko (2013), based on chlorophyll (Chl) a fluorescence Taniguchi and Miyake 2012). However, whenever the rate data, have reported that submerged leaves of heterophyllous of light-induced generation of NADPH and reduced fer- Nuphar lutea are susceptible to photoinhibition. Chlorophyll redoxin exceeds the rate of their oxidation, reductants a fluorescence is widely used to probe various aspects of accumulate in thylakoid membranes, as well as in the photosynthetic photochemical reactions (see e.g., Strasser stroma region. This results in cellular redox imbalance that and Strasser 1995; Papageorgiou and Govindjee 2004; favors an increase in one-electron reduction of molecular Strauss et al. 2006). Here, in this paper, we show for the first oxygen leading to the generation of reactive oxygen spe- time that floating leaves, as compared to submerged leaves, cies (ROS) (Demmig-Adams and Adams 2006; Yoshida not only exhibit a superior photosynthetic capacity (mea- et al. 2006, 2008; Møller et al. 2007; Kangasjarvi et al. sured in terms of PS I and PS II activities), but also show a 2012; Schmitt et al. 2014). ROS, in turn, cause(s) pho- superior potential to withstand photoinhibitory damage by toinhibition by either damaging components of photosyn- high photon flux density. This potential of floating leaves to thetic machinery, in particular Photosystem II (PS II), or withstand photoinhibitory damage is linked not only to a inhibiting/inactivating PS II repair mechanisms through large number of mitochondria in floating over submerged suppression of protein synthesis (Nishiyama et al. 2011). leaves, but it is also due to differences in CN-sensitive In addition, ROS also interact(s) with and inacti- cytochrome oxidase and CN-resistant alternative oxidase vate(s) several cellular macromolecules, which include pathways in mitochondria. 123 Photosynth Res Materials and methods electron transport, the reaction mixture was 20 mM tricine with 100 mM sucrose, 10 mM NaCl and 2 mM MgCl2 (at pH Plant material 7.8), and 1 mM pBQ. Maximum light intensity (or photon flux density, PFD) used was 920 lmol photons m-2 s-1.Based Potamogeton nodosus Poir (Family: Potamogetonaceae) was on the results of light saturation curve (Fig. 1), electron obtained from Kapalmochan pond, Bilaspur (District Yamuna transfer activity for PS I (DCPIPH2 ? MV ? O2); for PS II Nagar, Haryana, India). The temperature around the Kapal- (H2O ? pBQ); and for whole chain (H2O ? MV ? O2)of mochan pond varies between *18 °C (in March) and chloroplasts, isolated from floating and submerged leaves, *40 °C (in May) and solar irradiance at the surface of the were measured at a PFD of *920 and *230 lmol pho- pond generally ranges to be from 800 to 2,400 lmol pho- tons m-2 s-1, respectively, All experiments were
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