Knocking Down of Isoprene Emission Modifies the Lipid Matrix of Thylakoid Membranes and Influences the Chloroplast Ultrastructure in Poplar

Velikova, Violeta; Müller, Constanze; Ghirardo, Andrea; Rock, Theresa Maria; Aichler, Michaela; Walch, Axel; Schmitt‐Kopplin, Philippe; Schnitzler, Jörg‐Peter

doi:10.1104/pp.15.00612

Cited by 38 publications

(44 citation statements)

References 87 publications

(125 reference statements)

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“…The lower amount of protein members of the photosynthetic apparatus may influence the physiology of NE poplar under unstressed conditions and upon stress. While initial physiological measurements showed no significant differences in the net CO 2 assimilation rates of both genotypes (Behnke et al, 2007(Behnke et al, , 2009(Behnke et al, , 2010a, recent observations reported lower gas exchange (Way et al, 2013) and electron transport rates (Velikova et al, 2015) in the NE genotype compared with the IE genotype.…”

Section: Whole-proteome Analysis Highlights Some Alterations In the Pmentioning

confidence: 73%

Modulation of Protein S-Nitrosylation by Isoprene Emission in Poplar

et al. 2016

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ORCID IDs: 0000-0002-3422-4083 (J.M.-P.); 0000-0001-8410-5624 (J.B.); 0000-0002-9825-867X (J.-P.S.).Researchers have been examining the biological function(s) of isoprene in isoprene-emitting (IE) species for two decades. There is overwhelming evidence that leaf-internal isoprene increases the thermotolerance of plants and protects them against oxidative stress, thus mitigating a wide range of abiotic stresses. However, the mechanisms of abiotic stress mitigation by isoprene are still under debate. Here, we assessed the impact of isoprene on the emission of nitric oxide (NO) and the S-nitroso-proteome of IE and non-isoprene-emitting (NE) gray poplar (Populus 3 canescens) after acute ozone fumigation. The short-term oxidative stress induced a rapid and strong emission of NO in NE compared with IE genotypes. Whereas IE and NE plants exhibited under nonstressful conditions only slight differences in their S-nitrosylation pattern, the in vivo S-nitroso-proteome of the NE genotype was more susceptible to ozone-induced changes compared with the IE plants. The results suggest that the nitrosative pressure (NO burst) is higher in NE plants, underlining the proposed molecular dialogue between isoprene and the free radical NO. Proteins belonging to the photosynthetic light and dark reactions, the tricarboxylic acid cycle, protein metabolism, and redox regulation exhibited increased S-nitrosylation in NE samples compared with IE plants upon oxidative stress. Because the posttranslational modification of proteins via S-nitrosylation often impacts enzymatic activities, our data suggest that isoprene indirectly regulates the production of reactive oxygen species (ROS) via the control of the S-nitrosylation level of ROS-metabolizing enzymes, thus modulating the extent and velocity at which the ROS and NO signaling molecules are generated within a plant cell.It has been demonstrated that isoprene protects plants against a plethora of abiotic stresses (Singsaas et al., 1997;Behnke et al., 2007;Velikova et al., 2008;Vickers et al., 2009b). Since the discovery of the positive influence of isoprene emission on plants' photosynthetic processes in the early 1990s (Sharkey and Singsaas, 1995), many efforts have been made to explain the primary mechanism of isoprene functioning. Most attention was given to the hypothesis that isoprene improves the thermotolerance of the photosynthetic machinery by stabilizing chloroplast (thylakoid) membranes during short, high-temperature episodes (Sharkey and Singsaas, 1995;Loreto and Schnitzler, 2010). Successive studies underlined that isoprene helps maintain high rates of chloroplastic electron transport and CO 2 assimilation during heat stress and accelerates recovery from stress (Singsaas and Sharkey, 2000;Velikova et al., 2006;Behnke et al., 2010b;Way et al., 2011).One mechanistic explanation is that isoprene molecules are dissolved in thylakoid membrane and prevent membrane lipid denaturation following oxidative stress (Sharkey and Yeh, 2001). It was suggested that isoprene acts directly to st...

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Section: Whole-proteome Analysis Highlights Some Alterations In the Pmentioning

confidence: 73%

Modulation of Protein S-Nitrosylation by Isoprene Emission in Poplar

et al. 2016

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“…Because ETR is thylakoid membrane localized, reduced ETR in heatstressed NE plants may be explained as a consequence of altered membrane stability (Singsaas et al, 1997;Velikova et al, 2011) and/or of direct interaction of isoprene with reactive oxygen species, resulting in lower oxidative damage and lipid peroxidation (Loreto and Velikova, 2001;Velikova et al, 2005;Vickers et al, 2009). Recent findings by Velikova et al (2014Velikova et al ( , 2015 suggest that the lower ETR in NE plants may result from subcellular remodeling processes that occur in NE chloroplasts, possibly as a consequence of the RNA interference-mediated silencing of the ISPS. The analysis of the chloroplast ultrastructure, the proteome, and the lipid composition of the thylakoid membrane of IE and NE poplars (Velikova et al, , 2015 revealed a comprehensive structural and functional reorganization in the thylakoid membranes of NE plants.…”

Section: Isoprene Emission Is Not Essential For Poplar To Adapt To Famentioning

confidence: 99%

“…Recent findings by Velikova et al (2014Velikova et al ( , 2015 suggest that the lower ETR in NE plants may result from subcellular remodeling processes that occur in NE chloroplasts, possibly as a consequence of the RNA interference-mediated silencing of the ISPS. The analysis of the chloroplast ultrastructure, the proteome, and the lipid composition of the thylakoid membrane of IE and NE poplars (Velikova et al, , 2015 revealed a comprehensive structural and functional reorganization in the thylakoid membranes of NE plants. The lower amount of unsaturated fatty acids (i.e.…”

Section: Isoprene Emission Is Not Essential For Poplar To Adapt To Famentioning

confidence: 99%

Facing the Future: Effects of Short-Term Climate Extremes on Isoprene-Emitting and Nonemitting Poplar

Vanzo

Jud

et al. 2015

Plant Physiol.

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(H.R.); 0000-0002-9825-867X (J.-P.S.).Isoprene emissions from poplar (Populus spp.) plantations can influence atmospheric chemistry and regional climate. These emissions respond strongly to temperature, [CO 2 ], and drought, but the superimposed effect of these three climate change factors are, for the most part, unknown. Performing predicted climate change scenario simulations (periodic and chronic heat and drought spells [HDSs] applied under elevated [CO 2 ]), we analyzed volatile organic compound emissions, photosynthetic performance, leaf growth, and overall carbon (C) gain of poplar genotypes emitting (IE) and nonemitting (NE) isoprene. We aimed (1) to evaluate the proposed beneficial effect of isoprene emission on plant stress mitigation and recovery capacity and (2) to estimate the cumulative net C gain under the projected future climate. During HDSs, the chloroplastidic electron transport rate of NE plants became impaired, while IE plants maintained high values similar to unstressed controls. During recovery from HDS episodes, IE plants reached higher daily net CO 2 assimilation rates compared with NE genotypes. Irrespective of the genotype, plants undergoing chronic HDSs showed the lowest cumulative C gain. Under control conditions simulating ambient [CO 2 ], the C gain was lower in the IE plants than in the NE plants. In summary, the data on the overall C gain and plant growth suggest that the beneficial function of isoprene emission in poplar might be of minor importance to mitigate predicted short-term climate extremes under elevated [CO 2 ]. Moreover, we demonstrate that an analysis of the canopy-scale dynamics of isoprene emission and photosynthetic performance under multiple stresses is essential to understand the overall performance under proposed future conditions. Climate change will lead to an increase in global temperatures of at least 2°C in the near future (IPCC, 2014). There is at present substantial evidence that this climate change is leading to an increase in the frequency and intensity of extreme events such as heat and drought waves (Feyen and Dankers, 2009;Fischer and Schär, 2010;Perkins et al., 2012;Thornton et al., 2014), creating a sequence of recurring stress and recovery cycles for plants. Coumou and Rahmstorf (2012) showed that, in the last 15 years, five extreme heat wave events have occurred worldwide, four of which were observed also in Europe. Interactions between heat and drought under predicted elevated [CO 2 ] (IPCC, 2014) generate complex, often nonadditive physiological responses. Such effects cannot be predicted by singlefactor analyses and highlight the importance of carrying out controlled, multistress scenarios to investigate plant performance under future climate conditions (Clausen et al., 2011; Alemayehu et al., 2014).Photosynthesis, respiration, and photorespiration are the three dominating processes determining carbon (C) exchange and C metabolism in plants (Bauwe et al., 2010;Mahecha et al., 2010). In addition, the emission of biogenic volatile organic c...

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“…It is also shown that isoprene stabilizes thylakoid membrane structure and its function is closely associated with structural organization and functioning of plastidial membranes (Velikova et al . , ; Pollastri et al . ).…”

Section: Introductionmentioning

confidence: 99%

Physiological significance of isoprenoids and phenylpropanoids in drought response of Arundinoideae species with contrasting habitats and metabolism

Velikova

Brunetti

Tattini

et al. 2016

Plant Cell & Environment

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Physiological, biochemical and morpho-anatomical traits that determine the phenotypic plasticity of plants under drought were tested in two Arundinoideae with contrasting habitats, growth traits and metabolism: the fast-growing Arundo donax, which also is a strong isoprene emitter, and the slow-growing Hakonechloa macra that does not invest on isoprene biosynthesis. In control conditions, A. donax displayed not only higher photosynthesis but also higher concentration of carotenoids and lower phenylpropanoid content than H. macra. In drought-stressed plants, photosynthesis was similarly inhibited in both species, but substantially recovered only in A. donax after rewatering. Decline of photochemical and biochemical parameters, increased concentration of CO2 inside leaves, and impairment of chloroplast ultrastructure were only observed in H. macra indicating damage of photosynthetic machinery under drought. It is suggested that volatile and non-volatile isoprenoids produced by A. donax efficiently preserve the chloroplasts from transient drought damage, while H. macra invests on phenylpropanoids that are less efficient in preserving photosynthesis but likely offer better antioxidant protection under prolonged stress.

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Knocking Down of Isoprene Emission Modifies the Lipid Matrix of Thylakoid Membranes and Influences the Chloroplast Ultrastructure in Poplar

Cited by 38 publications

References 87 publications

Modulation of Protein S-Nitrosylation by Isoprene Emission in Poplar

Modulation of Protein S-Nitrosylation by Isoprene Emission in Poplar

Facing the Future: Effects of Short-Term Climate Extremes on Isoprene-Emitting and Nonemitting Poplar

Physiological significance of isoprenoids and phenylpropanoids in drought response of Arundinoideae species with contrasting habitats and metabolism

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