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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

The electrical signal-induced systemic photosynthetic response is accompanied by changes in the photochemical reflectance index in pea

Vladimir Sukhov https://orcid.org/0000-0002-8712-9127 A B , Ekaterina Sukhova A , Ekaterina Gromova A , Lyubov Surova A , Vladimir Nerush A and Vladimir Vodeneev A
+ Author Affiliations
- Author Affiliations

A Department of Biophysics, N.I. Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod, 603950, Russia.

B Corresponding author. Email: vssuh@mail.ru

Functional Plant Biology 46(4) 328-338 https://doi.org/10.1071/FP18224
Submitted: 17 August 2018  Accepted: 23 November 2018   Published: 10 January 2019

Abstract

Plants can be affected by numerous environmental stressors with spatially heterogeneous actions on their bodies. A fast systemic photosynthetic response, which is connected with long-distance electrical signalling, plays an important role in the adaptation of higher plants to the action of stressors. Potentially, measurement of the response by using a photochemical reflectance index (PRI) could be the basis of monitoring photosynthesis under spatially heterogeneous stressors; however, the method has not been previously used for investigating the systemic photosynthetic response. We investigated changes in PRI and photosynthetic parameters (quantum yields of PSI and PSII and nonphotochemical quenching) in intact leaves of pea (Pisum sativum L.) after local heating of another leaf and the propagation of electrical signals through the plant body. We showed that electrical signals decreased the quantum yields of PSI and PSII and increased the nonphotochemical quenching of intact leaves in times ranging from minutes to tens of minutes; the changes were strongly connected with changes in PRI. Additional analysis showed that changes in PRI were caused by an increase of the energy-dependent quenching induced by electrical signals. Thus PRI can be potentially used for monitoring the systemic photosynthetic response connected with long-distance electrical signalling.

Additional keywords: long-distance electrical signalling, nonphotochemical quenching, Pisum sativum.


References

Balzarolo M, Peñuelas J, Filella I, Portillo-Estrada M, Ceulemans R (2018) Assessing ecosystem isoprene emissions by hyperspectral remote sensing. Remote Sensing 10, 1086
Assessing ecosystem isoprene emissions by hyperspectral remote sensing.Crossref | GoogleScholarGoogle Scholar |

Beilby MJ (2007) Action potential in Charophytes. International Review of Cytology 257, 43–82.
Action potential in Charophytes.Crossref | GoogleScholarGoogle Scholar | 17280895PubMed |

Białasek M, Górecka M, Mittler R, Karpiński S (2017) Evidence for the involvement of electrical, calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis. Plant & Cell Physiology 58, 207–215.
Evidence for the involvement of electrical, calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Eitel JUH, Long DS, Gessler PE, Hunt ER (2008) Combined spectral index to improve ground-based estimates of nitrogen status in dryland wheat. Agronomy Journal 100, 1694–1702.
Combined spectral index to improve ground-based estimates of nitrogen status in dryland wheat.Crossref | GoogleScholarGoogle Scholar |

Evain S, Flexas J, Moya I (2004) A new instrument for passive remote sensing: 2. Measurement of leaf and canopy reflectance changes at 531 nm and their relationship with photosynthesis and chlorophyll fluorescence. Remote Sensing of Environment 91, 175–185.
A new instrument for passive remote sensing: 2. Measurement of leaf and canopy reflectance changes at 531 nm and their relationship with photosynthesis and chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |

Filella I, Porcar-Castell A, Munné-Bosch S, Bäck J, Garbulsky MF, Peñuelas J (2009) PRI assessment of long-term changes in carotenoids/chlorophyll ratio and short-term changes in de-epoxidation state of the xanthophyll cycle. International Journal of Remote Sensing 30, 4443–4455.
PRI assessment of long-term changes in carotenoids/chlorophyll ratio and short-term changes in de-epoxidation state of the xanthophyll cycle.Crossref | GoogleScholarGoogle Scholar |

Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant, Cell & Environment 30, 249–257.
Electrical signals and their physiological significance in plants.Crossref | GoogleScholarGoogle Scholar |

Gamon JA, Peñuelas J, Field CB (1992) A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment 41, 35–44.
A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency.Crossref | GoogleScholarGoogle Scholar |

Gamon JA, Huemmrich KF, Wong CY, Ensminger I, Garrity S, Hollinger DY, Noormets A, Peñuelas J (2016) A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers. Proceedings of the National Academy of Sciences of the United States of America 113, 13087–13092.
A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers.Crossref | GoogleScholarGoogle Scholar | 27803333PubMed |

Garbulsky MF, Peñuelas J, Gamon J, Inoue Y, Filella I (2011) The photochemical reflectance index (PRI) and the remote sensing of leaf, canopy and ecosystem radiation use efficiencies. A review and meta-analysis. Remote Sensing of Environment 115, 281–297.
The photochemical reflectance index (PRI) and the remote sensing of leaf, canopy and ecosystem radiation use efficiencies. A review and meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy A, Karpinski S, Mittler R (2016) ROS, calcium and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiology 171, 1606–1615.
ROS, calcium and electric signals: key mediators of rapid systemic signaling in plants.Crossref | GoogleScholarGoogle Scholar | 27208294PubMed |

Grams TEE, Lautner S, Felle HH, Matyssek R, Fromm J (2009) Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. Plant, Cell & Environment 32, 319–326.
Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf.Crossref | GoogleScholarGoogle Scholar |

Hilleary R, Gilroy S (2018) Systemic signaling in response to wounding and pathogens. Current Opinion in Plant Biology 43, 57–62.
Systemic signaling in response to wounding and pathogens.Crossref | GoogleScholarGoogle Scholar | 29351871PubMed |

Hlaváčková V, Krchňák P, Nauš J, Novák O, Špundová M, Strnad M (2006) Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta 225, 235–244.
Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning.Crossref | GoogleScholarGoogle Scholar | 16773374PubMed |

Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski P, Elsheery NI, Ferroni L, Guidi L, Hogewoning SW, Jajoo A, Misra AN, Nebauer SG, Pancaldi S, Penella C, Poli D, Pollastrini M, Romanowska-Duda ZB, Rutkowska B, Serôdio J, Suresh K, Szulc W, Tambussi E, Yanniccari M, Zivcak M (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynthesis Research 122, 121–158.
Frequently asked questions about in vivo chlorophyll fluorescence: practical issues.Crossref | GoogleScholarGoogle Scholar | 25119687PubMed |

Klughammer C, Schreiber U (2008) Saturation pulse method for assessment of energy conversion in PS I. PAM Application Notes 1, 11–14.

Krausko M, Perutka Z, Šebela M, Šamajová O, Šamaj J, Novák O, Pavlovič A (2017) The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis. New Phytologist 213, 1818–1835.
The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis.Crossref | GoogleScholarGoogle Scholar | 27933609PubMed |

Krupenina NA, Bulychev AA (2007) Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 1767, 781–788.
Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 17300741PubMed |

Liu L, Zhang Y, Jiao Q, Peng D (2013) Assessing photosynthetic light-use efficiency using a solar-induced chlorophyll fluorescence and photochemical reflectance index. International Journal of Remote Sensing 34, 4264–4280.
Assessing photosynthetic light-use efficiency using a solar-induced chlorophyll fluorescence and photochemical reflectance index.Crossref | GoogleScholarGoogle Scholar |

Magney TS, Eusden SA, Eitel JUH, Logan BA, Jiang J, Vierling LA (2014) Assessing leaf photoprotective mechanisms using terrestrial LiDAR: towards mapping canopy photosynthetic performance in three dimensions. New Phytologist 201, 344–356.
Assessing leaf photoprotective mechanisms using terrestrial LiDAR: towards mapping canopy photosynthetic performance in three dimensions.Crossref | GoogleScholarGoogle Scholar | 24032717PubMed |

Maxwell K, Johnson GN (2000) Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
Chlorophyll fluorescence – a practical guide.Crossref | GoogleScholarGoogle Scholar | 10938857PubMed |

Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2, ra45
The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli.Crossref | GoogleScholarGoogle Scholar | 19690331PubMed |

Osório J, Osório ML, Romano A (2012) Reflectance indices as nondestructive indicators of the physiological status of Ceratonia siliqua seedlings under varying moisture and temperature regimes. Functional Plant Biology 39, 588–597.
Reflectance indices as nondestructive indicators of the physiological status of Ceratonia siliqua seedlings under varying moisture and temperature regimes.Crossref | GoogleScholarGoogle Scholar |

Paulmann MK, Kunert G, Zimmermann MR, Theis N, Ludwig A, Meichsner D, Oelmüller R, Gershenzon J, Habekuss A, Ordon F, Furch ACU, Will T (2018) Barley yellow dwarf virus infection leads to higher chemical defense signals and lower electrophysiological reactions in susceptible compared to tolerant barley genotypes. Frontiers in Plant Science 9, 145
Barley yellow dwarf virus infection leads to higher chemical defense signals and lower electrophysiological reactions in susceptible compared to tolerant barley genotypes.Crossref | GoogleScholarGoogle Scholar | 29563918PubMed |

Pavlovič A, Slováková L, Pandolfi C, Mancuso S (2011) On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis). Journal of Experimental Botany 62, 1991–2000.
On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis).Crossref | GoogleScholarGoogle Scholar | 21289078PubMed |

Peñuelas J, Garbulsky MF, Filella I (2011) Photochemical reflectance index (PRI) and remote sensing of plant CO2 uptake. New Phytologist 191, 596–599.
Photochemical reflectance index (PRI) and remote sensing of plant CO2 uptake.Crossref | GoogleScholarGoogle Scholar | 21627667PubMed |

Porcar-Castell A, Garcia-Plazaola JI, Nichol CJ, Kolari P, Olascoaga B, Kuusinen N, Fernández-Marín B, Pulkkinen M, Juurola E, Nikinmaa E (2012) Physiology of the seasonal relationship between the photochemical reflectance index and photosynthetic light use efficiency. Oecologia 170, 313–323.
Physiology of the seasonal relationship between the photochemical reflectance index and photosynthetic light use efficiency.Crossref | GoogleScholarGoogle Scholar | 22481306PubMed |

Porcar-Castell A, Tyystjärvi E, Atherton J, van der Tol C, Flexas J, Pfündel EE, Moreno J, Frankenberg C, Berry JA (2014) Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges. Journal of Experimental Botany 65, 4065–4095.
Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges.Crossref | GoogleScholarGoogle Scholar | 24868038PubMed |

Rahimzadeh-Bajgiran P, Munehiro M, Omasa K (2012) Relationships between the photochemical reflectance index (PRI) and chlorophyll fluorescence parameters and plant pigment indices at different leaf growth stages. Photosynthesis Research 113, 261–271.
Relationships between the photochemical reflectance index (PRI) and chlorophyll fluorescence parameters and plant pigment indices at different leaf growth stages.Crossref | GoogleScholarGoogle Scholar | 22644476PubMed |

Retivin VG, Opritov VA, Lobov SA, Tarakanov SA, Khudyakov VA (1999) Changes in the resistance of photosynthesizing cotyledon cells of pumpkin seedlings to cooling and heating, as induced by the stimulation of the root system with KCl solution. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 46, 689–696.

Ripullone F, Rivelli AR, Baraldi R, Guarini R, Guerrieri R, Magnani F, Peñuelas J, Raddi S, Borghetti M (2011) Effectiveness of the photochemical reflectance index to track photosynthetic activity over a range of forest tree species and plant water statuses. Functional Plant Biology 38, 177–186.
Effectiveness of the photochemical reflectance index to track photosynthetic activity over a range of forest tree species and plant water statuses.Crossref | GoogleScholarGoogle Scholar |

Ruban AV (2015) Evolution under the sun: optimizing light harvesting in photosynthesis. Journal of Experimental Botany 66, 7–23.
Evolution under the sun: optimizing light harvesting in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 25336689PubMed |

Sherstneva ON, Vodeneev VA, Katicheva LA, Surova LM, Sukhov VS (2015) Participation of intracellular and extracellular pH changes in photosynthetic response development induced by variation potential in pumpkin seedlings. Biochemistry (Moscow) 80, 776–784.
Participation of intracellular and extracellular pH changes in photosynthetic response development induced by variation potential in pumpkin seedlings.Crossref | GoogleScholarGoogle Scholar |

Sherstneva ON, Surova LM, Vodeneev VA, Plotnikova YI, Bushueva AV, Sukhov VS (2016a) The role of the intra- and extracellular protons in the photosynthetic response induced by the variation potential in pea seedlings. Biochemistry (Moscow). Supplement Series A: Membrane and Cell Biology 10, 60–67.
The role of the intra- and extracellular protons in the photosynthetic response induced by the variation potential in pea seedlings.Crossref | GoogleScholarGoogle Scholar |

Sherstneva ON, Vodeneev VA, Surova LM, Novikova EM, Sukhov VS (2016b) Application of a mathematical model of variation potential for analysis of its influence on photosynthesis in higher plants. Biochemistry (Moscow). Supplement Series A: Membrane and Cell Biology 10, 269–277.
Application of a mathematical model of variation potential for analysis of its influence on photosynthesis in higher plants.Crossref | GoogleScholarGoogle Scholar |

Souza GM, Lüttge U (2015) Stability as a phenomenon emergent from plasticity–complexity–diversity in eco-physiology. In ‘Progress in botany. Vol. 76’. (Eds U Lüttge, W Beyschlag) pp. 277–290. (Springer: Berlin)

Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynthesis Research 130, 373–387.
Electrical signals as mechanism of photosynthesis regulation in plants.Crossref | GoogleScholarGoogle Scholar | 27154573PubMed |

Sukhov V, Orlova L, Mysyagin S, Sinitsina J, Vodeneev V (2012) Analysis of the photosynthetic response induced by variation potential in geranium. Planta 235, 703–712.
Analysis of the photosynthetic response induced by variation potential in geranium.Crossref | GoogleScholarGoogle Scholar | 22020752PubMed |

Sukhov V, Sherstneva O, Surova L, Katicheva L, Vodeneev V (2014a) Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea. Plant, Cell & Environment 37, 2532–2541.
Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea.Crossref | GoogleScholarGoogle Scholar |

Sukhov V, Surova L, Sherstneva O, Vodeneev V (2014b) Influence of variation potential on resistance of the photosynthetic machinery to heating in pea. Physiologia Plantarum 152, 773–783.
Influence of variation potential on resistance of the photosynthetic machinery to heating in pea.Crossref | GoogleScholarGoogle Scholar | 24730552PubMed |

Sukhov V, Surova L, Sherstneva O, Katicheva L, Vodeneev V (2015a) Variation potential influence on photosynthetic cyclic electron flow in pea. Frontiers in Plant Science 5, 766
Variation potential influence on photosynthetic cyclic electron flow in pea.Crossref | GoogleScholarGoogle Scholar | 25610447PubMed |

Sukhov V, Surova L, Sherstneva O, Bushueva A, Vodeneev V (2015b) Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea. Functional Plant Biology 42, 727–736.
Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea.Crossref | GoogleScholarGoogle Scholar |

Sukhov V, Surova L, Morozova E, Sherstneva O, Vodeneev V (2016) Changes in H+-ATP synthase activity, proton electrochemical gradient, and pH in pea chloroplast can be connected with variation potential. Frontiers in Plant Science 7, 1092
Changes in H+-ATP synthase activity, proton electrochemical gradient, and pH in pea chloroplast can be connected with variation potential.Crossref | GoogleScholarGoogle Scholar | 27499760PubMed |

Sukhov V, Gaspirovich V, Mysyagin S, Vodeneev V (2017) High-temperature tolerance of photosynthesis can be linked to local electrical responses in leaves of pea. Frontiers in Physiology 8, 763
High-temperature tolerance of photosynthesis can be linked to local electrical responses in leaves of pea.Crossref | GoogleScholarGoogle Scholar | 29033854PubMed |

Sukhova E, Sukhov V (2018a) Connection of the photochemical reflectance index (PRI) with the photosystem II quantum yield and nonphotochemical quenching can be dependent on variations of photosynthetic parameters among investigated plants: a meta-analysis. Remote Sensing 10, 771
Connection of the photochemical reflectance index (PRI) with the photosystem II quantum yield and nonphotochemical quenching can be dependent on variations of photosynthetic parameters among investigated plants: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Sukhova EM, Sukhov VS (2018b) Dependence of the CO2 uptake in a plant cell on the plasma membrane H+-ATPase activity: theoretical analysis. Biochemistry (Moscow). Supplement Series A: Membrane and Cell Biology 12, 146–159.
Dependence of the CO2 uptake in a plant cell on the plasma membrane H+-ATPase activity: theoretical analysis.Crossref | GoogleScholarGoogle Scholar |

Sukhova E, Akinchits E, Sukhov V (2017) Mathematical models of electrical activity in plants. The Journal of Membrane Biology 250, 407–423.
Mathematical models of electrical activity in plants.Crossref | GoogleScholarGoogle Scholar | 28711950PubMed |

Sukhova E, Mudrilov M, Vodeneev V, Sukhov V (2018) Influence of the variation potential on photosynthetic flows of light energy and electrons in pea. Photosynthesis Research 136, 215–228.
Influence of the variation potential on photosynthetic flows of light energy and electrons in pea.Crossref | GoogleScholarGoogle Scholar | 29086893PubMed |

Surova L, Sherstneva O, Vodeneev V, Katicheva L, Semina M, Sukhov V (2016a) Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves. Journal of Plant Physiology 202, 57–64.
Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves.Crossref | GoogleScholarGoogle Scholar | 27450494PubMed |

Surova L, Sherstneva O, Vodeneev V, Sukhov V (2016b) Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways. Plant Signaling & Behavior 11, e1145334
Variation potential propagation decreases heat-related damage of pea photosystem I by 2 different pathways.Crossref | GoogleScholarGoogle Scholar |

Szechyńska-Hebda M, Lewandowska M, Karpiński S (2017) Electrical signaling, photosynthesis and systemic acquired acclimation. Frontiers in Physiology 8, 684
Electrical signaling, photosynthesis and systemic acquired acclimation.Crossref | GoogleScholarGoogle Scholar | 28959209PubMed |

Trebacz K, Dziubinska H, Krol E (2006) Electrical signals in long distance communication in plants. In ‘Communication in plants. Neuronal aspects of plant life’. (Eds F Baluska, S Mancuso, D Volkmann) pp. 277–290. (Springer: Berlin)

Vítolo HF, Souza GM, Silveira JAG (2012) Cross-scale multivariate analysis of physiological responses to high temperature in two tropical crops with C3 and C4 metabolism. Environmental and Experimental Botany 80, 54–62.
Cross-scale multivariate analysis of physiological responses to high temperature in two tropical crops with C3 and C4 metabolism.Crossref | GoogleScholarGoogle Scholar |

Vodeneev VA, Akinchits EK, Orlova LA, Sukhov VS (2011) The role of Ca2+, H+, and Cl− ions in generation of variation potential in pumpkin plants. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 58, 974–981.
The role of Ca2+, H+, and Cl ions in generation of variation potential in pumpkin plants.Crossref | GoogleScholarGoogle Scholar |

Vodeneev V, Akinchits E, Sukhov V (2015) Variation potential in higher plants: mechanisms of generation and propagation. Plant Signaling & Behavior 10, e1057365
Variation potential in higher plants: mechanisms of generation and propagation.Crossref | GoogleScholarGoogle Scholar |

Vodeneev V, Mudrilov M, Akinchits E, Balalaeva I, Sukhov V (2018) Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus. Functional Plant Biology 45, 160–170.
Parameters of electrical signals and photosynthetic responses induced by them in pea seedlings depend on the nature of stimulus.Crossref | GoogleScholarGoogle Scholar |

Vredenberg W, Pavlovič A (2013) Chlorophyll a fluorescence induction (Kautsky curve) in a Venus flytrap (Dionaea muscipula) leaf after mechanical trigger hair irritation. Journal of Plant Physiology 170, 242–250.
Chlorophyll a fluorescence induction (Kautsky curve) in a Venus flytrap (Dionaea muscipula) leaf after mechanical trigger hair irritation.Crossref | GoogleScholarGoogle Scholar | 23177088PubMed |

Wahabzada M, Mahlein AK, Bauckhage C, Steiner U, Oerke EC, Kersting K (2016) Plant phenotyping using probabilistic topic models: uncovering the hyperspectral language of plants. Scientific Reports 6, 22482
Plant phenotyping using probabilistic topic models: uncovering the hyperspectral language of plants.Crossref | GoogleScholarGoogle Scholar | 26957018PubMed |

Zhang C, Filella I, Garbulsky MF, Peñuelas J (2016) Affecting factors and recent improvements of the photochemical reflectance index (PRI) for remotely sensing foliar, canopy and ecosystemic radiation-use efficiencies. Remote Sensing 8, 677
Affecting factors and recent improvements of the photochemical reflectance index (PRI) for remotely sensing foliar, canopy and ecosystemic radiation-use efficiencies.Crossref | GoogleScholarGoogle Scholar |

Zimmermann MR, Maischak H, Mithoefer A, Boland W, Felle HH (2009) System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiology 149, 1593–1600.
System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding.Crossref | GoogleScholarGoogle Scholar | 19129416PubMed |

Zinnert JC, Nelson JD, Hoffman AM (2012) Effects of salinity on physiological responses and the photochemical reflectance index in two co-occurring coastal shrubs. Plant and Soil 354, 45–55.
Effects of salinity on physiological responses and the photochemical reflectance index in two co-occurring coastal shrubs.Crossref | GoogleScholarGoogle Scholar |