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

Biochemical constrains limit the potential of the photochemical reflectance index as a predictor of effective quantum efficiency of photosynthesis during the winter spring transition in Jack pine seedlings

Florian Busch A B D E , Norman P. A. Hüner A and Ingo Ensminger A C
+ Author Affiliations
- Author Affiliations

A Department of Biology and The BIOTRON, The University of Western Ontario, London, ON N6A 5B7, Canada.

B Institute of Chemistry and Dynamics of the Geosphere ICG-III: Phytosphere, Research Centre Jülich, 52425 Jülich, Germany.

C Department of Cell and Systems Biology, University of Toronto, Mississauga, ON L5 L 1C6, Canada.

D Present address: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON M5S 3B2, Canada.

E Corresponding author. Email: florian.busch@utoronto.ca

Functional Plant Biology 36(11) 1016-1026 https://doi.org/10.1071/FP08043
Submitted: 5 March 2009  Accepted: 21 September 2009   Published: 5 November 2009

Abstract

Leaf reflectance spectral measurements are an emerging non-invasive technique that can be used to derive the photochemical reflectance index (PRI) to assess the physiological state of plants from leaf to ecosystem level. Changes in PRI are associated with changes in the xanthophyll cycle activity and provide an estimate of changes in the effective photochemical quantum efficiency (ΦII) during the growing season. However, we hypothesised that the correlation between PRI and ΦII might be poor when the xanthophyll cycle is primed for sustained thermal dissipation of the light energy absorbed. To test our hypothesis, we studied the recovery of winter acclimated Jack pine (Pinus banksiana Lamb.) seedlings that were exposed to different simulated spring recovery treatments in controlled environments. Different growth temperatures and light intensities were used to dissect the effect of these two factors on chlorophyll fluorescence, pigment composition and leaf reflectance. ΦII showed a clear response to temperature whereas PRI was mostly affected by light intensity. In contrast, the de-epoxidation state of the xanthophyll cycle pigments was both temperature and light dependent. Our data suggest that zeaxanthin-independent non-photochemical quenching is employed to various degrees in the different treatments. As a result, within the limits of our experimental setup, PRI could not explain the variation in ΦII. This indicates that an improved understanding of the different energy quenching mechanisms is critical to accurately interpret the PRI signal under environmental conditions where the predominant mode of excess energy dissipation does not involve a dynamic operation of the xanthophyll cycle, but a sustained mechanism of energy dissipation.

Additional keywords: chlorophyll a fluorescence, dehardening, PRI, xanthophyll cycle, zeaxanthin.


Acknowledgements

We thank Lawrence B. Flanagan for providing us with the spectroradiometer as well as Rebecca Zener for assisting with the data collection. We are also grateful to Heather Coiner and three unknown reviewers who provided helpful comments that greatly improved the quality of the manuscript. I.E. was supported by a Marie-Curie fellowship of the EU (PhysConFor, contract no. MOIF-CT-2004–002476). Financial support from NSERC and Canada Foundation for Innovation to N.P.A.H. is gratefully acknowledged.


References


Adams WW, Demmig-Adams B (1994) Carotenoid composition and down regulation of photosystem II in three conifer species during the winter. Physiologia Plantarum 92, 451–458.
CrossRef | CAS |

Adams WW , Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In ‘Advances in photosynthesis and respiration – chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindjee) pp. 583–604. (Springer: Dordrecht, The Netherlands)

Adams WW, Demmig-Adams B, Rosenstiel TN, Ebbert V (2001) Dependence of photosynthesis and energy dissipation activity upon growth form and light environment during the winter. Photosynthesis Research 67, 51–62.
CrossRef | CAS | PubMed |

Amiro BD, Barr AG, Black TA, Iwashita H, Kljun N , et al . (2006) Carbon, energy and water fluxes at mature and disturbed forest sites, Saskatchewan, Canada. Agricultural and Forest Meteorology 136, 237–251.
CrossRef |

Ananyev G, Kolber ZS, Klimov D, Falkowski PG, Berry JA, Rascher U, Martin R, Osmond B (2005) Remote sensing of heterogeneity in photosynthetic efficiency, electron transport and dissipation of excess light in Populus deltoides stands under ambient and elevated CO2 concentrations, and in a tropical forest canopy, using a new laser-induced fluorescence transient device. Global Change Biology 11, 1195–1206.
CrossRef |

Barr AG, Black TA, Hogg EH, Kljun N, Morgenstern K, Nesic Z (2004) Inter-annual variability in the leaf area index of a boreal aspen-hazelnut forest in relation to net ecosystem production. Agricultural and Forest Meteorology 126, 237–255.
CrossRef |

Barták M, Hajek J, Vrablikova H, Dubova J (2004) High-light stress and photoprotection in Umbilicaria antarctica monitored by chlorophyll fluorescence Imaging and changes in zeaxanthin and glutathione. Plant Biology 6, 333–341.
CrossRef | PubMed |

Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbency changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research 25, 173–185.
CrossRef | CAS |

Busch F, Hüner NPA, Ensminger I (2007) Increased air temperature during simulated autumn conditions does not increase photosynthetic carbon gain but affects the dissipation of excess energy in seedlings of the evergreen Conifer Jack Pine. Plant Physiology 143, 1242–1251.
CrossRef | CAS | PubMed |

Busch F, Hüner NPA, Ensminger I (2008) Increased air temperature during simulated autumn conditions impairs photosynthetic electron transport between photosystem II and photosystem I. Plant Physiology 147, 402–414.
CrossRef | CAS | PubMed |

Casper-Lindley C, Björkman O (1998) Fluorescence quenching in four unicellular algae with different light-harvesting and xanthophyll-cycle pigments. Photosynthesis Research 56, 277–289.
CrossRef | CAS |

Demmig-Adams B, Adams WW (1996a) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1, 21–26.
CrossRef |

Demmig-Adams B, Adams WW (1996b) Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198, 460–470.
CrossRef | CAS |

Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172, 11–21.
CrossRef | CAS | PubMed |

Demmig-Adams B, Gilmore AM, Adams WW (1996) Carotenoids 3. In vivo functions of carotenoids in higher plants. The FASEB Journal 10, 403–412.
CAS | PubMed |


Drolet GG, Huemmrich KF, Hall FG, Middleton EM, Black TA, Barr AG, Margolis HA (2005) A MODIS-derived photochemical reflectance index to detect inter-annual variations in the photosynthetic light-use efficiency of a boreal deciduous forest. Remote Sensing of Environment 98, 212–224.
CrossRef |

Ensminger I, Xylander M, Hagen C, Braune W (2001) Strategies providing success in a variable habitat: III. Dynamic control of photosynthesis in Cladophora glomerata. Plant, Cell & Environment 24, 769–779.
CrossRef | CAS |

Ensminger I, Sveshnikov D, Campbell DA, Funk C, Jansson S, Lloyd J, Shibistova O, Öquist G (2004) Intermittent low temperatures constrain spring recovery of photosynthesis in boreal Scots pine forests. Global Change Biology 10, 995–1008.
CrossRef |

Ensminger I, Busch F, Hüner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiologia Plantarum 126, 28–44.
CrossRef | CAS |

Ensminger I, Schmidt L, Lloyd J (2008) Soil temperature and intermittent frost modulate the rate of recovery of photosynthesis in Scots pine under simulated spring conditions. New Phytologist 177, 428–442.
CAS | PubMed |


Filella I, Peñuelas J, Llorens L, Estiarte M (2004) Reflectance assessment of seasonal and annual changes in biomass and CO2 uptake of a Mediterranean shrubland submitted to experimental warming and drought. Remote Sensing of Environment 90, 308–318.
CrossRef |

Gamon JA, Field CB, Bilger W, Björkman O, Fredeen AL, Peñuelas J (1990) Remote-sensing of the xanthophyll cycle and chlorophyll fluorescence in sunflower leaves and canopies. Oecologia 85, 1–7.
CrossRef |

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.
CrossRef |

Gamon JA, Serrano L, Surfus JS (1997) The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. Oecologia 112, 492–501.
CrossRef |

Gamon JA, Field CB, Fredeen AL, Thayer S (2001) Assessing photosynthetic downregulation in sunflower stands with an optically-based model. Photosynthesis Research 67, 113–125.
CrossRef | CAS | PubMed |

Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
CAS |


Gilmore AM, Ball MC (2000) Protection and storage of chlorophyll in overwintering evergreens. Proceedings of the National Academy of Sciences of the United States of America 97, 11 098–11 101.
CrossRef | CAS | PubMed |

Gilmore AM, Hazlett TL, Debrunner PG, Govindjee (1996) Photosystem II chlorophyll a fluorescence lifetimes and intensity are independent of the antenna size differences between barley wild-type and chlorina mutants: photochemical quenching and xanthophyll cycle-dependent nonphotochemical quenching of fluorescence. Photosynthesis Research 48, 171–187.
CrossRef | CAS |

Hall FG , Betts AK , Frolking S , Brown R , Chen JM , Chen W , Halldin S , Lettenmaier DP , Schafer J (2004) The boreal climate. In ‘Vegetation, water, humans and the climate: a new perspective on an interactive system’. (Eds P Kabat, M Claussen, PA Dirmeyer, JHC Gash, LB Deguenni, M Meybeck, RA Pielke, CJ Vörösmarty, RWA Hutjes, S Lütkemeier) pp. 93–114. (Springer Verlag: Berlin)

Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll protein complex. FEBS Letters 292, 1–4.
CrossRef | CAS | PubMed |

Hurry VM, Krol M, Öquist G, Huner NPA (1992) Effect of long-term photoinhibition on growth and photosynthesis of cold-hardened spring and winter wheat. Planta 188, 369–375.
CrossRef | CAS |

Ivanov AG, Sane PV, Zeinalov Y, Simidjiev I, Huner NPA, Öquist G (2002) Seasonal responses of photosynthetic electron transport in Scots pine (Pinus sylvestris L.) studied by thermoluminescence. Planta 215, 457–465.
CrossRef | CAS | PubMed |

Ivanov AG, Sane PV, Hurry V, Oquist G, Huner NPA (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynthesis Research 98, 565–574.
CrossRef | CAS | PubMed |

Johnson MP, Davison PA, Ruban AV, Horton P (2008) The xanthophyll cycle pool size controls the kinetics of non-photochemical quenching in Arabidopsis thaliana. FEBS Letters 582, 262–266.
CrossRef | CAS | PubMed |

Kornyeyev D, Holaday AS (2008) Corrections to current approaches used to calculate energy partitioning in photosystem II. Photosynthetica 46, 170–178.
CrossRef | CAS |

Krol M, Hurry V, Maxwell DP, Malek L, Ivanov AG, Huner NPA (2002) Low growth temperature inhibition of photosynthesis in cotyledons of jack pine seedlings (Pinus banksiana) is due to impaired chloroplast development. Canadian Journal of Botany 80, 1042–1051.
CrossRef |

Nichol CJ, Huemmrich KF, Black TA, Jarvis PG, Walthall CL, Grace J, Hall FG (2000) Remote sensing of photosynthetic-light-use efficiency of boreal forest. Agricultural and Forest Meteorology 101, 131–142.
CrossRef |

Nichol CJ, Lloyd J, Shibistova O, Arneth A, Roser C, Knohl A, Matsubara S, Grace J (2002) Remote sensing of photosynthetic-light-use efficiency of a Siberian boreal forest. Tellus. Series B, Chemical and Physical Meteorology 54, 677–687.
CrossRef |

Ottander C, Campbell D, Öquist G (1995) Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris. Planta 197, 176–183.
CrossRef | CAS |

Peñuelas J, Filella I, Gamon JA (1995) Assessment of photosynthetic radiation-use efficiency with spectral reflectance. New Phytologist 131, 291–296.
CrossRef |

Peñuelas J, Llusia J, Pinol J, Filella I (1997) Photochemical reflectance index and leaf photosynthetic radiation-use-efficiency assessment in Mediterranean trees. International Journal of Remote Sensing 18, 2863–2868.
CrossRef |

Rascher U, Pieruschka R (2008) Spatio–temporal variations of photosynthesis: the potential of optical remote sensing to better understand and scale light use efficiency and stresses of plant ecosystems. Precision Agriculture 9, 355–366.
CrossRef |

Repo T, Kalliokoski T, Domisch T, Lehto T, Mannerkoski H, Sutinen S, Finer L (2005) Effects of timing of soil frost thawing on Scots pine. Tree Physiology 25, 1053–1062.
PubMed |


Ruban AV, Young AJ, Horton P (1993) Induction of non-photochemical energy-dissipation and absorbency changes in leaves – evidence for changes in the state of the light-harvesting system of photosystem II in vivo. Plant Physiology 102, 741–750.
CAS | PubMed |


Soukupová J, Cséfalvay L, Urban O, Košvancová M, Marek M, Rascher U, Nedbal L (2008) Annual variation of the steady-state chlorophyll fluorescence emission of evergreen plants in temperate zone. Functional Plant Biology 35, 63–76.
CrossRef |

Stylinski CD, Gamon JA, Oechel WC (2002) Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species. Oecologia 131, 366–374.
CrossRef |

Trotter GM, Whitehead D, Pinkney EJ (2002) The photochemical reflectance index as a measure of photosynthetic light use efficiency for plants with varying foliar nitrogen contents. International Journal of Remote Sensing 23, 1207–1212.
CrossRef |

Verhoeven AS, Adams WW, Demmig-Adams B (1996) Close relationship between the state of the xanthophyll cycle pigments and photosystem II efficiency during recovery from winter stress. Physiologia Plantarum 96, 567–576.
CrossRef | CAS |

Weng JH, Chen YN, Liao TS (2006) Relationships between chlorophyll fluorescence parameters and photochemical reflectance index of tree species adapted to different temperature regimes. Functional Plant Biology 33, 241–246.
CrossRef | CAS |

Zarter CR, Adams WW, Ebbert V, Adamska I, Jansson S, Demmig-Adams B (2006) Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment. Plant, Cell & Environment 29, 869–878.
CrossRef | CAS | PubMed |








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