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

Assessing the xanthophyll cycle in natural beech leaves with hyperspectral reflectance

Rei Sonobe A and Quan Wang A B
+ Author Affiliations
- Author Affiliations

A Faculty of Agriculture, Shizuoka University, 836 Ohya, Shizuoka 422-8529, Japan.

B Corresponding author. Email: wang.quan@shizuoka.ac.jp

Functional Plant Biology 43(5) 438-447 https://doi.org/10.1071/FP15325
Submitted: 16 October 2015  Accepted: 14 January 2016   Published: 19 February 2016

Abstract

The xanthophyll cycle is critical for protecting the photosynthetic apparatus from light-induced oxidative stress. A clear view of the xanthophyll cycle is thus important for understanding abiotic stresses that are closely related to plant growth and reproduction. The epoxidation state (EPS) is well correlated with the photosynthetic radiation use efficiency, and is widely used for assessing the xanthophyll cycle. The hyperspectral index, photochemical reflectance index (PRI), has been claimed to be closely related with the EPS, and offers instantaneous information of photosynthetic activity: its applications are, however, largely limited to herbaceous and coniferous species, and few studies have ever focussed on both sunlit and shaded leaves of deciduous plants. In the present study, we examined the possibility of applying PRI for tracing the xanthophyll cycle in a typical deciduous species (Fagus crenata Blume) as well as other species in a cold-temperate mountainous area. This is based on a series of experiments with only light stress and other inhibited treatments. Furthermore, searching for new hyperspectral indices has also been attempted based on both original and first derivative spectra. Results revealed that PRI had low correlations with the EPS of deciduous leaves, especially for sunlit leaves. As a comparison, the newly identified dD677, 803, a differential type of index using reflectance derivatives at 677 and 803 nm, had a much better performance. The robustness of the newly identified index has been confirmed from both inhibitor-treatments and an additional dataset from other deciduous species. The proposed index is hence applicable for tracing the xanthophyll cycle in deciduous species.

Additional keywords: derivative spectra, EPS, PRI, shaded leaf, sunlit leaf.


References

Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In ‘Proceedings of the 2nd international symposium on information theory’. pp. 267–291. (Akademiai Kiado: Budapest, Hungary)

Akaike H (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.
A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |

Asensio D, Penuelas J, Ogaya R, Llusia J (2007) Seasonal soil and leaf CO2 exchange rates in a mediterranean holm oak forest and their responses to drought conditions. Atmospheric Environment 41, 2447–2455.
Seasonal soil and leaf CO2 exchange rates in a mediterranean holm oak forest and their responses to drought conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitFSrsrc%3D&md5=b773311e2bb61c450ebae8124b8d0534CAS |

Barton CVM, North PRJ (2001) Remote sensing of canopy light use efficiency using the photochemical reflectance index – model and sensitivity analysis. Remote Sensing of Environment 78, 264–273.
Remote sensing of canopy light use efficiency using the photochemical reflectance index – model and sensitivity analysis.Crossref | GoogleScholarGoogle Scholar |

Bilger W, Bjorkman O, Thayer SS (1989) Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves. Plant Physiology 91, 542–551.
Light-induced spectral absorbance changes in relation to photosynthesis and the epoxidation state of xanthophyll cycle components in cotton leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXks1Kn&md5=399802914da2994862e953087fa3ed18CAS | 16667067PubMed |

Bulda OV, Rassadina VV, Alekseichuk HN, Laman NA (2008) Spectrophotometric measurement of carotenes, xanthophylls, and chlorophylls in extracts from plant seeds. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 55, 544–551.
Spectrophotometric measurement of carotenes, xanthophylls, and chlorophylls in extracts from plant seeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVGjsLs%3D&md5=f079dbf8d21e33da942b59e8ba191268CAS |

Burns RP, Burns R (2008) Business research methods and statistics using SPSS. Available at: https://books.google.co.jp/books?id=bPvCRzBou3gC [Verified 8 February 2016]

Demetriades-Shah TH, Steven MD, Clark JA (1990) High-resolution derivative spectra in remote-sensing. Remote Sensing of Environment 33, 55–64.
High-resolution derivative spectra in remote-sensing.Crossref | GoogleScholarGoogle Scholar |

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

Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytologist 172, 11–21.
Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVyisrnE&md5=e3817291ef4998512b680ac4c2baabb7CAS | 16945085PubMed |

Draper NH (1998) ‘Applied regression analysis.’ (Wiley Interscience: New York, NY)

Filella I, Amaro T, Araus JL, Penuelas J (1996) Relationship between photosynthetic radiation-use efficiency of barley canopies and the photochemical reflectance index (PRI). Physiologia Plantarum 96, 211–216.
Relationship between photosynthetic radiation-use efficiency of barley canopies and the photochemical reflectance index (PRI).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XivFeksbY%3D&md5=2c94deec5a7f79527584332074ceb03bCAS |

Filella I, Porcar-Castell A, Munne-Bosch S, Back J, Garbulsky MF, Penuelas 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 |

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

Gamon JA, Penuelas 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, 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.
The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels.Crossref | GoogleScholarGoogle Scholar |

Gamon JA, Rahman AF, Dungan JL, Schildhauer M, Huemmrich KF (2006) Spectral network (specnet) – what is it and why do we need it? Remote Sensing of Environment 103, 227–235.
Spectral network (specnet) – what is it and why do we need it?Crossref | GoogleScholarGoogle Scholar |

Garbulsky MF, Penuelas 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 |

Goerner A, Reichstein M, Tomelleri E, Hanan N, Rambal S, Papale D, Dragoni D, Schmullius C (2011) Remote sensing of ecosystem light use efficiency with modis-based PRI. Biogeosciences 8, 189–202.
Remote sensing of ecosystem light use efficiency with modis-based PRI.Crossref | GoogleScholarGoogle Scholar |

Grace J, Nichol C, Disney M, Lewis P, Quaife T, Bowyer P (2007) Can we measure terrestrial photosynthesis from space directly, using spectral reflectance and fluorescence? Global Change Biology 13, 1484–1497.
Can we measure terrestrial photosynthesis from space directly, using spectral reflectance and fluorescence?Crossref | GoogleScholarGoogle Scholar |

Guyot G 1990. Optical properties of vegetation canopies. In ‘Applications of remote sensing in agriculture’. (Eds MD Steven, JA Clark)pp. 19–43. (Butterworths: London)

Hardy JT, Hoge FE, Yungel JK, Dodge RE (1992) Remote detection of coral bleaching using pulsed-laser fluorescence spectroscopy. Marine Ecology Progress Series 88, 247–255.
Remote detection of coral bleaching using pulsed-laser fluorescence spectroscopy.Crossref | GoogleScholarGoogle Scholar |

Howarth JF, Durako MJ (2013) Variation in pigment content of Thalassia testudinum seedlings in response to changes in salinity and light. Botanica Marina 56, 261–273.
Variation in pigment content of Thalassia testudinum seedlings in response to changes in salinity and light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXntlylurs%3D&md5=df848ab11fba9d180b358f047d6d9fa2CAS |

Kawabata Y, Takeda S (2014) Regulation of xanthophyll cycle pool size in response to high light irradiance in Arabidopsis. Plant Biotechnology 31, 229–240.
Regulation of xanthophyll cycle pool size in response to high light irradiance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXosV2itA%3D%3D&md5=521d258325af59c1547b383a48a0398eCAS |

Krause GH, Vernotte C, Briantais JM (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components. Biochimica et Biophysica Acta (BBA) – Bioenergetics 679, 116–124.
Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjtFyiuw%3D%3D&md5=d3c055782d61a14627b77ad820cd4a5fCAS |

Liu J, Li P, Wang X (2015) A new segmentation method for very high resolution imagery using spectral and morphological information. ISPRS Journal of Photogrammetry and Remote Sensing 101, 145–162.
A new segmentation method for very high resolution imagery using spectral and morphological information.Crossref | GoogleScholarGoogle Scholar |

Miszalski Z, Kornas A, Rozpadek P, Fischer-Schliebs E, Luettge U (2013) Independent fluctuations of malate and citrate in the cam species Clusia hilariana schltdl. under low light and high light in relation to photoprotection. Journal of Plant Physiology 170, 453–458.
Independent fluctuations of malate and citrate in the cam species Clusia hilariana schltdl. under low light and high light in relation to photoprotection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVCrs73M&md5=d388cc02575f8aa9516ad5305a187b60CAS | 23253483PubMed |

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.
Remote sensing of photosynthetic-light-use efficiency of boreal forest.Crossref | GoogleScholarGoogle Scholar |

Powles S (1984) Photoinhibition of photosynthesis induced by visible light. Annual Review of Plant Physiology 35, 15–44.
Photoinhibition of photosynthesis induced by visible light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXlt1KktLY%3D&md5=d44d74507e07d15e2159e70123f78226CAS |

Sha Z, Brown DG, Xie Y, Welsh WF, Bai Y (2014) Response of spectral vegetation indices to a stocking rate experiment in inner Mongolia, China. Remote Sensing Letters 5, 912–921.
Response of spectral vegetation indices to a stocking rate experiment in inner Mongolia, China.Crossref | GoogleScholarGoogle Scholar |

Shaw BP (1995) Changes in the levels of photosynthetic pigments in Phaseolus aureus Roxb. exposed to Hg and Cd at 2 stages of development: a comparative-study. Bulletin of Environmental Contamination and Toxicology 55, 574–580.
Changes in the levels of photosynthetic pigments in Phaseolus aureus Roxb. exposed to Hg and Cd at 2 stages of development: a comparative-study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXns1ejtro%3D&md5=919ed1cbfe072a1e882bad5357cfabc1CAS | 8555683PubMed |

Shay P-E, Kubien DS (2013) Field analysis of photoprotection in co-occurring cool climate C3 and C4 grasses. Physiologia Plantarum 147, 316–328.
Field analysis of photoprotection in co-occurring cool climate C3 and C4 grasses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltlGqu7k%3D&md5=996db59e36da790cf6d5b58ce6554753CAS | 22672001PubMed |

Simionato D, Basso S, Zaffagnini M, Lana T, Marzotto F, Trost P, Morosinotto T (2015) Protein redox regulation in the thylakoid lumen: the importance of disulfide bonds for violaxanthin de-epoxidase. FEBS Letters 589, 919–923.
Protein redox regulation in the thylakoid lumen: the importance of disulfide bonds for violaxanthin de-epoxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXktFeiu7w%3D&md5=5cd4b1df562443c6594780c5d8748251CAS | 25747136PubMed |

Song C, White BL, Heumann BW (2011) Hyperspectral remote sensing of salinity stress on red (Rhizophora mangle) and white (Laguncularia racemosa) mangroves on Galapagos Islands. Remote Sensing Letters 2, 221–230.
Hyperspectral remote sensing of salinity stress on red (Rhizophora mangle) and white (Laguncularia racemosa) mangroves on Galapagos Islands.Crossref | GoogleScholarGoogle Scholar |

Stagakis S, Markos N, Sykioti O, Kyparissis A (2014) Tracking seasonal changes of leaf and canopy light use efficiency in a Phlomis fruticosa mediterranean ecosystem using field measurements and multi-angular satellite hyperspectral imagery. ISPRS Journal of Photogrammetry and Remote Sensing 97, 138–151.
Tracking seasonal changes of leaf and canopy light use efficiency in a Phlomis fruticosa mediterranean ecosystem using field measurements and multi-angular satellite hyperspectral imagery.Crossref | GoogleScholarGoogle Scholar |

Suárez L, Zarco-Tejada PJ, González-Dugo V, Berni JAJ, Sagardoy R, Morales F, Fereres E (2010) Detecting water stress effects on fruit quality in orchards with time-series PRI airborne imagery. Remote Sensing of Environment 114, 286–298.
Detecting water stress effects on fruit quality in orchards with time-series PRI airborne imagery.Crossref | GoogleScholarGoogle Scholar |

Thayer SS, Bjorkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331–343.
Leaf xanthophyll content and composition in sun and shade determined by HPLC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslGrtr4%3D&md5=735130a511386c0a39ca2f53112ec1efCAS | 24419657PubMed |

Tsai F, Philpot W (1998) Derivative analysis of hyperspectral data. Remote Sensing of Environment 66, 41–51.
Derivative analysis of hyperspectral data.Crossref | GoogleScholarGoogle Scholar |

Wang Q, Iio A, Kakubari Y (2008a) Broadband simple ratio closely traced seasonal trajectory of canopy photosynthetic capacity. Geophysical Research Letters 35, L07401
Broadband simple ratio closely traced seasonal trajectory of canopy photosynthetic capacity.Crossref | GoogleScholarGoogle Scholar |

Wang Q, Iio A, Tenhunen J, Kakubari Y (2008b) Annual and seasonal variations in photosynthetic capacity of Fagus crenata along an elevation gradient in the Naeba Mountains, Japan. Tree Physiology 28, 277–285.
Annual and seasonal variations in photosynthetic capacity of Fagus crenata along an elevation gradient in the Naeba Mountains, Japan.Crossref | GoogleScholarGoogle Scholar | 18055438PubMed |

Wong CYS, Gamon JA (2015) Three causes of variation in the photochemical reflectance index (PRI) in evergreen conifers. New Phytologist 206, 187–195.
Three causes of variation in the photochemical reflectance index (PRI) in evergreen conifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtF2qsro%3D&md5=f6baf5b0b3858f8f672e61f3ebb02ab3CAS |

Yamamoto H, Kamite L (1972) The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochimica et Biophysica Acta 267, 538–543.
The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XltV2qtr0%3D&md5=ebb55308c4aeed6537a8234be7ccae8bCAS | 5047136PubMed |