Generality of relationships between leaf pigment contents and spectral vegetation indices in Mallorca (Spain)

Springer Science and Business Media LLC - Tập 17 - Trang 2097-2109 - 2017
Lea Hallik1,2, Taras Kazantsev3, Andres Kuusk1, Jeroni Galmés4, Magdalena Tomás4, Ülo Niinemets2,5
1Tartu Observatory, Tõravere, Estonia
2Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Tartu, Estonia
3Scientific Centre for Aerospace Research of the Earth, Institute of Geological Science, NASU, Kyiv, Ukraine
4Research Group on Plant Biology under Mediterranean Conditions, Departament de Biologia, Universitat de les Illes Balears, Palma de Mallorca, Spain
5Estonian Academy of Sciences, Tallinn, Estonia

Tóm tắt

Vegetation indices are calculated from reflectance data of discrete spectral bands. The reflectance signal in the visible spectral range is dominated by the optical properties of photosynthetic pigments in plant leaves. Numerous spectral indices have been proposed for the estimation of leaf pigment contents, but the efficacy of different indices for prediction of pigment content and composition for species-rich communities is unknown. Assessing the ability of different vegetation indices to predict leaf pigment content we identify the most suitable spectral indices from an experimental dataset consisting of field-grown high light exposed leaves of 33 angiosperm species collected in two sites in Mallorca (Spain) with contrasting leaf anatomy and pigment composition. Leaf-level reflectance spectra were recorded over the wavelength range of 400 – 900 nm and contents of chlorophyll a, chlorophyll b, total carotenoids, and anthocyanins were measured in 33 species from different plant functional types, covering a wide range of leaf structures and pigment content, five-fold to more than 10-fold for different traits. The best spectral region for estimation of leaf total chlorophyll content with least interference from carotenoids and anthocyanins was the beginning of near-infrared plateau well beyond 700 nm. Leaves of parallel-veined monocots and pinnate-veined dicots had different relationships between vegetation indices and pigments. We suggest that the nature and role of “far-red” chlorophylls which absorb light at longer wavelengths than 700 nm constitute a promising target for future remote sensing studies.

Tài liệu tham khảo

Barnes E, Clarke T, Richards S, Colaizzi PD, Haberland J, Kostrzewski M, Waller P, Choi C, Riley E, Thompson T (2000) Coincident Detection of Crop Water Stress, Nitrogen Status and Canopy Density Using Ground-Based Multispectral Data. In Proceedings of the Fifth International Conference on Precision Agriculture, p. [CD Rom] Bassi R, Caffarri S (2000) Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls. Photosynth Res 64:243–256. doi:10.1023/A:1006409506272 Blackburn GA (1998) Spectral indices for estimating photosynthetic pigment concentrations: a test using senescent tree leaves. Int J Remote Sens 19:657–675. doi:10.1080/014311698215919 Bornman JF, Vogelmann TC, Martin G (1991) Measurement of chlorophyll fluorescence within leaves using a fibre-optic microprobe. Plant Cell Environ 14:719–725. doi:10.1111/j.1365-3040.1991.tb01546.x Datt B (1998) Remote Sensing of Chlorophyll a, Chlorophyll b, Chlorophyll a+b, and Total Carotenoid Content in Eucalyptus Leaves. Remote Sens Environ 66:111–121. doi:10.1016/S0034-4257(98)00046-7 Datt B (1999) Visible/near infrared reflectance and chlorophyll content in Eucalyptus leaves. Int J Remote Sens 20(14):2741–2759 Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation: Tansley review. New Phytol 172:11–21. doi:10.1111/j.1469-8137.2006.01835.x Esteban R, Barrutia O, Artetxe U, Fernández-Marín B, Hernández A, García-Plazaola JI (2015a) Internal and external factors affecting photosynthetic pigment composition in plants: a meta-analytical approach. New Phytol 206:268–280. doi:10.1111/nph.13186 Esteban R, Moran JF, Becerril JF, García-Plazaola JI (2015b) Versatility of carotenoids: an integrated view on diversity, evolution, functional roles and environmental interactions. Environ Exp Bot 119:63–75. doi:10.1016/j.envexpbot.2015.04.009 Fan D-Y, Hope AB, Smith PJ, Jia H, Pace RJ, Anderson JM, Chow WS (2007) The stoichiometry of the two photosystems in higher plants revisited. Biochim Biophys Acta Bioenerg 1767:1064–1072. doi:10.1016/j.bbabio.2007.06.001 Féret J-B, François C, Gitelson A, Asner GP, Barry KM, Panigada C, Richardson AD, Jacquemoud S (2011) Optimizing spectral indices and chemometric analysis of leaf chemical properties using radiative transfer modeling. Remote Sens Environ 115:2742–2750. doi:10.1016/j.rse.2011.06.016 Fowler GJ, Visschers RW, Grief GG, van Grondelle R, Hunter CN (1992) Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands. Nature 355:848–850. doi:10.1038/355848a0 Caffarri S, Kouřil R, Kereïche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28:3052–3063. doi:10.1038/emboj.2009.232 Gibasiewicz K, Szrajner A, Ihalainen JA, Germano M, Dekker JP, van Grondelle R (2005) Characterization of low-energy chlorophylls in the PSI-LHCI supercomplex from Chlamydomonas reinhardtii. A site-selective fluorescence study. J Phys Chem B 109:21180–21186. doi:10.1021/jp0530909 Gitelson AA, Merzlyak MN (1994) Quantitative estimation of chlorophyll- a using reflectance spectra: Experiments with autumn chestnut and maple leaves. J Photochem Photobiol B Biol 22:247–252. doi:10.1016/1011-1344(93)06963-4 Gobets B, van Grondelle R (2001) Energy transfer and trapping in photosystem I. Biochim Biophys Acta 1507:80–99. doi:10.1016/S0005-2728(01)00203-1 Gulías J, Cifre J, Jonasson S, Medrano H, Flexas J (2009) Seasonal and inter-annual variations of gas exchange in thirteen woody species along a climatic gradient in the Mediterranean island of Mallorca. Flora - Morphol, Distrib, Funct Ecol Plants 204:169–181. doi:10.1016/j.flora.2008.01.011 Hallik L, Kull O, Niinemets Ü, Aan A (2009) Contrasting correlation networks between leaf structure, nitrogen and chlorophyll in herbaceous and woody canopies. Basic Appl Ecol 10:309–318. doi:10.1016/j.baae.2008.08.001 Hallik L, Niinemets Ü, Kull O (2012) Photosynthetic acclimation to light in woody and herbaceous species: a comparison of leaf structure, pigment content and chlorophyll fluorescence characteristics measured in the field. Plant Biol 14:88–99. doi:10.1111/j.1438-8677.2011.00472.x Hansen U, Fiedler B, Rank B (2002) Variation of pigment composition and antioxidative systems along the canopy light gradient in a mixed beech/oak forest: a comparative study on deciduous tree species differing in shade tolerance. Trees - Struct Funct 16:354–364. doi:10.1007/s00468-002-0163-9 Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151. doi:10.1016/S1360-1385(98)01200-X Havaux M, Tardy F, Lemoine Y (1998) Photosynthetic light-harvesting function of carotenoids in higher-plant leaves exposed to high light irradiances. Planta 205:242–250. doi:10.1007/s004250050317 Hogewoning SW, Wientjes E, Douwstra P, Trouwborst G, van Ieperen W, Croce R, Harbinson J (2012) Photosynthetic quantum yield dynamics: from photosystems to leaves. Plant Cell 24:1921–1935. doi:10.1105/tpc.112.097972 Huete A, Didan K, Miura T, Rodriguez EP, Gao X, Ferreira LG (2002) Overview of the radiometric and biophysical performance of the MODIS vegetation indices. Remote Sens Environ 83:195–213. doi:10.1016/S0034-4257(02)00096-2 Ihalainen JA, Rätsep M, Jensen PE, Scheller HV, Croce R, Bassi R, Korppi-Tommola JEI, Freiberg A (2003) Red spectral forms of chlorophylls in green plant PSI—a site-selective and high-pressure spectroscopy study. J Phys Chem B 107:9086–9093. doi:10.1021/jp034778t Imanishi J, Nakayama A, Suzuki Y, Imanishi A, Ueda N, Morimoto Y, Yoneda M (2010) Nondestructive determination of leaf chlorophyll content in two flowering cherries using reflectance and absorptance spectra. Landsc Ecol Eng 6:219–234. doi:10.1007/s11355-009-0101-8 Kira O, Linker R, Gitelson A (2015) Non-destructive estimation of foliar chlorophyll and carotenoid contents: focus on informative spectral bands. Int J Appl Earth Obs 38:251–260. doi:10.1016/j.jag.2015.01.003 Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857–865. doi:10.1046/j.1365-3040.2003.01017.x Krause GH, Koroleva OY, Dalling JW, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ 24:1345–1352. doi:10.1046/j.0016-8025.2001.00786.x Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. doi:10.1016/0076-6879(87)48036-1 Lliteras N, Romartinez R, Carbonell M, Llop C, Alonso C (2012) Estratègia Balear de Canvi climàtic 2013–2020. Una visió global del canvi climàtic. Direcció General de Medi Natural, Educació Ambiental i Canvi Climàtic. Balearic Islands Government Maccioni A, Agati G, Mazzinghi P (2001) New vegetation indices for remote measurement of chlorophylls based on leaf directional reflectance spectra. J Photochem Photobiol B 61:52–61. doi:10.1016/S1011-1344(01)00145-2 Marin A, Passarini F, van Stokkum IHM, van Grondelle R, Croce R (2011) Minor complexes at work: light-harvesting by carotenoids in the photosystem II antenna complexes CP24 and CP26. Biophys J 100:2829–2838. doi:10.1016/j.bpj.2011.04.029 Matsubara S, Krause GH, Aranda J, Virgo A, Beisel KG, Jahns P, Winter K (2009) Sun-shade patterns of leaf carotenoid composition in 86 species of neotropical forest plants. Funct Plant Biol 36:20–36. doi:10.1071/FP08214 Melkozernov AN (2001) Excitation energy transfer in photosystem I from oxygenic organisms. Photosynth Res 70:129–153. doi:10.1023/A:1017909325669 Morosinotto T, Breton J, Bassi R, Croce R (2003) The nature of a chlorophyll ligand in Lhca proteins determines the far red fluorescence emission typical of photosystem I. J Biol Chem 278:49223–49229. doi:10.1074/jbc.M309203200 Mutanga O, Skidmore AK (2004) Narrow band vegetation indices overcome the saturation problem in biomass estimation. Int J Remote Sens 25:3999–4014. doi:10.1080/01431160310001654923 Nicotra AB, Hofmann M, Siebke K, Ball MC (2003) Spatial patterning of pigmentation in evergreen leaves in response to freezing stress. Plant Cell Environ. 26: 1893–1904. doi:10.1046/j.1365-3040.2003.01106.x Niinemets Ü (2010a) A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance. Ecol Res 25:693–714. doi:10.1007/s11284-010-0712-4 Niinemets Ü (2010b) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manag 260:1623–1639. doi:10.1016/j.foreco.2010.07.054 Niinemets Ü, Bilger W, Kull O, Tenhunen JD (1998) Acclimation to high irradiance in temperate deciduous trees in the field: changes in xanthophyll cycle pool size and in photosynthetic capacity along a canopy light gradient. Plant Cell Environ 21:1205–1218. doi:10.1046/j.1365-3040.1998.00364.x Niinemets Ü, Kollist H, García-Plazaola JI, Hernández A, Becerril JM (2003) Do the capacity and kinetics for modification of xanthophyll cycle pool size depend on growth irradiance in temperate trees? Plant Cell Environ 26:1787–1801. doi:10.1046/j.1365-3040.2003.01096.x Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G (2002) The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiol 129:235–243. doi:10.1104/pp.010943 Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82. doi:10.1016/j.molp.2014.12.007 Oja V, Eichelmann H, Peterson RB, Rasulov B, Laisk A (2003) Deciphering the 820 nm signal: redox state of donor side and quantum yield of photosystem I in leaves. Photosynth Res 78:1–15. doi:10.1023/A:1026070612022 Oja V, Bichele I, Hüve K, Rasulov B, Laisk A (2004) Reductive titration of photosystem I and differential extinction coefficient of P700+ at 810–950 nm in leaves. Biochim Biophys Acta Bioenerg 1658:225–234. doi:10.1016/j.bbabio.2004.06.006 Opriş O, Copaciu F, Soran M-L, Ristoiu D, Niinemets Ü, Copolovici L (2013) Influence of nine antibiotics on key secondary metabolites and physiological characteristics in Triticum aestivum: leaf volatiles as a promising new tool to assess toxicity. Ecotoxicol Environ Saf 87:70–79. doi:10.1016/j.ecoenv.2012.09.019 Peñuelas J, Baret F, Filella I (1995) Semi-empirical indices to assess carotenoids/chlorophyll a ratio from leaf spectral reflectance. Photosynthetica 31:221–230 http://prodinra.inra.fr/record/117560 Pettai H, Oja V, Freiberg A, Laisk A (2005a) Photosynthetic activity of far-red light in green plants. Biochim Biophys Acta (BBA) - Bioenergetics 1708:311–321. doi:10.1016/j.bbabio.2005.05.005 Pettai H, Oja V, Freiberg A, Laisk A (2005b) The long-wavelength limit of plant photosynthesis. FEBS Lett 579:4017–4019. doi:10.1016/j.febslet.2005.04.088 Pettorelli N, Wegmann M, Skidmore A, Mücher S, Dawson TP, Fernandez M, Lucas R, Schaepman ME, Wang T, O'Connor B, Jongman RHG, Kempeneers P, Sonnenschein R, Leidner AK, Böhm M, He KS, Nagendra H, Dubois G, Fatoyinbo T, Hansen MC, Paganini M, de Klerk HM, Asner GP, Kerr JT, Estes AB, Schmeller DS, Heiden U, Rocchini D, Pereira HM, Turak E, Fernandez N, Lausch A, Cho MA, Alcaraz-Segura D, McGeoch MA, Turner W, Mueller A, St-Louis V, Penner J, Vihervaara P, Belward A, Reyers B, Geller GN (2016) Framing the concept of satellite remote sensing essential biodiversity variables: challenges and future directions. Remote Sens Ecol Conserv 2:122–131. doi:10.1002/rse2.15 Polívka T, Sundström V (2004) Ultrafast dynamics of carotenoid excited states from solution to natural and artificial systems. Chem Rev 104:2021–2071. doi:10.1021/cr020674n Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156. doi:10.1023/A:1020470224740 Poulson ME, Vogelmann TC (1990) Epidermal focussing and effects upon photosynthetic light-harvesting in leaves of Oxalis. Plant Cell Environ 13:803–811. doi:10.1111/j.1365-3040.1990.tb01096.x Rivadossi A, Zucchelli G, Garlaschi FM, Jennings RC (1999) The importance of PS I chlorophyll red forms in light-harvesting by leaves. Photosynth Res 60:209–215. doi:10.1023/A:1006236829711 Savitzky A, Golay MJE (1964) Smoothing and differentiation of data by simplified least squares procedures. Anal Chem 36:1627–1639. doi:10.1021/ac60214a047 Siebke K, Ball MC (2009) Non-destructive measurement of chlorophyll b: a ratios and identification of photosynthetic pathways in grasses by reflectance spectroscopy. Funct Plant Biol 36:857–866. doi:10.1071/FP09201 Sims DA, Gamon JA (2002) Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. Remote Sens Environ 81:337–354. doi:10.1016/S0034-4257(02)00010-X Skidmore AK, Pettorelli N, Coops NC, Geller GN, Hansen M, Lucas R, Mücher CA, O'Connor B, Paganini M, Pereira HM, Schaepman ME, Turner W, Wang T, Wegmann M (2015) Environmental science: agree on biodiversity metrics to track from space. Nature 523:403–405 Smith WK, Vogelmann TC, DeLucia EH, Bell DT, Shepherd KA (1997) Leaf form and photosynthesis: do leaf structure and orientation interact to regulate internal light and carbon dioxide? Bioscience 47:785–793. doi:10.2307/1313100 Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant Cell Environ 18:1111–1128. doi:10.1111/j.1365-3040.1995.tb00623.x Terashima I, Saeki T (1985) A new model for leaf photosynthesis incorporating the gradients of light environment and of photosynthetic properties of chloroplasts within a leaf. Ann Bot 56:489–499 http://www.jstor.org/stable/42764247 Thapper A, Mamedov F, Mokvist F, Hammarström L, Styring S (2009) Defining the far-red limit of photosystem II in spinach. Plant Cell 21:2391–2401. doi:10.1105/tpc.108.064154 Thenkabail PS, Mariotto I, Gumma MK, Middleton EM, Landis DR, Huemmrich KF (2013) Selection of Hyperspectral Narrowbands (HNBs) and Composition of Hyperspectral Twoband Vegetation Indices (HVIs) for Biophysical Characterization and Discrimination of Crop Types Using Field Reflectance and Hyperion/EO-1 Data. IEEE J Sel Top Appl Earth Obs Remote Sens 6:427–439. doi:10.1109/JSTARS.2013.2252601 Tosens T, Niinemets Ü, Vislap V, Eichelmann H, Castro-Díez P (2012) Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: how structure constrains function. Plant Cell Environ 35:839–856. doi:10.1111/j.1365-3040.2011.02457.x Ustin SL, Gitelson AA, Jacquemoud S, Schaepman M, Asner GP, Gamon JA, Zarco-Tejada P (2009) Retrieval of foliar information about plant pigment systems from high resolution spectroscopy. Remote Sens Environ 113:S67–S77. doi:10.1016/j.rse.2008.10.019 Vihervaara P, Auvinen AP, Mononen L, Törmä M, Ahlroth P, Anttila S, Böttcher K, Forsius M, Heino J, Heliölä J, Koskelainen M, Kuussaari M (2017) How essential biodiversity variables and remote sensing can help national biodiversity monitoring. Glob Ecol Conserv 10:43–59 Vogelmann TC, Martin G (1993) The functional-significance of palisade tissue—penetration of directional versus diffuse light. Plant Cell Environ 16:65–72. doi:10.1111/j.1365-3040.1993.tb00845.x Vogelmann TC, Nishio JN, Smith WK (1996) Leaves and light capture: light propagation and gradients of carbon fixation within leaves. Trends Plant Sci 1:65–71. doi:10.1016/S1360-1385(96)80031-8 Wientjes E, Croce R (2011) The light-harvesting complexes of higher-plant photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem J 433:477–485. doi:10.1042/BJ20101538 Wientjes E, Roest G, Croce R (2012) From red to blue to far-red in Lhca4: how does the protein modulate the spectral properties of the pigments? Biochim Biophys Acta Bioenerg 1817:711–717. doi:10.1016/j.bbabio.2012.02.030 Zucchelli G, Jennings RC, Garlaschi FM (1990) The presence of long-wavelength chlorophyll a spectral forms in the light-harvesting chlorophyll a/b protein complex II. J Photochem Photobiol B Biol 6:381–394. doi:10.1016/1011-1344(90)85112-A