title: The photochemical reflectance index provides an optical indicator of spring photosynthetic activation in evergreen conifers.
abstract: In evergreens, the seasonal down-regulation and reactivation of photosynthesis is largely invisible and difficult to assess with remote sensing. This invisible phenology may be changing as a result of climate change. To better understand the mechanism and timing of these hidden physiological transitions, we explored several assays and optical indicators of spring photosynthetic activation in conifers exposed to a boreal climate. The photochemical reflectance index (PRI), chlorophyll fluorescence, and leaf pigments for evergreen conifer seedlings were monitored over 1 yr of a boreal climate with the addition of gas exchange during the spring. PRI, electron transport rate, pigment levels, light-use efficiency and photosynthesis all exhibited striking seasonal changes, with varying kinetics and strengths of correlation, which were used to evaluate the mechanisms and timing of spring activation. PRI and pigment pools were closely timed with photosynthetic reactivation measured by gas exchange. The PRI provided a clear optical indicator of spring photosynthetic activation that was detectable at leaf and stand scales in conifers. We propose that PRI might provide a useful metric of effective growing season length amenable to remote sensing and could improve remote-sensing-driven models of carbon uptake in evergreen ecosystems.
authors: Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, T6G 2E3, Canada.
authors: Christopher Y S
authors: CYS
authors: Wong
authors: Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, T6G 2E3, Canada.|Department Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada.
authors: John A
authors: JA
authors: Gamon
mesh_terms: D000064:Acclimatization; D002980:Climate; D015536:Down-Regulation; D004579:Electron Transport; D008027:Light; D010777:Photochemistry; D010788:Photosynthesis / Q000502:physiology* / Q000528:radiation effects; D028223:Pinus / Q000502:physiology* / Q000528:radiation effects; D018515:Plant Leaves / Q000502:physiology / Q000528:radiation effects; D018526:Plant Transpiration / Q000502:physiology / Q000528:radiation effects; D012621:Seasons; D036226:Seedlings / Q000502:physiology / Q000528:radiation effects; D013312:Stress, Physiological
keywords: acclimation; chlorophyll fluorescence; cold stress; evergreen conifers; photochemical reflectance index (PRI); photosynthesis; pigments; spring activation
references: Adams WW, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V. 2002. Photosynthesis and photoprotection in overwintering plants. Plant Biology 4: 545-557.
references: Adams WW, Demmig-Adams B, Verhoeven AS, Barker DH. 1995. Photoinhibion during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation. Australian Journal of Plant Physiology 22: 261-276.
references: Adams WW, Zarter CR, Ebbert V, Demmig-Adams B. 2004. Photoprotective strategies of overwintering evergreens. BioScience 54: 41-49.
references: Apps MJ, Kurz WA, Luxmoore RJ, Nilsson LO, Sedjo RA, Schmidt R, Simpson LG, Vinson TS. 1993. Boreal forests and tundra. Water Air and Soil Pollution 70: 39-53.
references: Baker NR. 2008. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59: 89-113.
references: Baroli I, Niyogi KK. 2000. Molecular genetics of xanthophyll-dependent photoprotection in green algae and plants. Philosophical Transactions of the Royal Society of London Series B - Biological Sciences 355: 1385-1393.
references: 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.
references: Bigras FJ, Ryyppo A, Lindstrom A, Stattin E. 2001. Cold acclimaion and deacclimation of shoots and roots of conifer seedlings. In: Bigras FJ, Colombo SJ, eds. Conifer cold hardiness. Dordrecht, the Netherlands: Kluwer Academic, 57-88.
references: Björkman O, Demmig-Adams B. 1994. Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In: Schulze E-D, Caldwell M, eds. Ecophysiology of photosynthesis. Berlin, Heidelberg, Germany: Springer, 17-47.
references: Butler WL. 1978. Energy distribution in photochemical apparatus of photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 29: 345-378.
references: Canadell JG, Le Quéré C, Raupach MR, Field CB, Buitenhuis ET, Ciais P, Conway TJ, Gillett NP, Houghton RA, Marland G. 2007. Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proceedings of the National Academy of Sciences, USA 104: 18866-18870.
references: Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A et al. 2005. Europe-wide reduction in primary productivity caused by the heat and drought in 2003. Nature 437: 529-533.
references: Ciais P, Tans PP, Trolier M, White JWC, Francey RJ. 1995. A large northern-hemisphere terrestrial CO2 sink indicated by the 13C/12C ratio of atmospheric CO2. Science 269: 1098-1102.
references: Demmig-Adams B, Adams WW. 1992. Photoprotection and other responses of plants to high light stress. Annual Review of Plant Physiology and Plant Molecular Biology 43: 599-626.
references: Demmig-Adams B, Adams WW. 1996. The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science 1: 21-26.
references: Demmig-Adams B, Cohu CM, Muller O, Adams WW. 2012. Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynthesis Research 113: 75-88.
references: 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.
references: Esteban R, Jiménez MS, Morales D, Jiménez ET, Hormaetxe K, Becerril JM, Osmond B, García-Plazaola JI. 2008. Short- and long-term modulation of the lutein epoxide and violaxanthin cycles in two species of the Lauraceae: sweet bay laurel (Laurus nobilis L.) and avocado (Persea americana Mill.). Plant Biology 10: 288-297.
references: 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.
references: Frankenberg C, Fisher JB, Worden J, Badgley G, Saatchi SS, Lee JE, Toon GC, Butz A, Jung M, Kuze A et al. 2011. New global observations of the terrestrial carbon cycle from GOSAT: patterns of plant fluorescence with gross primary productivity. Geophysical Research Letters 38: L17706.
references: Gamon JA, Berry JA. 2012. Facultative and constitutive pigment effects on the Photochemical Reflectance Index (PRI) in sun and shade conifer needles. Israel Journal of Plant Sciences 60: 85-95.
references: 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.
references: Gamon JA, Qiu H. 1999. Ecological applications of remote sensing at multiple scales. In: Pugnaire FI, Valladares F, eds. Handbook of functional plant ecology. New York, NY, USA: Marcel Dekker, 805-846.
references: 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.
references: Gamon JA, Surfus JS. 1999. Assessing leaf pigment content and activity with a reflectometer. New Phytologist 143: 105-117.
references: Garbulsky MF, Peñuelas J, Gamon JA, 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.
references: García-Plazaola JI, Faria T, Abadía J, Abadía A, Chaves MM, Pereira JS. 1997. Seasonal changes in xanthophyll composition and photosynthesis of cork oak (Quercus suber L.) leaves under Mediterranean climate. Journal of Experimental Botany 48: 1667-1674.
references: Garrity SR, Eitel JUH, Vierling LA. 2011. Disentangling the relationships between plant pigments and the photochemical reflectance index reveals a new approach for remote estimation of carotenoid content. Remote Sensing of Environment 115: 628-635.
references: Gilmore AM, Ball MC. 2000. Protection and storage of chlorophyll in overwintering evergreens. Proceedings of the National Academy of Sciences, USA 97: 11098-11101.
references: Goodale CL, Apps MJ, Birdsey RA, Field CB, Heath LS, Houghton RA, Jenkins JC, Kohlmaier GH, Kurz W, Liu SR et al. 2002. Forest carbon sinks in the Northern Hemisphere. Ecological Applications 12: 891-899.
references: Goulden ML, Munger JW, Fan SM, Daube BC, Wofsy SC. 1996. Exchange of carbon dioxide by a deciduous forest: response to interannual climate variability. Science 271: 1576-1578.
references: Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P. 2009. Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chemical Physics Letters 483: 262-267.
references: Horton P, Ruban AV, Walters RG. 1996. Regulation of light harvesting in green plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 655-684.
references: Hüner NPA, Öquist G, Sarhan F. 1998. Energy balance and acclimation to light and cold. Trends in Plant Science 3: 224-230.
references: IPCC. 2007. Solomon S, Qin M, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL, eds. Climate change 2007: the physical science basis. Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge, UK: Cambridge University Press.
references: Jahns P, Holzwarth AR. 2012. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochimica Et Biophysica Acta - Bioenergetics 1817: 182-193.
references: Kurz WA, Apps MJ. 1999. A 70-year retrospective analysis of carbon fluxes in the Canadian forest sector. Ecological Applications 9: 526-547.
references: Kurz WA, Stinson G, Rampley GJ, Dymond CC, Neilson ET. 2008. Risk of natural disturbances makes future contribution of Canada's forests to the global carbon cycle highly uncerain. Proceedings of the National Academy of Sciences, USA 105: 1551-1555.
references: Le Quéré C, Raupach MR, Canadell JG, Marland G, Bopp L, Ciais P, Conway TJ, Doney SC, Feely RA, Foster P et al. 2009. Trends in the sources and sinks of carbon dioxide. Nature Geoscience 2: 831-836.
references: Levitt J. 1980. Responses of plants to environmental stresses. New York, NY, USA: Academic Press.
references: Maxwell K, Johnson GN. 2000. Chlorophyll fluorescence: a practical guide. Journal of Experimental Botany 51: 659-668.
references: Meroni M, Rossini M, Guanter L, Alonso L, Rascher U, Colombo R, Moreno J. 2009. Remote sensing of solar-induced chlorophyll fluorescence: review of methods and applications. Remote Sensing of Environment 113: 2037-2051.
references: Middleton EM, Cheng YB, Hilker T, Black TA, Krishnan P, Coops NC, Huemmrich KF. 2009. Linking foliage spectral responses to canopy-level ecosystem photosynthetic light-use efficiency at a Douglas-fir forest in Canada. Canadian Journal of Remote Sensing 35: 166-188.
references: Monson RK, Sparks JP, Rosenstiel TN, Scott-Denton LE, Huxman TE, Harley PC, Turnipseed AA, Burns SP, Backlund B, Hu J. 2005. Climatic influences on net ecosystem CO2 exchange during the transition from wintertime carbon source to springtime carbon sink in a high-elevation, subalpine forest. Oecologia 146: 130-147.
references: Myneni RB, Keeling CD, Tucker CJ, Asrar G, Nemani RR. 1997. Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386: 698-702.
references: 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.
references: 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.
references: Oh S, Adams WW, Demmig-Adams B, Koh SC. 2013. Seasonal photoprotective responses in needles of Korean Fir (Abies koreana) over an altitudinal gradient on Mount Halla, Jeju Island, Korea. Arctic Antarctic and Alpine Research 45: 238-248.
references: Öquist G, Hüner NPA. 2003. Photosynthesis of overwintering evergreen plants. Annual Review of Plant Biology 54: 329-355.
references: Ottander C, Campbell D, Öquist G. 1995. Seasonal changes in photosystem II organization and pigment composition in Pinus sylvestris. Planta 197: 176-183.
references: Pan YD, Birdsey RA, Fang JY, Houghton R, Kauppi PE, Kurz WA, Phillips OL, Shvidenko A, Lewis SL, Canadell JG et al. 2011. A large and persistent carbon sink in the World's forests. Science 333: 988-993.
references: Peñuelas J, Filella I, Gamon JA. 1995. Assessment of photosynthetic radiation-use efficiency with spectral reflectance. New Phytologist 131: 291-296.
references: Porcar-Castell A. 2011. A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris. Physiologia Plantarum 143: 139-153.
references: Porcar-Castell A, Garcia-Plazaola JI, Nichol CJ, Kolari P, Olascoaga B, Kuusinen N, Fernandez-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.
references: 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.
references: Powles SB. 1984. Photoinhibition of photosynthesis induced by visible light. Annual Review of Plant Physiology and Plant Molecular Biology 35: 15-44.
references: Rahman AF, Cordova VD, Gamon JA, Schmid HP, Sims DA. 2004. Potential of MODIS ocean bands for estimating CO2 flux from terrestrial vegetation: a novel approach. Geophysical Research Letters 31: 4.
references: Randerson JT, Field CB, Fung IY, Tans PP. 1999. Increases in early season ecosystem uptake explain recent changes in the seasonal cycle of atmospheric CO2 at high northern latitudes. Geophysical Research Letters 26: 2765-2768.
references: Richardson AD, Black TA, Ciais P, Delbart N, Friedl MA, Gobron N, Hollinger DY, Kutsch WL, Longdoz B, Luyssaert S et al. 2010. Influence of spring and autumn phenological transitions on forest ecosystem productivity. Philosophical Transactions of the Royal Society B - Biological Sciences 365: 3227-3246.
references: Richardson AD, Hollinger DY, Dail DB, Lee JT, Munger JW, O'Keefe J. 2009. Influence of spring phenology on seasonal and annual carbon balance in two contrasting New England forests. Tree Physiology 29: 321-331.
references: Ruban AV, Johnson MP, Duffy CDP. 2012. The photoprotective molecular switch in the photosystem II antenna. Biochimica Et Biophysica Acta-Bioenergetics 1817: 167-181.
references: Slayback DA, Pinzon JE, Los SO, Tucker CJ. 2003. Northern hemisphere photosynthetic trends 1982-99. Global Change Biology 9: 1-15.
references: Stylinski CD, Gamon JA, Oechel WC. 2002. Seasonal patterns of reflectance indices, carotenoid pigments and photosynthesis of evergreen chaparral species. Oecologia 131: 366-374.
references: Telfer A. 2005. Too much light? How β-carotene protects the photosystem II reaction centre. Photochemical & Photobiological Sciences 4: 950-956.
references: Thayer SS, Björkman O. 1990. Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23: 331-343.
references: Thurner M, Beer C, Santoro M, Carvalhais N, Wutzler T, Schepaschenko D, Shvidenko A, Kompter E, Ahrens B, Levick SR et al. 2014. Carbon stock and density of northern boreal and temperate forests. Global Ecology and Biogeography 23: 297-310.
references: Verhoeven A. 2014. Sustained energy dissipation in winter evergreens. New Phytologist 201: 57-65.
references: 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.
references: Verhoeven AS, Adams WW, Demmig-Adams B. 1999. The xanthophyll cycle and acclimation of Pinus ponderosa and Malva neglecta to winter stress. Oecologia 118: 277-287.
references: Vogg G, Heim R, Hansen J, Schäfer C, Beck E. 1998. Frost hardening and photosynthetic performance of Scots pine (Pinus sylvestris L.) needles. I. Seasonal changes in the photosynthetic apparatus and its function. Planta 204: 193-200.
references: Wong CYS, Gamon JA. 2015. Three causes of variation in the photochemical reflectance index (PRI) in evergreen conifers. New Phytologist 206: 187-195.
references: Xu L, Myneni RB, Chapin FS, Callaghan TV, Pinzon JE, Tucker CJ, Zhu Z, Bi J, Ciais P, Tømmervik H et al. 2013. Temperature and vegetation seasonality diminishment over northern lands. Nature Climate Change 3: 581-586.