Zeaxanthin-independent energy quenching and alternative electron sinks cause a decoupling of the relationship between the photochemical reflectance index (PRI) and photosynthesis in an evergreen conifer during spring

Fréchette, Emmanuelle; Wong, Christopher Y. S.; Junker, Laura Verena; Chang, C. Y.; Ensminger, Ingo

doi:10.1093/jxb/erv427

Cited by 36 publications

(40 citation statements)

References 60 publications

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“…Field studies have confirmed that chlorophyll/ carotenoid ratios closely track the seasonal photosynthetic activity of Mediterranean climate evergreen leaves (21,23). This conclusion is further supported by recent spectral and kinetic evidence that demonstrates a close coincidence between seasonal photosynthetic activity, chlorophyll/carotenoid ratios, and spectral reflectance in evergreen conifers (24)(25)(26). Together, these studies suggest that satellite indices of changing pigment levels might provide reliable indicators of evergreen photosynthetic phenology.…”

Section: Significancesupporting

confidence: 65%

“…However, over annual time periods, the primary driver of the PRI at leaf and canopy scales is the changing leaf carotenoid pigment pool, typically expressed as the changing ratio of chlorophyll to carotenoid pigments (or its inverse), and not the xanthophyll cycle per se (21)(22)(23)(24)(25). This observation of changing pigment content is particularly relevant for northern evergreen conifers that undergo large seasonal swings in photosynthetic activity and carotenoid pigment levels associated with temperature extremes (24)(25)(26)(27)(28). These findings have led us to reconsider the function of carotenoid pigments in the context of detecting photosynthetic phenology in evergreen conifers.…”

Section: Significancementioning

confidence: 99%

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A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers

Gamon

Huemmrich

Wong

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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In evergreen conifers, where the foliage amount changes little with season, accurate detection of the underlying "photosynthetic phenology" from satellite remote sensing has been difficult, presenting challenges for global models of ecosystem carbon uptake. Here, we report a close correspondence between seasonally changing foliar pigment levels, expressed as chlorophyll/carotenoid ratios, and evergreen photosynthetic activity, leading to a "chlorophyll/carotenoid index" (CCI) that tracks evergreen photosynthesis at multiple spatial scales. When calculated from NASA's Moderate Resolution Imaging Spectroradiometer satellite sensor, the CCI closely follows the seasonal patterns of daily gross primary productivity of evergreen conifer stands measured by eddy covariance. This discovery provides a way of monitoring evergreen photosynthetic activity from optical remote sensing, and indicates an important regulatory role for carotenoid pigments in evergreen photosynthesis. Improved methods of monitoring photosynthesis from space can improve our understanding of the global carbon budget in a warming world of changing vegetation phenology.carotenoid pigments | evergreen conifers | gross primary productivity | chlorophyll/carotenoid index | CCI T he biosphere helps regulate atmospheric composition and climate, in part through the exchange of radiatively active gases, primarily carbon dioxide. About half of the "extra" carbon added to the atmosphere by human activity is rapidly absorbed by the biosphere, effectively slowing climate change relative to what would occur without this uptake (1, 2). The exact mechanism and spatiotemporal distribution of the terrestrial component of this carbon sink have been ongoing research topics for many years. In a warming world, the timing of photosynthetic activity is also changing, with unknown impacts on ecosystem productivity. These shifting patterns of seasonal photosynthetic activity, or "photosynthetic phenology," affect the biospheric-atmospheric gas exchange, further influencing atmospheric composition and climate (3-5). Faced with these uncertainties, quantifying the spatial and temporal patterns of biosphere/atmosphere carbon fluxes for different biomes and understanding their proximal controls remain central goals of global carbon cycle science.Northern forests make a large contribution to global photosynthetic carbon fixation and are an important component of the global carbon budget. However, northern evergreen conifers, including evergreen conifers of the vast boreal regions, present particular challenges to global carbon cycle monitoring (6). Their seasonal activity may be changing with an earlier growing season, with important implications for the biospheric carbon budget. A simple hypothesis has been that a longer growing season results in greater carbon uptake, particularly for northern ecosystems where photosynthetic activity has been temperature-limited (3, 7). By contrast, warmer growing seasons are also more likely to cause drought, restricting ecosystem carbon uptake...

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Section: Significancesupporting

confidence: 65%

Section: Significancementioning

confidence: 99%

A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers

Gamon

Huemmrich

Wong

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

264

243

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“…The balance between photochemical and carbon assimilation processes ensured by the action of the xanthophyll cycle maintains vegetation in a state optimal for photosynthesis [10]. Extensive studies have been conducted in recent years to explain impairment in the PRI-LUE relationship during spring caused by increased PSI activity upon recovering photosynthesis functions [55,56]. It is furthermore assumed that ATP consumption and cyclic electron flow around PSI help maintain the integrity of chloroplasts in cold environments [57].…”

Section: Use Of Pri For Determining Photosynthetic Parametersmentioning

confidence: 99%

Potential of Photochemical Reflectance Index for Indicating Photochemistry and Light Use Efficiency in Leaves of European Beech and Norway Spruce Trees

et al. 2018

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Hyperspectral reflectance is becoming more frequently used for measuring the functions and productivity of ecosystems. The purpose of this study was to re-evaluate the potential of the photochemical reflectance index (PRI) for evaluating physiological status of plants. This is needed because the reasons for variation in PRI and its relationships to physiological traits remain poorly understood. We examined the relationships between PRI and photosynthetic parameters in evergreen Norway spruce and deciduous European beech grown in controlled conditions during several consecutive periods of 10-12 days between which the irradiance and air temperature were changed stepwise. These regime changes induced significant changes in foliar biochemistry and physiology. The responses of PRI corresponded particularly to alterations in the actual quantum yield of photosystem II photochemistry (Φ PSII ). Acclimation responses of both species led to loss of PRI sensitivity to light use efficiency (LUE). The procedure of measuring PRI at multiple irradiance-temperature conditions has been designed also for testing accuracy of ∆PRI in estimating LUE. A correction mechanism of subtracting daily measured PRI from early morning PRI has been performed to account for differences in photosynthetic pigments between irradiance-temperature regimes. Introducing ∆PRI, which provided a better estimate of non-photochemical quenching (NPQ) compared to PRI, also improved the accuracy of LUE estimation. Furthermore, ∆PRI was able to detect the effect of drought, which is poorly observable from PRI.

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“…Additionally, photoprotective carotenoid pigments accumulate in leaves, especially the xanthophylls, zeaxanthin, and lutein that contribute to nonphotochemical quenching (NPQ) via thermal dissipation of excess light energy (Busch et al, 2007;Verhoeven et al, 2009;Demmig-Adams et al, 2012). Prolonged exposure to low temperature induces sustained nonphotochemical quenching (NPQ S ), where zeaxanthin constitutively dissipates excess light energy (Ensminger et al, 2004;Demmig-Adams et al, 2012;Fréchette et al, 2015).…”

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confidence: 99%

Elevated temperature and CO2 stimulate late season photosynthesis but impair cold hardening in pine

et al. 2016

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Rising global temperature and CO 2 levels may sustain late-season net photosynthesis of evergreen conifers but could also impair the development of cold hardiness. Our study investigated how elevated temperature, and the combination of elevated temperature with elevated CO 2 , affected photosynthetic rates, leaf carbohydrates, freezing tolerance, and proteins involved in photosynthesis and cold hardening in Eastern white pine (Pinus strobus). We designed an experiment where control seedlings were acclimated to long photoperiod (day/night 14/10 h), warm temperature (22°C/15°C), and either ambient (400 mL L 21 ) or elevated (800 mmol mol 21 ) CO 2 , and then shifted seedlings to growth conditions with short photoperiod (8/16 h) and low temperature/ambient CO 2 (LTAC), elevated temperature/ambient CO 2 (ETAC), or elevated temperature/elevated CO 2 (ETEC). Exposure to LTAC induced down-regulation of photosynthesis, development of sustained nonphotochemical quenching, accumulation of soluble carbohydrates, expression of a 16-kD dehydrin absent under long photoperiod, and increased freezing tolerance. In ETAC seedlings, photosynthesis was not down-regulated, while accumulation of soluble carbohydrates, dehydrin expression, and freezing tolerance were impaired. ETEC seedlings revealed increased photosynthesis and improved water use efficiency but impaired dehydrin expression and freezing tolerance similar to ETAC seedlings. Sixteen-kilodalton dehydrin expression strongly correlated with increases in freezing tolerance, suggesting its involvement in the development of cold hardiness in P. strobus. Our findings suggest that exposure to elevated temperature and CO 2 during autumn can delay down-regulation of photosynthesis and stimulate late-season net photosynthesis in P. strobus seedlings. However, this comes at the cost of impaired freezing tolerance. Elevated temperature and CO 2 also impaired freezing tolerance. However, unless the frequency and timing of extreme low-temperature events changes, this is unlikely to increase risk of freezing damage in P. strobus seedlings.

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Zeaxanthin-independent energy quenching and alternative electron sinks cause a decoupling of the relationship between the photochemical reflectance index (PRI) and photosynthesis in an evergreen conifer during spring

Abstract: HighlightDecoupling of the photochemical reflectance index and photosynthesis in evergreen conifers during spring is caused by energy-quenching mechanisms that remain undetected by leaf reflectance measurements and remote sensing.

Cited by 36 publications

References 60 publications

A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers

A remotely sensed pigment index reveals photosynthetic phenology in evergreen conifers

Potential of Photochemical Reflectance Index for Indicating Photochemistry and Light Use Efficiency in Leaves of European Beech and Norway Spruce Trees

Elevated temperature and CO2 stimulate late season photosynthesis but impair cold hardening in pine

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