Photosynthetic Acclimation to Light Gradients

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[Plant Signaling & Behavior 3:12, 1116-1118; December 2008]; 2008 Landes Bioscience

of magnitudes which often leads to disturbed and reduced photosynthetic efficiency. Such variations in illumination occur on differentime scales. Fluctuating light evoked by passing clouds or leaf move

ments triggers short-term responses such as energy quenching (NPQor state transitions.1-3 These processes act at the posttranslational leveand are reversible within seconds to minutes.4,5 Slow changes in thelight environment, in contrast, need to be counterbalanced by moresustainable processes, so called long-term responses, which restruc-ture the photosynthetic complexes within the thylakoid membranein number and size. This involves changes in gene expression andre-modulations of metabolism.6,7 So far, two distinct long-term lighacclimation processes have been described (i) the long-term responseto changes in light quantity whereupon an adjustment of PSIILHCII antenna size occurs and (ii) the long-term response (LTR)to light quality gradients which acts under low light conditions

and counteracts imbalances in excitation between the photosystemsmainly by re-adjustment of PSI/PSII ratio (Fig. 1A).8-11 Imbalancein photosynthetic electron transport due to changing light quality aresensed within the chloroplast via changes in the redox state of mobileelectron carriers (i.e. PQ.) of the transport chain and this, in turn,activates an intraplastidial gene regulation network in order to adjustthe stoichiometry of photosynthetic complexes. This mechanismassures an unhindered electron flow and prevents the photosyntheticapparatus from photo-oxidative damages. This regulation networkextends also to photosynthetic and metabolic genes encoded in thenucleus and therefore constitutes an important retrograde (plastid-to-nucleus) flow of information.12-14 The LTR is an evolutionaryconserved feature that can be found in photosynthetic organisms

ranging from cyanobacteria over unicellular algae up to plants.15-19To investigate this mechanism at molecular and physiological leve

we mimicked light quality gradients using a light system causingpreferential excitation of either PSI or PSII.8 In a recent study wedemonstrated that the LTR to light quality is an indispensable mech-anism for plants to survive under imbalanced excitation. As a finameasure for effectiveness of acclimation we determined seed production and found that plants lacking the LTR (e.g., in the stn7-mutantproduce 50% less seeds than WT under long-term alternating lightqualities.20 According to the Hardy-Weinberg rule of populationgenetics less fit individuals may become extinct in an exponentia

Dense plant populations or canopies exhibit a strong enrich-ment in far-red wavelengths which leads to unequal excitationof the two photosystems. In the long-term plants acclimate to

changes in light quality by adjusting photosystem stoichiom-etry and antenna structure, a mechanism called here long-termresponse (LTR). Using an artificial light system it is possible tomimic such naturally occurring gradients in light quality undercontrolled laboratory conditions. By this means we recentlydemonstrated that the LTR is crucial for plant fitness and survivalof Arabidopsis. We could also demonstrate that the chlorophyllfluorescence parameter Fs/Fm is a genuine non-invasive functionalindicator for acclimatory changes during the LTR. Here we givesupportive data that the Fs/Fm can be also used to monitor theLTR in field experiments in which Arabidopsis plants were growneither under canopies or wavelength-neutral shade. Furthermoreour data support the notion that acclimation responses to lightquality and light quantity are separate mechanisms. Thus, thelong-term response to light quality represents an important anddistinct acclimation strategy for improving plant survival underchanging light quality conditions.

Photosynthetic Acclimation to Light Quality is Essential forPlant Survival

The sessile lifestyle of plants requires sophisticated acclimationprogrammes to cope with the steadily changing environment and tooptimize growth and reproduction. Light as one essential environ-mental factor can vary in its composition and intensity in the order

*Correspondence to: Thomas Pfannschmidt; Friedrich Schiller University Jena;

Department of Plant Physiology; Dornburger Str. 159; Jena, Thuringia 07743

Germany; Tel.: +493641949236; Email: [email protected]

Submitted: 09/10/08; Accepted: 09/17/08

Previously published online as a Plant Signaling & BehaviorE-publication:

http://www.landesbioscience.com/journals/psb/article/7038

Addendum to: Wagner R, Dietzel L, Brutigam K, Fischer W, Pfannschmidt T. The

long-term response to fluctuating light quality is an important and distinct light accli-

mation mechanism that supports survival of Arabidopsis thaliana under low light

conditions. Planta 2008; 228:57387; PMID: 18542996; DOI: 10.1007/s00425-

008-0760-y.

Article Addendum

Photosynthetic acclimation to light gradients in plant stands comes outof shade

Lars Dietzel and Thomas Pfannschmidt*

Institute for General Botany and Plant Physiology; Friedrich-Schiller University Jena; Jena, Thuringia Germany

Abbreviations: LTR, long-term response to light quality; PS, photosystem; LHC, light harvesting complex; PQ, plastoquinone; TRX, thioredoxin; NPQ, non-photochemical quenching; PAR, photosynthetically active radiation

Key words: photosynthetic acclimation, redox control, long-term responses, light quality, Arabidopsis, plant fitness


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Long-term response to light quality

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Fs/Fm value is a robust photosynthetic parameter to indicate lighquality acclimation. How this non-invasively measured parametecan be linked to molecular markers and signalling cascades is a challenging field for future research (Fig. 1B).

Material and Methods

Arabidopsis thaliana Col-0 plants for the field experiment were grown on soil for 5 weeks at an illumination of 80 mophotons*m-2*s-1 and 9 h-light 15 h-dark-cycle. The plants were thentransferred to the Botanical Garden of the Friedrich-Schiller-University

Jena under a beech canopy and under neutral shade at a place nearby. Lightqualities were recorded at the sites with spectroradiometer (GER1500Geophysical and Environmental Research Corp., Millbrook (NY)USA). PAR was determined using the Hansatech QuantithermQRT1 light-meter (Norfolk, UK). Chlorophyll-fluorescence wa

manner. This means that the homozygous mutant allele would benearly extinct within 10 generations (1.6% allele frequency). Hence,it can be concluded that even small changes in the ability of plantsto acclimate to different light situations may have huge effects on thesurvival of the species.

Using Chlorophyll Fluorescence to Monitor LTR

We developed and refined physiological markers for this photo-synthetic acclimation. The ratio of chlorophyll (Chl) a over Chl b isa well known structural indicator for changes in PS-stoichiometryand/or LHC-antenna size.7,10 As a second marker we establisheda functional indicator, the chlorophyll fluorescence parameter Fs/Fm. The steady state fluorescence yield (Fs) of PSI-light acclimatedplants (PSI-plants) was found to be constantly higher than that ofplants acclimated to PSII-light when determined under standardconditions. This rise in fluorescence can be best explained by thereadjustment of PS stoichiometry leading to a higher PSII/PSI ratioin PSI-plants than in PSII-plants resulting in a less efficient transferof electrons into photosynthetic products under the measuringlight of the fluorometer.21 But are changes in Fs/Fm and Chl a/b

independent from short-term responses such as state transitionsand feedback-de-excitation mechanisms (NPQ)? To address thisquestion, we shifted PSI-plants to PSII-light and recorded Fs/Fmat different time points after the shift. The kinetics demonstratedthat the major changes in Fs/Fm occurred 1224 h after the lightshift indicating that state transitions had no or only little effect onthis parameter.20 Furthermore, we tested the ability to perform theLTR in an NPQ-deficient mutant and found a WT-like responseindicating that the fast energy quenching via PsbS has no effect onthe performance of the LTR.20 We further tested whether the Fs/Fmparameter is affected by different light quantities. We determinedFs/Fm from plants acclimated to WL conditions ranging from1560 mol photons*s-1*m-2 PAR and found no changes whereas

plants shifted from PSI-light (24 mol photons*s-1*m-2 PAR) toPSII-light (12 mol photons*s-1*m-2 PAR) and vice versa exhibitedsignificant differences of 4050% in the Fs/Fm. Taken together, thisclearly demonstrates that light quality and light quantity acclima-tion are functionally distinct although they occur within the sametime range.20

Occurrence of LTR in the Field

Here we give supportive data that the LTR is not only restrictedto controlled lab conditions. In a field experiment we transferred

Arabidopsis to different natural low light habitats. One set of seed-lings was acclimated to shade under a canopy of beeches, the controlgroup was left in light quality-neutral shade of identical flux densityin photosynthetically active radiation (20 mol photons*m-2*s-1).The Fs/Fm value of plants acclimated 10 d to shade under a canopy

was about 50% higher than that of plants grown in neutral shade.This corresponds to the results we obtained in laboratory experimentsand strongly supports the notion that photosynthetic acclimation todifferent light qualities is a crucial mechanism for plant fitness infield conditions. Since the light intensity in the field experiments wasset equally in neutral shade and canopy shade this indicates that theLTR is not overridden by other environmental factors such as illumi-nation changes in the day night cycle and differences in temperatureor humidity during the day. This provides further evidence that the

Figure 1. Light gradients in a plant canopy. (A) Varying light intensities aredepicted as grey triangle, light quality gradients are given as red triangleUnder saturating light the photosynthetic electron transport chain (includingPQH2 and TRX) is highly reduced and feedback-de-excitation mechanismsrestore the redox-poise in the photosynthetic light reaction. Enrichment of farred wavelengths can be observed under light limiting conditions in plant canopies which preferentially excite PSI leading to a redox imbalance betweenthe photosystems and oxidation of the PQ-pool. By this means a signal isgenerated which leads to an adjustment of photosystem stoichiometry, thyla

koid structure and metabolism as a consequence of the LTR For further detailssee text. (B) Fs/Fm parameter as a marker of LTR under laboratory and fieldconditions. Plants acclimated to either PSI-light or shade of a canopy (canwere shifted for 23 days to PSII-light or a neutral (neut) shade and viceversa. The plants show a comparable acclimation pattern with similar highFs/Fm values under PSI-light and canopy shade, respectively, whereas plantacclimated to PSII-light or neutral shade exhibit drastically lower values. PARunder all light conditions was set to ~20 mol photons*m-2*s-1.


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measured with a PAM-2000 device (Walz, Effeltrich, Germany).22 After 7 days of acclimation half of the population was shiftedbetween the sites for further 3 days. The experiment took placeMay 21st to 31st 2008. Weather data from Jena during the experimentcan be found at www.bgc-jena.mpg.de/wetter/mpi_roof_2008a.zip

Acknowledgements

This work was supported by grants from the DeutscheForschungsgemeinschaft to TP, FOR804 and by the NWP programmeof Thuringia. We gratefully acknowledge Prof. Dr. Frank Hellwigand Thomas Bopp for help in performing field experiments in theBotanical Garden of Friedrich-Schiller-University Jena.

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Photosynthetic Acclimation to Light Gradients