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First published online April 1, 2009; 10.1104/pp.109.137828 Plant Physiology 150:977-986 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Quantitative Genetic Analysis of Thermal Dissipation in Arabidopsis1,[W],[OA]Department of Plant and Microbial Biology, University of California, Berkeley, California 94720–3102
Feedback deexcitation is a photosynthetic regulatory mechanism that can protect plants from high light stress by harmlessly dissipating excess absorbed light energy as heat. To understand the genetic basis for intraspecies differences in thermal dissipation capacity, we investigated natural variation in Arabidopsis (Arabidopsis thaliana). We determined the variation in the amount of thermal dissipation by measuring nonphotochemical quenching (NPQ) of chlorophyll fluorescence in Arabidopsis accessions of diverse origins. Ll-1 and Sf-2 were selected as high NPQ Arabidopsis accessions, and Columbia-0 (Col-0) and Wassilewskija-2 were selected as relatively low NPQ accessions. In spite of significant differences in NPQ, previously identified NPQ factors were indistinguishable between the high and the low NPQ accessions. Intermediate levels of NPQ in Ll-1 x Col-0 F1 and Sf-2 x Col-0 F1 compared to NPQ levels in their parental lines and continuous distribution of NPQ in F2 indicated that the variation in NPQ is under the control of multiple nuclear factors. To identify genetic factors responsible for the NPQ variation, we developed a polymorphic molecular marker set for Sf-2 x Col-0 at approximately 10-centimorgan intervals. From quantitative trait locus (QTL) mapping with undistorted genotype data and NPQ measurements in an F2 mapping population, we identified two high NPQ QTLs, HQE1 (high qE 1, for high energy-dependent quenching 1) and HQE2, on chromosomes 1 and 2, and the phenotype of HQE2 was validated by analysis of near isogenic lines. Neither QTL maps to a gene that had been identified previously in extensive forward genetics screens using induced mutants, suggesting that quantitative genetics can be used to find new genes affecting thermal dissipation.
Plants require light energy, by definition, to drive photosynthesis. However, too much light causes photooxidative damage in plants (Barber and Andersson, 1992  ). Thus, plants have diverse defense mechanisms against high light stress (Niyogi, 1999). For example, chloroplasts can move to absorb less light energy (Kasahara et al., 2002), and light-harvesting antenna size in chloroplasts can be reduced (Anderson, 1986). Plants also can harmlessly dissipate excess absorbed light energy as heat (Müller et al., 2001), and they have alternative electron transport pathways to relieve overreduction of electron transport components under stress conditions (Niyogi, 2000; Ort and Baker, 2002).
Thermal dissipation is mediated by a mechanism called feedback deexcitation. Feedback deexcitation dissipates excess absorbed light energy as heat, thereby protecting plants from high-light stress (Horton et al., 1994
Naturally occurring variation in NPQ capacity has been observed in different plant species (Johnson et al., 1993
This kind of natural variation in plant traits, in most cases, shows continuous variations that are under the control of polygenic factors, and quantitative genetic studies are required to understand the genetic basis of the variation (Alonso-Blanco and Koornneef, 2000 In this article, we report natural variation of NPQ among Arabidopsis accessions and test the hypothesis that the variation between a high NPQ accession (Sf-2) and a low NPQ accession (Columbia-0 [Col-0]) is related to the PsbS protein. We measured induction and relaxation of NPQ in Arabidopsis accessions and divided them into high and low NPQ accessions. Biochemical and molecular biological experiments did not associate the NPQ differences with PsbS or other previously identified NPQ factors. Genetic analyses revealed that the differences are controlled by polygenic nuclear factors. To identify these factors, we performed QTL mapping using Sf-2 x Col-0 F2 progeny as a mapping population and identified two high NPQ QTLs. The significance of NPQ variation and possible roles for these QTLs in thermal dissipation are discussed.
NPQ in Arabidopsis Accessions To study the natural variation of NPQ capacity, we initially measured total NPQ in 62 Arabidopsis accessions (Supplemental Table S1). The tested accessions originated from diverse growth conditions, and parental lines of recombinant inbred lines (RILs) that are available or will be available in the near future were also included (http://www.inra.fr/internet/Produits/vast/RILs.htm). To focus on the major qE component, NPQ was measured for 10 min during actinic illumination with 1500 µmol photons m–2 s–1, followed by 5 min in the dark to determine its relaxation. All NPQ measurements were done between 1 and 5 PM to exclude any possible effects of circadian control of NPQ. The results showed that there are variations in NPQ capacity among Arabidopsis accessions (Supplemental Table S1) and that most of the NPQ is qE because it relaxed very fast in the dark (data not shown). Based on these measurements, the accessions were classified into high NPQ and low NPQ Arabidopsis accessions. Ll-1, Sf-2, Ts-1, Van-0, Mz-0, Mr-0, and Kin-0 are high NPQ Arabidopsis accessions containing total NPQ capacity higher than 3.0, whereas Col-0, Landsberg erecta (Ler), and Wassilewskija-2 (Ws-2), so-called lab accessions, are low NPQ Arabidopsis accessions having total NPQ capacity below 2.5 (Supplemental Table S1). Interestingly, the three highest accessions, Ll-1, Sf-2, and Ts-1, all originated from Spain. Except for Ll-1, the other high NPQ accessions have been used as parental lines of RILs, but the RILs were not yet available at the time these experiments were initiated. We decided to use Ll-1 and Sf-2 as high NPQ accessions and Col-0 and Ws-2 as low NPQ accessions for further measurement and characterization. After growing these selected accessions together in identical growth conditions, we measured their NPQ in the next generation. Ll-1 and Sf-2 showed significantly higher total NPQ than Col-0 and Ws-2 after 3 min in actinic illumination (P < 0.01), and the NPQ differences became larger with time (P < 0.001) (Fig. 1 ).
Characterization of NPQ Factors in Selected Accessions
Photosynthetic efficiency and previously identified NPQ factors were compared between these high and low NPQ accessions. First of all, quantum yield of PSII (
To check differences in xanthophyll cycle activity, the contents of each xanthophyll cycle pigment were determined. The deepoxidated xanthophylls, antheraxanthin (A) and zeaxanthin (Z), are generated from violaxanthin (V) by V deepoxidase (VDE) in high light (Yamamoto et al., 1962 ). In low light (150 µmol photons m–2 s–1), Ll-1, Sf-2, Col-0, and Ws-2 contained a very small proportion of deepoxidated forms (A and Z). After being exposed to high light (1,700 µmol photons m–2 s–1) for 4 and 40 min, all accessions showed very similar levels of deepoxidation (Fig. 2C). These results indicated that the high and low NPQ accessions contain functional VDE and that there are no differences in VDE activation by high light between the two groups. Additionally, the chlorophyll a/b ratios reflecting the PSII antenna size were similar to each other (Fig. 2D).
Third, the amount of the PsbS protein was compared. PsbS is required for qE, and qE (and total NPQ) is proportionally increased as the PsbS protein level increases (Li et al., 2000
NPQ of Sf-2 x Col-0 F1 and F2 Progenies
To understand the genetic basis of the NPQ variation, we crossed Ll-1 and Sf-2 to Col-0 and measured induction and relaxation of NPQ in F1 and F2 progenies. Col-0 was used as a low NPQ parental line because the genomic DNA sequences of Col-0 are completely determined, and physical map positions of molecular markers are also available (Arabidopsis Genome Initiative, 2000
Determination of Genotypes
To determine genotype in the F2 mapping population, we developed a polymorphic DNA marker set (Supplemental Table S2). Using the polymorphic markers, genotypes at each marker position were determined in 72 F2 progeny. The genotyping was almost complete, with only a few missing genotype data. From the genotype data, genotype frequencies at marker positions were calculated (Supplemental Fig. S1). The G-test (Dytham, 2003
To find chromosome regions that are responsible for the high NPQ phenotype of Sf-2, we conducted QTL mapping using the R/qtl program (Broman et al., 2003
We also did QTL mapping using NPQ values measured at each minute and found interesting differences between HQE1 and HQE2 (Fig. 6, A–I). The LOD score of HQE1 became significant after 3 min in actinic illumination (Fig. 6C); thereafter, HQE1 remained as a significant high NPQ QTL during the 10-min measurement. At 6 min, HQE1 alone explained 27.9% of total NPQ variance (Table I). The support interval of HQE1 at 6 min was 23 to 47 cM, which was narrower than the interval at 10 min (Table I). In contrast, the response of HQE2 to the actinic light was relatively slower than that of HQE1. HQE2 became a significant QTL after 7 min in the light (Fig. 6G), and it remained significant until the end of the 10-min measurement. Therefore, from 3 to 6 min, only HQE1 seems to be responsible for the high NPQ, and from 7 min in the actinic light, both HQE1 and HQE2 may control the high NPQ phenotype. To confirm our NPQ QTL mapping, we generated near isogenic lines, NQE2, harboring the Sf-2 allele of HQE2 in the Col-0 background. F1 plants of Sf-2 and Col-0 cross were backcrossed to Col-0 four times, and lines were selected based on genotyping. NPQ measurements indicated that NQE2 showed higher NPQ than control lines containing the Col-0 allele of HQE2 (Fig. 7 ).
In our survey of natural variation of NPQ capacity in Arabidopsis, we tried to find some accessions that have much less NPQ than other accessions. In such cases, it might be relatively straightforward to determine the genetic basis for the NPQ difference, as found for other traits (Maloof et al., 2001 ). However, so far, we could not find Arabidopsis accessions having very low NPQ. That might be because NPQ is an important photoprotection mechanism without which plants would suffer more oxidative stress (Li et al., 2002b) and show much lower fitness estimated by lifetime seed production (Külheim et al., 2002).
Several accessions exhibited relatively high NPQ compared to the standard lab accession, Col-0. Why do the high NPQ accessions have a higher capacity for thermal dissipation than other accessions? We found a significant, but very weak correlation between latitude and NPQ among European accessions (data not shown). The latitude of geographical origin has been shown to have a significant relationship with variation of other traits in Arabidopsis (Li et al., 1998
Another possible explanation for the weak relationship between latitude and NPQ is that mechanisms other than NPQ may play a major role in photoprotection in some accessions (Johnson et al., 1993
Strong relationships were observed between deepoxidation state and NPQ capacity among plant species as well as among plants of the same species grown in different light conditions (Johnson et al., 1993 The response of HQE1 to photosynthetically active light was faster than that of HQE2 (Fig. 6, A–J). After being exposed to actinic illumination for 3 min, HQE1 became a significant high NPQ QTL (Fig. 6C), and from 7 min, both HQE1 and HQE2 were responsible for the high NPQ (Fig. 6G). These results indicated that early NPQ induction might be affected by HQE1 alone, and saturated NPQ levels might be explained by both HQE1 and HQE2 without any interaction between HQE1 and HQE2. Therefore, it could be speculated that sudden changes in light intensity would be dealt with by NPQ controlled by HQE1 and that, if the high light intensity continues, HQE2 and HQE1 together increase NPQ capacity to cope with the high light. Although HQE1 was the only identified significant QTL between 3 and 6 min, the NPQ measured during that period time was widely distributed (Fig. 5). In conclusion, we were able to identify high and low NPQ Arabidopsis accessions and map QTLs that influence NPQ in two of these accessions. This information provides a guideline for selection of appropriate RILs and experimental design for future NPQ QTL mapping. We have also developed DNA molecular markers showing polymorphisms between Sf-2 and Col-0 that can be used for genotyping of Sf-2 x Col-0 RILs. Although we had hypothesized that the difference in NPQ between the accessions would be related to PsbS, no differences in known NPQ factors were found. Analysis of other accessions might reveal cases in which NPQ variation is related to PsbS. Identification of the high NPQ QTLs described here will eventually make it possible to clone new genes responsible for high NPQ.
Plant Materials and Growth Conditions Arabidopsis (Arabidopsis thaliana) seeds were obtained from the Arabidopsis Biological Resource Center and from the seed collection of the Niyogi laboratory. Before planting on soil, the seeds were kept in water at 4°C for 1 week. Arabidopsis plants were grown in short-day conditions (10 h light/14 h dark) for 5 to 6 weeks in a light- (150 µmol photons m–2 s–1) and temperature (22°C)-controlled growth chamber before chlorophyll fluorescence measurements and leaf tissue harvests.
Plants were dark-adapted for 2 h before NPQ measurement. The measurement began at 1 PM, and all measurements were completed by 5 PM. Chlorophyll fluorescence parameters were measured on attached rosette leaves using an FMS2 fluorometer (Hansatech) during actinic illumination with 1,500 µmol photons m–2 s–1 for 10 min, followed by darkness for 5 min. NPQ was calculated as (Fm – Fm')/Fm', with Fm and Fm' being maximum fluorescence measured after dark adaptation and in the light-adapted condition, respectively, by applying a saturating pulse of light.
Pigment analyses were done following Niyogi laboratory protocols with some modifications (Müller-Moulé et al., 2002
Total proteins were extracted from plant leaves of each accession. Leaf tissue (200 mg) was frozen in liquid nitrogen and then ground to a fine powder. To the tissue powder, 200 µL protein extraction buffer (4% [w/v] SDS, 25 mM Tris-HCl, pH 8.8, and 2.5% [v/v] glycerol) was added to the tissue powder. Following further grinding in the buffer, the protein samples were denatured in boiling water for 5 min. After centrifugation for 3 min, the supernatant was separated and then kept in a –70°C freezer. The protein concentration was determined using a Bio-Rad Protein assay kit (Bio-Rad Laboratories), and 30 µg of total proteins were loaded in each well of a precast 10% to 20% Tris-Glycine gel (Invitrogen). The separated proteins were blotted onto a nitrocellulose membrane (Schleicher & Schuell) using a semidry transfer unit (Hoefer Pharmacia Biotech). For quantification of the PsbS protein, a polyclonal antibody raised against a PsbS oligopeptide was used (Li et al., 2002a Genomic DNA sequences were determined from PCR-amplified DNA. For PCR from genomic DNA, primers were designed using the web-based Primer3 program (http://www.broad.mit.edu/cgi-bin/primer/primer3_www.cgi), and PCR products were separated on agarose gels and then purified using a gel extraction kit (Qiagen). Sequencing of purified DNA was performed using the Big-Dye Terminator v3.0 ready reaction cycle sequencing kit (Applied Biosystems) and an ABI 3100 automated DNA sequencer (Applied Biosystems).
PCR conditions for previously available markers were obtained from The Arabidopsis Information Resource, and restriction enzymes used for each marker are listed in Supplemental Table S2. For NQE2, CZSOD2 and T27E13 were used to determine genotypes between ER and C4H, and COP1 and VE017 were used for genotyping between C4H and NGA168. The newly generated insertion/deletion markers for Sf-2 x Col-0 were C42050 (forward: 5'-GCTGAGTATAGAGCAGGTTGGTG-3'; reverse: 5'-CGTCCTGTTTCAATTTGTCATC-3') and D01650 (forward: 5'-CTGCTTTTAGACCGCTTTCC-3'; reverse: 5'-TCCCAATGCTAAGTTCTGCTG-3'). PCR for C42050 was annealed at 60°C and polymerized at 72°C for 30 s. Annealing for D01650 was at 59°C, and polymerization lasted for 1 min. The PCR products of C42050 and D01650 were separated on 3% and 1.2% agarose gels, respectively. The newly developed cleaved-amplified polymorphic sequence markers were SNP397C (forward: 5'-TTTGAGCTTGTTTCCTCGTG-3'; reverse: 5'-ATATCTGTGGGGTTGCTTGG-3'), A44575 (forward: 5'-CAAACCCAAAACCAAAGCTG-3'; reverse: 5'-TGCTTACATGGGGGAAAAAG-3'), SNP299C (forward: 5'-TTGAAGGCATGAGTTGTTGG-3'; reverse: 5'-CGCCGATTTAGTACGACTACG-3'), and D12320 (forward: 5'-TGGGAGAGCCTAATGTTTCTG-3'; reverse: 5'-CCAACCACCAAATCCTTCAC-3'). The PCR reactions of SNP397C and SNP299C were annealed at 58°C and polymerized for 1 min, and then the PCR products were digested with HpyCh4 IV and DdeI, respectively. Amplified A44575 DNA following PCR at 59°C annealing and 1 min polymerization was digested with HinfI. PCR for D12320 was done at 59°C annealing and 30 s polymerization, and then DdeI-digested fragments were separated on 3% agarose gels.
For genotyping, genomic DNA was extracted as follows: frozen small leaves were ground in a 1.5-mL tube and then the fine powder was thawed in 10 µL of alkali solution (0.5 N NaOH) (Klimyuk et al., 1993
Test statistics including ANOVA, Student's t test and multiple comparison tests were calculated using Microsoft Excel and XLSTAT. Following the genotyping, a G-test was used to test whether the genotype ratio at each marker position fitted to the expected F2 segregation ratio (Supplemental Fig. S1) (Dytham, 2003
QTL mapping was performed using the R/qtl program (Broman et al., 2003
The following materials are available in the online version of this article.
We thank Jae Pasari and Carsten Külheim for technical support and Prof. Anastasios Melis for providing the D1 antibody. This manuscript was improved by the critical comments of Ben Gutman, Heidi Ledford, and Xiao-Ping Li. Our special thanks go to Dr. Dan Kliebenstein, who gave us initiative for this study. Received February 26, 2009; accepted March 30, 2009; published April 1, 2009.
1 This work was supported by the Office of Basic Energy Sciences, Chemical Sciences Division, U.S. Department of Energy (contract DE–AC03–76SF000098). 
2 Present address: Plant Biology Laboratory, Salk Institute, La Jolla, CA 92037. The author responsible for the distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Krishna K. Niyogi (niyogi{at}nature.berkeley.edu).
[W] The online version of this article contains Web-only data.
[OA] Open access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.137828 * Corresponding author; e-mail niyogi{at}nature.berkeley.edu.
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PSII) measuring the proportion of energy used for photochemistry (Maxwell and Johnson, 2000
