Abstract

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.

Highlights

  • Feedback deexcitation is a photosynthetic regulatory mechanism that can protect plants from high light stress by harmlessly dissipating excess absorbed light energy as heat

  • We report natural variation of nonphotochemical quenching (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

  • After being exposed to high light (1,700 mmol photons m22 s21) 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 V deepoxidase (VDE) and that there are no differences in VDE activation by high light between the two groups

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Summary

Present address

Plant Biology Laboratory, Salk Institute, La Jolla, CA 92037. Naturally occurring variation in NPQ capacity has been observed in different plant species (Johnson et al, 1993; Demmig-Adams and Adams, 1994; DemmigAdams, 1998). Genetic analyses revealed that the differences are controlled by polygenic nuclear factors To identify these factors, we performed QTL mapping using Sf-2 3 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. 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 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)

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