UV Radiation Induces Specific Changes in the Carotenoid Profile of Arabidopsis thaliana

Abstract

UV-B and UV-A radiation are natural components of solar radiation that can cause plant stress, as well as induce a range of acclimatory responses mediated by photoreceptors. UV-mediated accumulation of flavonoids and glucosinolates is well documented, but much less is known about UV effects on carotenoid content. Carotenoids are involved in a range of plant physiological processes, including photoprotection of the photosynthetic machinery. UV-induced changes in carotenoid profile were quantified in plants (Arabidopsis thaliana) exposed for up to ten days to supplemental UV radiation under growth chamber conditions. UV induces specific changes in carotenoid profile, including increases in antheraxanthin, neoxanthin, violaxanthin and lutein contents in leaves. The extent of induction was dependent on exposure duration. No individual UV-B (UVR8) or UV-A (Cryptochrome or Phototropin) photoreceptor was found to mediate this induction. Remarkably, UV-induced accumulation of violaxanthin could not be linked to protection of the photosynthetic machinery from UV damage, questioning the functional relevance of this UV response. Here, it is argued that plants exploit UV radiation as a proxy for other stressors. Thus, it is speculated that the function of UV-induced alterations in carotenoid profile is not UV protection, but rather protection against other environmental stressors such as high intensity visible light that will normally accompany UV radiation.

Keywords: UV-B; arabidopsis; carotenoid; photoreceptor; photosynthesis; xanthophyll.

Figure 1

Simplified plant carotenoid biosynthetic pathway. Text in red refers to the enzymes LCY-ε (lycopene epsilon cyclase), LCY-β (lycopene beta cyclase), BCH (carotenoid beta-ring hydroxylase), ZEP (zeaxanthin epoxidase), VDE (violaxanthin de-epoxidase)) that catalyse various steps of the carotenoid pathway. Mutants in several of these genes were used in this study as specified in Table 1 (ZEP, aba1; LCY-ε, lut1; VDE, npq1-2; LCY-β and VDE, szl1-1npq1-2).

Figure 2

Carotenoid contents (µg·g⁻¹ FW, except DEPS) of wild-type Arabidopsis thaliana (Col-0) exposed to varying durations of UV. Plants were subjected to UV treatment for 3.75 h daily and harvested after 18 h on days 2, 4, 6, 8 and 10. Bar plots show means and error bars indicate standard error for n = 5. The text in each panel shows the outcome of a two-way ANOVA across treatment and exposure duration. The stars above pairs of bars show the outcome of t-tests between the UV treatments. In both cases * (p < 0.05), ** (p < 0.01), *** (p < 0.001), **** (p < 0.0001), depict significant differences with ns depicting a non-significant difference.

Figure 3

Photosynthetic efficiency of wild-type Arabidopsis thaliana (Col-0) exposed to varying durations of UV. Plants were subjected to UV treatment for 3.75 h daily and harvested after 18 h on days 2, 4, 6, 8 and 10. F_v/F_m: the maximum quantum efficiency of photosystem II (PSII); Y(II): the quantum efficiency of PSII under steady-state light conditions; Y(NO): yield of non-regulated non-photochemical energy dissipation and Y(NPQ): the yield of the regulated non-photochemical energy dissipation. Bar plots show means and error bars for n = 5. The text in each panel shows the outcome of a two-way ANOVA across treatment and exposure duration. The stars above pairs of bars show the outcome of t-tests between the UV treatments. In both cases * (p < 0.05), ** (p < 0.01) and *** (p < 0.001) depict significant differences with ns depicting a non-significant difference.

Figure 4

Photosynthetic efficiency of wild-type (WT) and photoreceptor deficient Arabidopsis thaliana (Col-0) exposed to UV; cry1cry2 (cryptochrome), phot1phot2 (phototropin) and uvr8 (UV-B photoreceptor). Plants were subjected to UV treatment for 3.75 h daily and harvested after 18 h on day 4. F_v/F_m: the maximum quantum efficiency of photosystem II (PSII); Y(II): the quantum efficiency of PSII under steady-state light conditions; Y(NO): yield of non-regulated non-photochemical energy dissipation and Y(NPQ): the yield of regulated non-photochemical energy dissipation. Bar plots show means and error bars indicate standard error for n = 5. The text in each panel shows the outcome of a two-way ANOVA across treatment and exposure duration. The stars above pairs of bars show the outcome of t-tests between the UV treatments. In both cases * (p < 0.05), ** (p < 0.01) and *** (p < 0.001) depict significant differences with ns depicting a non-significant difference.

Figure 5

Carotenoid contents (µg·g⁻¹ FW, except DEPS) of wild-type (WT) and carotenoid biosynthesis (aba1-6, lut1, npq1-2, npq4-1 and szl1-1npq1-2) impaired Arabidopsis thaliana (Col-0). Plants were subjected to UV treatment for 3.75 h daily and harvested after 18 h on day 4. Bar plots show means and error bars indicate standard error for n = 5. The text in each panel shows the outcome of a two-way ANOVA across treatment and exposure duration. The stars above pairs of bars show the outcome of t-tests between the UV treatments. In both cases * (p < 0.05), ** (p < 0.01) and *** (p < 0.001) depict significant differences with ns depicting a non-significant difference.

Figure 6

Photosynthetic efficiency of wild-type (WT) and carotenoid biosynthesis (aba1-6, lut1, npq1-2, npq4-1 and szl1-1npq1-2) impaired Arabidopsis thaliana (Col-0). Plants were subjected to UV treatment for 3.75 h daily and harvested after 18 h on day 4. F_v/F_m: the maximum quantum efficiency of photosystem II (PSII); Y(II): the quantum efficiency of PSII under steady-state light conditions; Y(NO): yield of non-regulated non-photochemical energy dissipation and Y(NPQ): the yield of regulated non-photochemical energy dissipation. Bar plots show means and error bars indicate standard error for n = 5. The text in each panel shows the outcome of a two-way ANOVA across treatment and exposure duration. The stars above pairs of bars show the outcome of t-tests between the UV treatments. In both cases * (p < 0.05) and *** (p < 0.001) depict significant differences with ns depicting a non-significant difference.

Figure 7

Principal component analysis showing the distribution of UV treated and/or control carotenoid impaired Arabidopsis genotypes (score plot), based on the influence of carotenoids and photosynthetic efficiency parameters (loading plot).