Lutein-mediated photoprotection of photosynthetic machinery in Arabidopsis thaliana exposed to chronic low ultraviolet-B radiation

Citation

Biswas, D.K., Ma, B.L., Xu, H., Li, Y., Jiang, G. (2020). Lutein-mediated photoprotection of photosynthetic machinery in Arabidopsis thaliana exposed to chronic low ultraviolet-B radiation. Journal of Plant Physiology, [online] 248 http://dx.doi.org/10.1016/j.jplph.2020.153160

Plain language summary

Plant response to UV radiations depends on the nature of UV-B treatments and the extent of plant adaptation and acclimation to UV-B. Studies have shown that the ratio of total carotenoids to chlorophyll may decrease or increase in the UV-B-exposed plants. The level of ß-carotene is generally found to be increased and decreased in the plants exposed to UV-A and high UV-B, respectively. Similarly, plant exposure to UVA alone increases the level of total carotenoids, while plant exposure to low UV-B decreases total carotenoid levels in some Arabidopsis ecotypes. Available research report on the effects of low UV-B on Arabidopsis thaliana demonstrates a reduction in rosette diameter and inflorescence length, but an increase in the numbers of flowering stems, indicating that chronic low UV-B treatment mostly causes redistribution of resources
rather than cessation of growth. Although low UV-B dose has no significant effect on growth, it can alter reactive
oxygen species (ROS) metabolism through an up-regulation of enzymes of the phenylpropanoid pathway and anti-oxidative systems. This may lead to changes in the content, composition and functions of carotenoids including xanthophyll cycle pigments, and hence plant UV-B tolerance.

In this research, we hypothesized that low UV-B might alter carotenoid profile, which can modulate light harvesting and photoprotection of PSII in plants. In addition to low UV-B, a low Photosynthetically Active Radiation (PAR) is also used in the present study as high-PAR intensities are reported to modify changes in gene expression.

In this study, we found that exposure of plants to chronic low UV-B for 10 days had no adverse effect on PSII function and plant growth. Despite a lack of visible UV-B stress, plants showed differential acclimation responses to chronic radiation treatments in terms of induction of phenolics and carotenoid profile. Plants raised at PAR+UV-A+B showed higher induction of total phenolics than those raised at both PAR+UV-A and PAR-only regimes. A higher accumulation of violaxanthin and neoxanthin was observed in plants grown under PAR+UV-A and PAR+UVA+B than in those grown under PAR-only. The levels of lutein, 9-cis ß-carotene and total ß-carotene were found to be increased in plants raised under PAR+UV-A+B than in those raised under PAR and PAR +UV-A. Plant UV-B tolerance as determined by plant exposure to acute high UV-B stress for 4 h following chronic radiation treatments indicated an occurrence of photoinhibition of PSII due to an increase in a non-radiative thermal deactivation as documented by an increase in F0 for the plants raised under both PAR and PAR+UV-A regimes. On the other hand, plant exposure to acute high UV-B for 6 h following plant exposure to chronic PAR and PAR+UV-A regimes resulted in an occurrence of damage to the PSII reaction centers as evidenced by significant decrease in Fm in those plants. The results also indicated that UV-A-induced higher accumulations of violaxanthin and neoxanthin along with low induction of phenolics were not associated with plant UV-B protection. Taken together, the findings of this study indicate that xanthophyll cycle pigments were not involved in plant UV-B protection, but induction of phenolics and lutein-mediated development of qN were involved in photoprotection of PSII in the plants against UV-B-induced oxidative stress. The results from this study is valuable in the understanding of plant acclimation to low UV-B and the role of specific carotenoid in light harvesting, photoprotection of PSII and plant UV-B tolerance.

Abstract

Ecologically relevant low UV-B is reported to alter reactive oxygen species metabolism and anti-oxidative systems through an up-regulation of enzymes of the phenylpropanoid pathway. However, little is known about low UV-B-induced changes in carotenoid profile and their impacts on light harvesting and photoprotection of photosystem II (PSII) in plants. We investigated carotenoids profile, chlorophyll pigments, phenolics, photosynthetic efficiency and growth in Arabidopsis thaliana (Col-0) plants grown under photosynthetically active radiation (PAR), PAR+ ultraviolet (UV)-A and PAR+UV-A+B regimes for 10 days in order to assess plant acclimation to low UV-B radiation. A chlorophyll fluorescence assay was used to examine UV-B tolerance in plants further exposed to acute high UV-B for 4 and 6 h following a 10-day growth under different PAR and UV regimes. We found that both PAR+ UV-A and PAR+UV-A+B regimes had no negative effect on quantum efficiency, electron transport rate, rosette diameter, relative growth rate and shoot dry weight of plants. Chronic PAR+ UV-A regime considerably (P < 0.05) increased violaxanthin (26 %) and neoxanthin (92 %) content in plants. Plant exposure to chronic PAR+UV-A+B significantly (P < 0.05) increased violaxanthin (48 %), neoxanthin (63 %), lutein (33 %), 9-cis ß-carotene (28 %), total ß-carotene (29 %) and total phenolics (108 %). The maximum photochemical efficiency (Fv/Fm) in leaves was found to be positively correlated with total phenolics (rho = 0.81 and rho = 0.91, P < 0.05 for 4 and 6 h, respectively) and non-photochemical quenching (qN) (rho = 0.81 and rho = 0.84, P < 0.05 for 4 and 6 h, respectively) in plants exposed to acute high UV-B for 4 and 6 h following a 10-day growth under chronic PAR+UV-A+B. There was also a significant positive correlation (rho = 0.93, P < 0.01) between qN and lutein content in the plants exposed to acute high UV-B stress for 4 h following plant exposure to chronic PAR+UV-A+B. The findings from our study indicate that plants grown under chronic PAR+UV-A+B displayed higher photoprotection of PSII against acute high UV-B stress than those grown under PAR and PAR+ UV-A regimes. An induction of phenolics and lutein-mediated development of qN were involved in the photoprotection of PSII against UV-B-induced oxidative stress.