Examining the photoprotection hypothesis for adaxial foliar anthocyanin accumulation by revisiting comparisons of green- and red-leafed varieties of coleus (Solenostemon scutellarioides)

Abstract

Although plants rely on light to drive energy production via photosynthesis, excess light can be harmful. Plants have evolved photoprotective mechanisms to mitigate this threat, including thermal energy dissipation, the most common form of which involves de-epoxidized constituents of the xanthophyll cycle facilitating the conversion of excess excitation energy to heat. A role in photoprotection has also been proposed for red anthocyanins when they accumulate near the adaxial leaf surface. Here, we compared the response to experimental light stress of a red-leafed (anthocyanin rich) and a green-leafed variety of coleus [Solenostemon scutellarioides (L.) Codd], examining chlorophyll fluorescence emission and pigment composition. After experimentally imposed intense white light, red- and green-leafed coleus exhibited manifestations of light stress (decreased photosystem II quantum efficiency) of a similar magnitude. This, considered alone, could be interpreted as evidence that anthocyanins do not serve a photoprotective role. However, during excess light exposure, the green-leafed variety employed a greater level of thermal energy dissipation and possessed correspondingly higher xanthophyll cycle pool sizes and de-epoxidation states. During exposure to red light, which anthocyanins absorb very poorly, levels of thermal energy dissipation did not differ between coleus varieties. Taken together, our findings suggest that adaxial anthocyanins minimize stress associated with excess light absorption and that the green-leafed variety of coleus compensated for its much lower levels of adaxial anthocyanins by invoking higher levels of energy dissipation. Thus, anthocyanin accumulation should be considered alongside the suite of photoprotective mechanisms employed by photosynthetic tissues.

Multiple functional roles of anthocyanins in plant-environment interactions

“…Red-leafed morphs sometimes hold a smaller pool of the xanthophyll pigments violaxanthin, antheraxanthin and zeaxanthin (VAZ) as compared with green-leafed morphs when grown under high sunlight, which is consistent with the idea that anthocyanins might in part compensate for the effects of deepoxidation of violaxanthin in the photo-protective xanthophyll cycle (Cavender-Bares et al, 1999;Logan et al, 2015). Consistent with this, the VAZ pool and the de-epoxidation state (DES) of VAZ were found to be markedly greater in a green than a red basil cultivar growing in full sunlight .…”

Photosynthetic activity of variegated leaves of Coleus × hybridus hort. cultivars characterised by chlorophyll fluorescence techniques

“…Both groups of pigments participate in photoprotection but their mode of action may be either similar or different. While Cars dissipate energy as heat, the effect of anthocyanins is light attenuating (shading) of the photosynthetic tissue (Neill and Gould 2003, Nielsen and Simonsen 2011, Liakopoulos and Spanorigas 2012, Henry et al 2012, Logan et al 2015. In Coleus, anthocyanins are accumulated on the adaxial surface of the leaves, and provide photoprotection to LHC (Burger and Edwards 1996, Henry et al 2012, Logan et al 2015.…”

“…While Cars dissipate energy as heat, the effect of anthocyanins is light attenuating (shading) of the photosynthetic tissue (Neill and Gould 2003, Nielsen and Simonsen 2011, Liakopoulos and Spanorigas 2012, Henry et al 2012, Logan et al 2015. In Coleus, anthocyanins are accumulated on the adaxial surface of the leaves, and provide photoprotection to LHC (Burger and Edwards 1996, Henry et al 2012, Logan et al 2015. Anthocyanins may participate in photoprotection through their antioxidant capacity, and some are capable of absorbing parts of the UV spectra similarly to the Cars (Neill and Gould 2003, Khoo et al 2011, Takahashi and Badger 2011.…”

“…Anthocyanins may participate in photoprotection through their antioxidant capacity, and some are capable of absorbing parts of the UV spectra similarly to the Cars (Neill and Gould 2003, Khoo et al 2011, Takahashi and Badger 2011. In the absence of anthocyanins, green leaves utilise thermal energy dissipation via the xanthophyll cycle (Henry et al 2012, Logan et al 2015. In our experiment, it can be reflected by high NPQ values, and according to many authors (Maxwell and Johnson 2000, Montanaro et al 2007, Sofo et al 2009, Bączek-Kwinta et al 2011, it can be related to energy dissipation as heat via the xanthophyll cycle and other Cars, as well as conformational changes in PSII antennae (LHC).…”

“…They are accumulated in vacuoles of adaxial epidermal or palisade parenchyma cells and act as a photoshield, especially in developing and senescing leaves as well as during exposure to intense light in combination with environmental stresses, such as low temperature or low nutrient availability (Gould 1995, Henry et al 2012, Liakopoulos and Spanorigas 2012, Logan et al 2015.…”