Shedding light on the dark side of xanthophyll cycles

Abstract

Summary Xanthophyll cycles are broadly important in photoprotection, and the reversible de‐epoxidation of xanthophylls typically occurs in excess light conditions. However, as presented in this review, compiling evidence in a wide range of photosynthetic eukaryotes shows that xanthophyll de‐epoxidation also occurs under diverse abiotic stress conditions in darkness. Light‐driven photochemistry usually leads to the pH changes that activate de‐epoxidases (e.g. violaxanthin de‐epoxidase), but in darkness alternative electron transport pathways and luminal domains enriched in monogalactosyl diacyl glycerol (which enhance de‐epoxidase activity) likely enable de‐epoxidation. Another ‘dark side’ to sustaining xanthophyll de‐epoxidation is inactivation and/or degradation of epoxidases (e.g. zeaxanthin epoxidase). There are obvious benefits of such activity regarding stress tolerance, and indeed this phenomenon has only been reported in stressful conditions. However, more research is required to unravel the mechanisms and understand the physiological roles of dark‐induced formation of zeaxanthin. Notably, the de‐epoxidation of violaxanthin to antheraxanthin and zeaxanthin in darkness is still a frequently ignored process, perhaps because it questions a previous paradigm. With that in mind, this review seeks to shed some light on the dark side of xanthophyll de‐epoxidation, and point out areas for future work.

Freezing induces an increase in leaf spectral transmittance of forest understorey and alpine forbs

“…Fresh leaves from the understorey species showed high F v /F m values of 0.82, and similarly, fresh leaves of the alpine species had high F v /F m at 0.78 on average. Values of F v /F m slightly below 0.8, such as these, are common under optimal conditions for alpine species generally [24,25,62]. Acclimation of photosynthetic apparatus from freezing-tolerant species to low temperatures is usually accompanied by a downregulation of predawn F v /F m values [23,24].…”

“…These sudden fluctuations in temperature during periods when full physiological function is still returning to overwintering leaves often causes chlorophyll degradation [16] and stimulates accumulation of antioxidant pigments, such as anthocyanins, which ameliorate stress at low temperatures [17,18], and other flavonoids which have additional roles including UV-screening, frost protection and herbivory defence [17,[19][20][21]. Freezing, also generates changes in the pigment composition of leaves: for instance, in frost-tolerant leaves freezing induces the de-epoxidation of xanthophyll cycle carotenoids involved in photoprotection [22], even in darkness [23][24][25].…”

Xanthophyll cycles in the juniper haircap moss (Polytrichum juniperinum) and Antarctic hair grass (Deschampsia antarctica) on Livingston Island (South Shetland Islands, Maritime Antarctica)

“…Among other gaps in knowledge, the relationship between the operation of the VAZ cycle and the photochemical efficiency has not been characterised in all ecosystems and plant functional groups. In addition, it has been shown that particular conditions, such as desiccation, can lead to the accumulation of Z in darkness (Fernández-Marín et al 2021). Additionally, low temperatures block ZE activity, impeding the reconversion of Z into V during the night (Verhoeven 2014).…”

The Loroxanthin Cycle: A New Type of Xanthophyll Cycle in Green Algae (Chlorophyta)

“…The final one is the Lutein – Siphonaxanthin (LS) cycle ( Raniello et al, 2006 ; for more details see García-Plazaola et al, 2007 ). Most cycles consist of the de-epoxidation of xanthophylls in (light) stress and their epoxidation in the absence of stress [low light (LL) or darkness; Goss and Latowski, 2020 ; Fernández-Marín et al, 2021 ]. The epoxy- and epoxy-free xanthophylls have different properties that favor light-harvesting or photoprotection ( Havaux, 1998 ).…”