Dehydration-mediated activation of the xanthophyll cycle in darkness: is it related to desiccation tolerance?

Abstract

The development of desiccation tolerance by vegetative tissues was an important step in the plants' conquest of land. To counteract the oxidative stress generated under these conditions the xanthophyll cycle plays a key role. Recent reports have shown that desiccation itself induces de-epoxidation of xanthophyll cycle pigments, even in darkness. The aim of the present work was to study whether this trait is a common response of all desiccation-tolerant plants. The xanthophyll cycle activity and the maximal photochemical efficiency of PS II (F(v)/F(m)) as well as β-carotene and α-tocopherol contents were compared during slow and rapid desiccation and subsequent rehydration in six species pairs (with one desiccation-sensitive and one desiccation-tolerant species each) belonging to different taxa. Xanthophyll cycle pigments were de-epoxidised in darkness concomitantly with a decrease in F(v)/F(m) during slow dehydration in all the desiccation-tolerant species and in most of the desiccation-sensitive ones. De-epoxidation was reverted in darkness by re-watering in parallel with the recovery of the initial F(v)/F(m). The stability of the β-carotene pool confirmed that its hydroxylation did not contribute to zeaxanthin formation. The α-tocopherol content of most of the species did not change during dehydration. Because it is a common mechanism present in all the desiccation-tolerant taxa and in some desiccation-sensitive species, and considering its role in antioxidant processes and in excess energy dissipation, the induction of the de-epoxidation of xanthophyll cycle pigments upon dehydration in the dark could be understood as a desiccation tolerance-related response maintained from the ancestral clades in the initial steps of land occupation by plants.

The Physcomitrella patens Chloroplast Proteome Changes in Response to Protoplastation

“…Notably, the observed significant decrease in chlorophyll fluorescence during maceration of protonema is similar to the quenching that occurs in many poikilohydric plants in response to dehydration (Heber et al, 2006; Nabe et al, 2007; Fukuda et al, 2008; Heber, 2008; Fernandez-Marin et al, 2011). Similar quenching can also take place in poikilohydric plant chloroplasts as a response to osmotic stress (Azzabi et al, 2012).…”

“…Similar quenching can also take place in poikilohydric plant chloroplasts as a response to osmotic stress (Azzabi et al, 2012). Though the quenching mechanism is not well understood, it is known to be triggered by the dehydration-mediated activation of the xanthophyll cycle (Fernandez-Marin et al, 2011), Psbs- and LHCSR-dependent pathways (Peers et al, 2009) and conformational rearrangement of pigment-protein complexes (Heber, 2008). For P. patens , there are two simultaneous mechanisms for quenching: Psbs-dependent, which is specific for higher plants, and LHCSR-dependent, which is typical of algae (Gerotto et al, 2012).…”

Photoprotective Strategies of Mediterranean Plants in Relation to Morphological Traits and Natural Environmental Pressure: A Meta-Analytical Approach

“…Thus, high predawn AZ/VAZ values were observed only in plants with a low stomatal conductance (Figure 5D). Drought-stress induction of overnight retention of A+Z has been described in desert and desiccation-tolerant plants (Barker et al, 2002; Fernández-Marín et al, 2011, 2013). Here, we confirm that this mechanism is also activated at milder stress levels, such as that exerted by Mediterranean summer, being more universal than previously expected.…”

Effects of hypo- and hypersalinity on photosynthetic performance of Sargassum fusiforme (Fucales, Heterokontophyta)

“…Prolonged immersion under hypersalinity condition may cause dissociation of oxygen evolving complex of PSII (Allakhverdiev and Murata 2008). Under such circumstance, xanthophyll cycle, which is one of the most important photoprotection processes in algae and plants involved in the dissipation of excessive energy via modulating the architecture of LHCII (García-Plazaola et al 2012, Jahns and Holzwarth 2012, Ruban et al 2012, could be activated in most desiccation-tolerant algal species (Harker et al 1999, Gévaert et al 2003, Fernández-Marín et al 2011a, 2011b, Xie et al 2013. In contrast, the effects of hyposalinity condition on the photosynthesis and the operation of xanthophyll cycle in marine algae are relatively less investigated, though such condition also often occurs in estuarine and intertidal zone, e.g.…”