A comparison of pine and spruce in recovery from winter stress; changes in recovery kinetics, and the abundance and phosphorylation status of photosynthetic proteins during winter

Abstract

During winter evergreens maintain a sustained form of thermal energy dissipation that results in reduced photochemical efficiency measured using the chlorophyll fluorescence parameter Fv/Fm. Eastern white pine (Pinus strobus L.) and white spruce [Picea glauca (Moench) Voss] have been shown to differ in their rate of recovery of Fv/Fm from winter stress. The goal of this study was to monitor changes in photosynthetic protein abundance and phosphorylation status during winter recovery that accompany these functional changes. An additional goal was to determine whether light-dependent changes in light harvesting complex II (LHCII) phosphorylation occur during winter conditions. We used a combination of field measurements and recovery experiments to monitor chlorophyll fluorescence and photosynthetic protein content and phosphorylation status. We found that pine recovered three times more slowly than spruce, and that the kinetics of recovery in spruce included a rapid and slow component, while in pine there was only a rapid component to recovery. Both species retained relatively high amounts of the light harvesting protein Lhcb5 (CP26) and the PsbS protein during winter, suggesting a role for these proteins in sustained thermal dissipation. Both species maintained high phosphorylation of LHCII and the D1 protein in darkness during winter. Pine and spruce differed in the kinetics of the dephosphorylation of LHCII and D1 upon warming, suggesting the rate of dephosphorylation of LHCII and D1 may be important in the rapid component of recovery from winter stress. Finally, we demonstrated that light-dependent changes in LHII phosphorylation do not continue to occur on subzero winter days and that needles are maintained in a phosphorylation pattern consistent with the high light conditions to which those needles are exposed. Our results suggest a role for retained phosphorylation of both LHCII and D1 in maintenance of the photosynthetic machinery in a winter conformation that maximizes thermal energy dissipation.

Direct energy transfer from photosystem II to photosystem I confers winter sustainability in Scots Pine

“…In conclusion, during early spring only a very small fraction of the absorbed light energy in PSII antennae is utilized for PSII photochemistry (ΦPSII) and the fast inducible NPQ (qE) is low since it not only requires a high ΔpH 3,6,17 but there is a strong static quenching present already. On the other hand protection from extreme oxidative stress and rearrangement of thylakoid complexes are likely coupled to the high zeaxanthin content [51][52][53] (Supplementary table 2), and probably to pronounced phosphorylation of antenna and core proteins present under these conditions 54 . In this situation, the excess energy is dissipated primarily through direct energy transfer from PSII to PSI, which appears in steady-state (PAM) fluorescence measurements as a non-regulated constitutive energy quenching.…”

The unique photosynthetic apparatus of Pinaceae: analysis of photosynthetic complexes in Picea abies

“…During winter and early spring a sustained form of non-photochemical light energy dissipation is activated, which takes several days to fully relax even in favorable conditions (Verhoeven, 2013). During winter quenching, Pinaceae also retain large amounts of the xanthophyll cycle pigments zeaxanthin and antheraxanthin (Ottander et al , 1995; Verhoeven et al ., 1996, 1999, 2009; Merry et al , 2017). The acclimation process also involves changes in thylakoid protein phosphorylation and in the relative abundance of photosynthetic proteins (Ottander et al , 1995; Verhoeven et al , 2009; Merry et al , 2017).…”

“…During winter quenching, Pinaceae also retain large amounts of the xanthophyll cycle pigments zeaxanthin and antheraxanthin (Ottander et al , 1995; Verhoeven et al ., 1996, 1999, 2009; Merry et al , 2017). The acclimation process also involves changes in thylakoid protein phosphorylation and in the relative abundance of photosynthetic proteins (Ottander et al , 1995; Verhoeven et al , 2009; Merry et al , 2017). However, results in the literature on this topic vary depending on the species investigated and on environmental conditions during the studies (for review see Verhoeven, 2014).…”

Is zeaxanthin needed for desiccation tolerance? Sustained forms of thermal dissipation in tolerant versus sensitive bryophytes

“…A separate goal of our study was to determine whether alterations in phosphorylation of thylakoid proteins occurs in response to desiccation. There is some evidence that retained phosphorylation of LHCII and PSII core proteins (particularly D1) might provide a form of photoprotection in extreme stress conditions such as low temperatures by enhancing spillover quenching (Merry et al, 2017; Tikkanen & Aro, 2014). It is thought that, in nonstressful conditions, the dephosphorylation of LHCII that occurs in high light conditions reduces the connectivity between PSII and PSI and prevents energy spillover from PSII to PSI (Mekala et al, 2015; Tikkanen & Aro, 2014).…”

“…Additionally, phosphorylation of the PSII core proteins D1, D2, and CP43 are thought to signal protein damage to the PSII proteins and thus facilitate the PSII repair cycle (Järvi et al, 2015; Tikkanen et al, 2008). A study examining the thylakoid protein phosphorylation of conifer needles during winter found increased retention of LHCII and D1 protein phosphorylation regardless of light environment, suggesting a potential role for increased connectivity between LHCII and PSI that may allow for increased sustained forms of thermal dissipation involving spillover quenching between the PSII and PSI (Merry et al, 2017). Currently, it is not known whether there is a role for adjustments in thylakoid protein phosphorylation during the extreme stress of desiccation.…”