Protection and storage of chlorophyll in overwintering evergreens

Abstract

How evergreen species store and protect chlorophyll during exposure to high light in winter remains unexplained. This study reveals that the evergreen snow gum (Eucalyptus pauciflora Sieb. ex Spreng.) stores and protects its chlorophylls by forming special complexes that are unique to the winter-acclimated state. Our in vivo spectral and kinetic characterizations reveal a prominent component of the chlorophyll fluorescence spectrum around 715 nm at 77 K. This band coincides structurally with a loss of chlorophyll and an increase in energy-dissipating carotenoids. Functionally, the band coincides with an increased capacity to dissipate excess light energy, absorbed by the chlorophylls, as heat without intrathylakoid acidification. The increased heat dissipation helps protect the chlorophylls from photo-oxidative bleaching and thereby facilitates rapid recovery of photosynthesis in spring.U nder favorable light and temperatures, most plants operate with a high quantum efficiency (better than 80%) to use absorbed photons to catalyze photosynthetic electron transport, ATP synthesis, and carbon fixation. However, photosynthetic efficiency in leaves of evergreens such as holly (1), pines (2, 3), and snow gum (4, 5), naturally declines to very low levels during winter and remains inhibited until conditions become favorable for growth in spring. These evergreen species maintain significant levels of chlorophyll (Chl), which exists in a state that has not been characterized previously with respect to the Chl electronic-excited state or fluorescence lifetimes, or the Chl excitation vs. emission spectra of photosystems I and II (PSI and PSII). This characterization is essential for understanding mechanisms of Chl protection and storage in overwintering evergreens.We report that winter acclimation of the photosynthetic apparatus in the snow gum Eucalyptus pauciflora Sieb. ex Spreng results in a large loss of Chl in the leaf and profound changes in the Chl a fluorescence emission spectrum at 77 K in the form of a broad emission maximum featured in the 715-nm region. Concomitantly there is a significant increase in the amplitudes of room temperature PSII Chl a fluorescence emission components with subnanosecond fluorescence lifetimes. The subnanosecond lifetime components indicate a more rapid rate of thermal excitation dissipation compared to the main 2.5-ns components (6) that typify the deacclimated state. Although the spectral and kinetic changes during winter acclimation are induced by excess light and chloroplast intrathylakoid acidification (6, 7), the slowly reversing changes during deacclimation are sustained largely independently of intrathylakoid acidification. The enhanced thermal dissipation during winter acclimation correlates with a massive build-up of the same xanthophyll cycle pigments (8) that are most widely known to correlate with PSII thermal dissipation when there is intrathylakoid acidification (6,7,(9)(10)(11)(12). The primary steps of winter deacclimation correlate with a slow, stoichiometric conversi...

A Mechanism of Nonphotochemical Energy Dissipation, Independent from PsbS, Revealed by a Conformational Change in the Antenna Protein CP26

“…These characteristics are similar to those found in long term overwinter quenching (Verhoeven et al, 1999;Gilmore and Ball, 2000). Previous results demonstrated the existence of a form of sustained (Z þ A)-dependent energy dissipation, detected in cold-acclimated leaves and retained even upon warming; this mechanism is correlated with slow Z þ A to violaxanthin conversion and is not associated to nocturnal maintenance of low lumenal pH (Verhoeven et al, 1998).…”

“…Both types of quenching have been proposed to imply conformational changes in LHC proteins (Gilmore and Ball, 2000;Horton et al, 2000). Our data show that such a conformational change actually occurs in the case of dark-resistant, pH-independent quenching.…”

“…Genetic analysis has identified PsbS as a gene product indispensable for qE, while zeaxanthin and lutein appear as modulators of qE amplitude Pogson et al, 1998). Zeaxanthin accumulation also has been involved in long term (overwinter) downregulation of photosynthesis (Verhoeven et al, 1999;Gilmore and Ball, 2000). Current understanding of energy dissipation suggests that PsbS catalyzes qE upon protonation of lumenal-exposed residues (Li et al, 2002b) and binding of zeaxanthin.…”

Increased Air Temperature during Simulated Autumn Conditions Does Not Increase Photosynthetic Carbon Gain But Affects the Dissipation of Excess Energy in Seedlings of the Evergreen Conifer Jack Pine

“…2C). Previous work also showed that a higher amount of aggregated LHCs is associated with improved photoprotection in overwintering evergreens and other plants (Horton et al, 1991;Ruban et al, 1993;Ottander et al, 1995;Gilmore and Ball, 2000;Krol et al, 2002). Reorganization of pigment-protein complexes, which is indicated by an increased aggregation state of LHCII, was observed in all but the LD/HT control treatment (Fig.…”

“…In evergreen conifers, this q I is also associated with the termination of growth and induction of frost hardiness . In this q I state, a reorganization of the photosynthetic apparatus may protect conifer needles by dissipating excess energy as heat independent of a pH gradient (Gilmore and Ball, 2000;Ensminger et al, 2006). Overwintering evergreen conifers seem to be able to shift between the dynamic and the sustained antenna quenching (q O ) modes for dissipating excess energy .…”