Activation of photoprotective winter photoinhibition in plants from different environments: a literature compilation and meta‐analysis

Abstract

Overwintering plants face a pronounced imbalance between light capture and use of that excitation for photosynthesis. In response, plants upregulate thermal dissipation, with concomitant reductions in photochemical efficiency, in a process characterized by a slow recovery upon warming. These sustained depressions of photochemical efficiency are termed winter photoinhibition (WPI) here. WPI has been extensively studied in conifers and in few overwintering crops, but other plant species have received less attention. Furthermore, the literature shows some controversies about the association of WPI with xanthophylls and the environmental conditions that control xanthophylls conversion. To overview current knowledge and identify knowledge gaps on WPI mechanisms, we performed a comprehensive meta-analysis of literature published over the period 1991-2011. All publications containing measurements of Fv/Fm for a cold period and a corresponding warm control were included in our final database of 190 studies on 162 species. WPI was estimated as the relative decrease in Fv/Fm. High WPI was always accompanied by a high (A + Z)/(V + A + Z). Activation of lasting WPI was directly related to air temperature, with a threshold of around 0°C. Tropical plants presented earlier (at a temperature of >0°C) and higher WPI than non-tropical plants. We conclude that (1) activation of a xanthophyll-dependent mechanism of WPI is a requisite for maintaining photosynthetic structures at sub-zero temperatures, while (2) absence (or low levels) of WPI is not necessarily related to low (A + Z)/(V + A + Z); and (3) the air temperature that triggers lasting WPI, and the maximum level of WPI, do not depend on plant growth habit or bioclimatic origin of species.

Xanthophyll Cycle Activity in Two Prominent Arctic Shrub Species

“…Although it is difficult to compare xanthophyll interconversion rates among studies, our (Z+A) dark-retention data (Figs. 3 and 4) from arctic species are in line with similarly collected data from species growing in harsh environments as reported in the meta-analysis by Miguez et al (2015, and their Fig. 2, part b).…”

“…The majority of field-based studies has been conducted in temperate, semi-arid, and Mediterranean climates, with only limited investigations conducted in the end-members of our global climate system, such as tropical rainforest (Königer et al, 1995;Matsubara et al, 2009;Krause et al, 2012);desert (Barker and Adams, 1997;Barker et al, 2002); boreal forest (Ensminger et al, 2004;Yamazaki et al, 2007;Porcar-Castell et al, 2008; or tundra (this study). Indeed, three recent meta-analyses suggest that total xanthophyll pools and the relative concentration of zeaxanthin are clear indicators of the response of plants to harsh growing conditions or environmental stress (Wujeska et al, 2013;Esteban et al, 2015;Miguez et al, 2015), but these studies lack data reported in more extreme environments, particularly at high latitudes and the tundra biome.…”

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

“…Under severe stress conditions, specially low temperature, the VAZ cycle does not reach a complete relaxation (Demmig-Adams and Adams, 1996; Demmig-Adams et al, 2006), and AZ/VAZ is typically higher than 0.5 before dawn (Míguez et al, 2015). This process has been characterized in detail in boreal conifers and alpine evergreens (Verhoeven, 2014; Míguez et al, 2017) involving profound change in the organization of photosynthetic apparatus.…”

Enhanced thylakoid photoprotection can increase yield and canopy radiation use efficiency in rice

“…PsbS-dependent qE can be generated within seconds but the synthesis of zeaxanthin and its reconversion back to violaxanthin in low-light occurs on a timescale of minutes 22–24 leading to the suggestion that zeaxanthin persistence is a ‘memory’ of high-light events, enabling a rapid response to a re-occurrence of saturating light 2 . Slower-relaxing components of NPQ include qI or inhibitory quenching which can be formed as a result of damage to PSII and its repair which is a process requiring time, energy and protein synthesis 25,26 or from the more persistent retention of zeaxanthin 27 .…”