Abstract
Low temperature in winter depresses rates of photosynthesis, which, in evergreen plants, can exacerbate imbalances between light absorption and photochemical light use. Damage that could result from increased excess light absorption is minimized by the conversion of excitation energy to heat in a process known as energy dissipation, which involves the de-epoxidized carotenoids of the xanthophyll cycle. Overwintering evergreens employ sustained forms of energy dissipation observable even after lengthy periods of dark acclimation. Whereas most studies of photoprotective energy dissipation examine one or a small number of species; here, we measured the levels of sustained thermal energy dissipation of seventy conifer taxa growing outdoors under common-garden conditions at the Red Butte Garden in Salt Lake City, Utah, U.S.A. (forty nine taxa were also sampled for needle pigment content). We observed an extremely wide range of wintertime engagement of sustained energy dissipation; the percentage decrease in dark-acclimated photosystem II quantum efficiency from summer to winter ranged from 6 to 95%. Of the many pigment-based parameters measured, the magnitude of the seasonal decrease in quantum efficiency was most closely associated with the seasonal increase in zeaxanthin content expressed on a total chlorophyll basis, which explained only slightly more than one-third of the variation. We did not find evidence for a consistent wintertime decrease in needle chlorophyll content. Thus, the prevailing mechanism for winter decreases in solar-induced fluorescence emitted by evergreen forests may be decreases in fluorescence quantum yield, and wintertime deployment of sustained energy dissipation likely underlies this effect.
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Study data available via the Bowdoin Digital Commons.
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Acknowledgements
David Bowling and Barry Logan wish Russell Monson well on the occasion of his retirement and thank him for many years of mentoring, support and friendship. We thank Jason Baker and Marita Tewes at Red Butte Garden for permission to work in the garden and for logistical support.
Funding
This study was supported by the U. S. National Science Foundation Macrosystems and NEON-Enable Science Program (awards 1926090 and 1925992) and Division of Undergraduate Education (award 0088517). AW-M and DMB received travel support from the Grua-O’Connell Fund (Bowdoin College).
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DRB conceived of the study, which he designed with BAL. AW-M, MAG, DB, and AL performed chlorophyll fluorescence analyses. AW-M, DB, JSR and ES characterized needle chlorophyll and carotenoid composition. AW-M and CS led statistical analyses. AW-M conceived of and created figures. AW-M wrote the manuscript; all other authors provided editorial advice.
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Communicated by Kaoru Kitajima.
In this first-of-its-kind common-garden study, we report astonishing variation among seventy conifer taxa in their winter engagement of sustained energy dissipation, a key photoprotective mechanism.
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442_2021_5038_MOESM2_ESM.tiff
Supplementary file2 Temperature throughout period of winter measurement. Blue bars represent minimum and maximum temperature in 2019. Shown in gray bars are minimum and maximum temperature normals from 1981-2010. Days of measurement indicated by darker blue bars (TIFF 122510 KB)
442_2021_5038_MOESM3_ESM.tiff
Supplementary file3 Correlation matrix of parameters. Only relationships with p < 0.05 are represented with circles. Color denotes r2 as indicated, as does circle size. Abbreviations: A antheraxanthin; chl a chlorophyll a; chl b chlorophyll b; L lutein; N neoxanthin; PSII 200 and PSII 1600 photosystem II efficiency at 200 and 1600 µmol m-2 s-1, respectively; Z zeaxanthin. Pigment contents are on a needle fresh mass basis or, where indicated, on a total chlorophyll basis. n = 49 (pigment parameters) or 70 (parameters derived from chlorophyll fluorescence analysis) (TIFF 122510 KB)
442_2021_5038_MOESM4_ESM.tiff
Supplementary file4 Summer (pink) and winter (blue) needle pigment compositions on a fresh mass basis for individual taxa (genotype code [WT wildtype, C cultivar, D dwarf cultivar] and USDA numerical hardiness rating included). Abbreviations: A antheraxanthin; BC beta-carotene; chl a chlorophyll a; chl b chlorophyll b; L lutein; N neoxanthin; Z zeaxanthin. n = 49 (TIFF 134418 KB)
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Walter-McNeill, A., Garcia, M.A., Logan, B.A. et al. Wide variation of winter-induced sustained thermal energy dissipation in conifers: a common-garden study. Oecologia 197, 589–598 (2021). https://doi.org/10.1007/s00442-021-05038-y
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DOI: https://doi.org/10.1007/s00442-021-05038-y