Differences in the photosynthetic plasticity of ferns and Ginkgo grown in experimentally controlled low [O2]:[CO2] atmospheres may explain their contrasting ecological fate across the Triassic-Jurassic mass extinction boundary

Abstract

Background and Aims Fluctuations in [CO2] have been widely studied as a potential driver of plant evolution; however, the role of a fluctuating [O2]:[CO2] ratio is often overlooked. The present study aimed to investigate the inherent physiological plasticity of early diverging, extant species following acclimation to an atmosphere similar to that across the Triassic-Jurassic mass extinction interval (TJB, approx. 200 Mya), a time of major ecological change. Methods Mature plants from two angiosperm (Drimys winteri and Chloranthus oldhamii), two monilophyte (Osmunda claytoniana and Cyathea australis) and one gymnosperm (Ginkgo biloba) species were grown for 2 months in replicated walk-in Conviron BDW40 chambers running at TJB treatment conditions of 16 % [O2]- 1900 ppm [CO2] and ambient conditions of 21 % [O2]-400 ppm [CO2], and their physiological plasticity was assessed using gas exchange and chlorophyll fluorescence methods. Key Results TJB acclimation caused significant reductions in the maximum rate of carboxylation (VCmax) and the maximum electron flow supporting ribulose-1,5-bisphosphate regeneration (Jmax) in all species, yet this downregulation had little effect on their light-saturated photosynthetic rate (Asat). Ginkgo was found to photorespire heavily under ambient conditions, while growth in low [O2]:[CO2] resulted in increased heat dissipation per reaction centre (DIo/RC), severe photodamage, as revealed by the species' decreased maximum efficiency of primary photochemistry (Fv/Fm) and decreased in situ photosynthetic electron flow (Jsitu). Conclusions It is argued that the observed photodamage reflects the inability of Ginkgo to divert excess photosynthetic electron flow to sinks other than the downregulated C3 and the diminished C2 cycles under low [O2]:[CO2]. This finding, coupled with the remarkable physiological plasticity of the ferns, provides insights into the underlying mechanism of Ginkgoales' near extinction and ferns' proliferation as atmospheric [CO2] increased to maximum levels across the TJB.