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 [CO 2 ] have been widely studied as a potential driver of plant evolution; however, the role of a fluctuating [O 2 ]:[CO 2 ] 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 % [O 2 ]-1900 ppm [CO 2 ] and ambient conditions of 21 % [O 2 ]-400 ppm [CO 2 ], 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 ( V Cmax ) and the maximum electron flow supporting ribulose-1,5-bisphosphate regeneration ( J max ) in all species, yet this downregulation had little effect on their light-saturated photosynthetic rate ( A sat ). Ginkgo was found to photorespire heavily under ambient conditions, while growth in low [O 2 ]:[CO 2 ] resulted in increased heat dissipation per reaction centre ( DI o / RC ), severe photodamage, as revealed by the species' decreased maximum efficiency of primary photochemistry ( F v / F m ) 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 C 3 and the diminished C 2 cycles under low [O 2 ]:[CO 2 ]. 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 [CO 2 ] increased to maximum levels across the TJB.

Keywords: Ginkgo biloba; Triassic–Jurassic boundary; angiosperms; gymnosperms; high CO2; low O2; mesophyll conductance; monilophytes; photodamage; photorespiration; photosynthetic plasticity; stomatal conductance.

Fig. 1.

Light-saturated photosynthesis (A_sat) of the test species under ambient (400 ppm CO₂, 21 % O₂) and TJB (1900 ppm CO₂, 16 % O₂) atmospheric conditions (leaf temperature = 20 ºC). n = 3–4 depending on the species. The error bars denote 1 s.d. Asterisks indicate statistically significant differences between treatments for each species (P ≤ 0·05).

Fig. 2.

(A) Operational chloroplastic CO₂ concentrations (C_c) of the test species under ambient atmospheric conditions (400 ppm CO₂, 21 % O₂). Data are means ± s.d. from 3–4 measurements. Different letters denote statistically significant differences (P ≤ 0·05) between species. (B) Mesophyll conductance (g_m), stomatal conductance at saturating light intensity (g_s) and total conductance [g_t = (g_m × g_s)/(g_m + g_s)] of the test species under ambient atmospheric conditions (400 ppm. CO₂, 21 % O₂). n = 3–4 depending on species. The error bars denote 1 s.d. Different letters for each parameter denote statistically significant differences (P ≤ 0·05) between species.

Fig. 3.

(A) Relationship (y = 7·35x – 1·03, r² = 0·82, P = 0·033) between the observed changes in the combined in situ oxygenation/carboxylation rate (DV_C + V_O) and the corresponding changes of the in situ electron transport rate supporting RuBP regeneration (DJ_situ). Data are differences resulting after subtraction of the mean values of the ambient treatment (400 ppm CO₂, 21 % O₂) from the corresponding values of the TJB (1900 ppm CO₂, 16 % O₂) treatment, (B) Relationship (y = 16·15x + 8·98, r² = 0·95, P = 0·005) between the observed changes in the in situ oxygenation rate (DV_O) and the corresponding changes in the in situ electron transport rate supporting RuBP regeneration (DJ_situ). Data are differences resulting after subtraction of the mean values of the ambient treatment (400 ppm CO₂, 21 % O₂) from the corresponding values of the TJB (1900 ppm CO₂, 16 % O₂) treatment.

Fig. 4.

Relationship (y = 244x + 192, r² = 0·95, P = 0·003) between the relative observed changes in the in situ oxygenation rate [Rel. DV_O  = (V_Oamb – V_OTJB)/V_Oamb] and the corresponding changes in the maximum rate of carboxylation (DV_Cmax). DV_Cmax data are differences resulting after subtraction of the mean values of the ambient treatment (400 ppm CO₂, 21 % O₂) from the corresponding values of the TJB (1900 ppm CO₂, 16 % O₂) treatment.

Fig. 5.

(A) Normalized (relative to ambient values) values of maximum efficiency of primary photochemistry (Normalized F_v/F_m) and (B) normalized values of heat dissipation per reaction centre (Normalized DI_o/RC) of the test species under ambient (400 ppm CO₂, 21 % O₂, black outline) and TJB (1900 ppm CO₂, 16 % O₂, grey outline) atmospheric conditions. In both (A) and (B) the box signifies the distribution of the 25–75 % quartiles, the median and average are represented by a vertical line and an open square within the box, respectively, and the whiskers indicate the s.d. Outliers are represented by filled circles. n = 10–18 depending on species. Coloured boxes denote within-species significant differences relative to ambient treatment values (P ≤ 0·05).

Fig. 6.

(A) Relationship (y = 0·0028x – 0·0047, r² = 0·91, P = 0·011) between the observed changes in the maximum efficiency of primary photochemistry (DF_v/F_m) and the corresponding changes of in situ electron transport rate supporting RuBP regeneration (DJ_situ). Data are differences resulting after subtraction of the mean values of the ambient treatment (400 ppm. CO₂, 21 % O₂) from the corresponding values of the TJB (1900 ppm CO₂, 16 % O₂) treatment. (B) Relationship (y = 0·048x + 0·026, r² = 0·96, P = 0·004) between the observed changes in the maximum efficiency of primary photochemistry (DF_v/F_m) and the corresponding changes of the in situ oxygenation rate (DV_O). Data are differences resulting after subtraction of the mean values of the ambient treatment (400 ppm CO₂, 21 % O₂) from the corresponding values of the TJB (1900 ppm CO₂, 16 % O₂) treatment.

Fig. 7.

Schematic model depicting the changes in the energy flows of Ginkgo and ferns when acclimated to TJB atmospheric conditions. The thickness of the arrows is representative of the relative magnitude, and the flows that change under low [O₂]:[CO₂] are outlined with red colour. LHC, light-harvesting complex, E_ABS, absorbed energy; Q, heat dissipation; J, photosynthetic electron flow; J_O, photosynthetic electron flow supporting photorespiratory metabolism; J_C, photosynthetic electron supporting photosynthesis; DI_o/RC, heat dissipation per reaction centre, F_v/F_m, maximum efficiency of primary photochemistry.