To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms

Abstract

A comparative study has been made of the photosynthetic physiological ecology and carbon isotope discrimination characteristics for modern-day bryophytes and closely related algal groups. Firstly, the extent of bryophyte distribution and diversification as compared with more advanced land plant groups is considered. Secondly, measurements of instantaneous carbon isotope discrimination (D), photosynthetic CO 2 assimilation and electron transport rates were compared during the drying cycles. The extent of surface diffusion limitation (when wetted), internal conductance and water use efficiency (WUE) at optimal tissue water content (TWC) were derived for liverworts and a hornwort from contrasting habitats and with differing degrees of thallus ventilation (as intra-thalline cavities and internal airspaces). We also explore how the operation of a biophysical carbon-concentrating mechanism (CCM) tempers isotope discrimination characteristics in two other hornworts, as well as the green algae Coleochaete orbicularis and Chlamydomonas reinhardtii. The magnitude of D was compared for each life form over a drying curve and used to derive the surface liquid-phase conductance (when wetted) and internal conductance (at optimal TWC). The magnitude of external and internal conductances, and WUE, was higher for ventilated, compared with non-ventilated, liverworts and hornworts, but the values were similar within each group, suggesting that both factors have been optimized for each life form. For the hornworts, leakiness of the CCM was highest for Megaceros vincentianus and C. orbicularis (approx. 30%) and, at 5%, lowest in C. reinhardtii grown under ambient CO 2 concentrations. Finally, evidence for the operation of a CCM in algae and hornworts is considered in terms of the probable role of the chloroplast pyrenoid, as the origins, structure and function of this enigmatic organelle are explored during the evolution of land plants.

Functional Hybrid Rubisco Enzymes with Plant Small Subunits and Algal Large Subunits

“…This phenotype appears to result from the loss of the chloroplast pyrenoid (Fig. 5), which is associated with the algal CCM (10,11,78,79). The mutants grow better in air than other Chlamydomonas CCM mutants (74,75), perhaps indicating that some components of the CCM are still functional but Rubisco is in a CO 2 -limited environment.…”

Bryophyte gas‐exchange dynamics along varying hydration status reveal a significant carbonyl sulphide (COS) sink in the dark and COS source in the light

“…The mat‐forming liverwort Marchantia polymorpha L. has gametophytes with a complex thallus structure and occasional static pores to improve ventilation (Meyer et al ., 2008). The loosely packed weft‐moss Scleropodium purum (Hedw.)…”

Rubisco small-subunit α-helices control pyrenoid formation inChlamydomonas

“…For physiological analysis, cells were grown as described in ref. 27. Plasmids and Host Transformation.…”

“…Discrimination against the stable carbon isotope (Δ 13 C) was measured using a mass spectrometer, downstream of an open gas cuvettete system, after cold trapping of air passing over photosynthetic active Chlamydomonas, into a vacuum line and water vapor scrubbing, as described previously (27). Leakage was calculated from Δ 13 C, fractionation during carboxylation (27‰), discrimination during dissolution of CO 2 (1.1‰), and liquid phase diffusion (0.7‰), using the authors' model (27).…”

“…The activity of a CCM in wild type and helix AB was confirmed by measuring real-time carbon isotope discrimination (Δ 13 C). This measure was used to derive the extent of CCM efficiency or leakage (26,27), which is low (typically <10%) for a fully functional CCM in Chlamydomonas and high (theoretically up to 100%) for photosynthesis reliant solely on CO 2 diffusion. The helix AB transformants, with their restored pyrenoid, …”