Adaptation to deep shade environments: Novel biophysical and biochemical properties of bizonoplasts, unique epidermal chloroplasts of two Selaginella species

Background/Question/Methods

Bizonoplasts are unique giant chloroplasts with dimorphic ultrastructure located in the dorsal epidermal cells of leaves of shade-adapted Selaginella erythropus and S. heterostachys. This chloroplast is characterized by two zones: an upper zone occupied by parallel layers of 2–4 stacked thylakoid membranes and a lower zone containing both unstacked stromal thylakoids and grana structure, similar to the common chloroplasts of land plants. In these two deep-shade Selaginella, the enlargement of the dorsal epidermal cells into funnel-shaped, photosynthetic cells coupled with specific localization of a large bizonoplast in the lower part of the cell are clear adaptive modifications to deep shade. To understand the functional differentiation between the upper and lower zones of a bizonoplast, chloroplasts were sampled from the ventral microphylls of S. erythropus and S. heterostachys and quantitative immunogold labeling was performed for four key photosynthetic proteins, psaA of photosystem I (PSI), psbA of photosystem II (PSII), RbcL of rubisco and AtpA of ATPase. In addition, a computer simulation of the optical features of the upper zone was conducted to explore the ecophysiological implications of this unique structure

Results/Conclusions

Our results show that the four key photosynthetic proteins occur in both the upper and lower zones of a bizonoplast. However, the upper zone is significantly enriched in PSI, while the lower zone is significantly enriched in PSII and rubisco, with ATPase evenly distributed between the two zones. The simulation indicates that the layered structure of the upper zone causes reflection of green light but permits transmission or absorption of most photosynthetic active radiation (PAR). Based on these results, it is clear that the dimorphic ultrastructure of a bizonoplast has differential physiological functions in a single plastid: the large concave upper zone with layers of parallel and horizontally extended 2–4 stacked thylakoid membranes may facilitate photon capture and increase the effective light capturing area. Moreover, the PSI enriched upper zone should facilitate capture of far red light, which is enriched in low light environments, while the lower zone, filled with numerous grana with higher ratio of PSII and rubisco, should aid absorption of infrared light and starch synthesis. Finally, the funnel-shaped dorsal epidermal cells surrounded by intercellular space will assist reflection of transmitted PAR back to the upper zone of the bizonoplast and thus maximize light absorption.