Novel adaptation to deep shade environments in basal vascular plants: Bizonoplasts of Selaginella

Background/Question/Methods

Low light conditions can be extremely challenging to autotrophic organisms. Some members of the ancient plant genus Selaginella have found a novel solution to extremely low light conditions in chloroplast structure and associated leaf anatomy, potentially allow them to thrive despite strong shade from other plants. Chloroplast morphology and ultrastructure varies very little among vascular plant species, but recently, the deep shade Lycophyte S. erythropus was found to have highly modified chloroplasts among numerous anatomical features enhancing light capture. This unique chloroplast (termed a bizonoplast) has unusual ultrastructure, with an upper zone of parallel layers of 2-4 stacked thylakoid membranes, although the lower zone contains both the stromal thylakoids and grana structure general to the entire chloroplast of most land plants. The bizonoplast is extremely large (20 μm) and cup-shaped with individual bizonoplasts filling much of the large funnel-shaped dorsal epidermal cells in this species. Given very little study of chloroplast diversity in Selaginella, we surveyed local 12 species of Selaginella native to Taiwan and one desert species, S. arizonica, native to USA to see if bizonoplasts are found in other species and are consistently associated with deep shade. General light, electron, and confocal microscopy were used in this study.

Results/Conclusions

Selaginella heterostachys is here reported as the second species of vascular plant with bizonoplasts. It occurs densely shaded by other plants (PAR 4–39 μmol/m²s at mid-day: 0.2-0.3% full sun) in moderately damp rocky habitat with shallow soil layers. The bizonoplast found in S. heterostachys is similar to that of S. erythropus in ultrastructure. However, the bizonoplasts of S. heterostachys have a different shape and are similar to a catcher’s mitt (for photons instead of balls), with a lobed structure, which we conjecture is flexible, changing form to the prevailing light conditions. Selaginella heterostachys and S. erythropus belong to different subgenera of Selaginella suggesting the potential for this chloroplast to be found generally in this genus when environmental conditions are right. Giant chloroplasts were commonly found in deep shade Selaginella, but of the 13 species in this study, only S. heterostachys has bizonoplasts. Thus, environmental prerequisites for bizonoplasts could not be fully characterized. Functional trait analysis is current a major thrust in plant ecology, but with very different traits from those considered here, and very different taxa. When wider taxonomic diversity is considered, rather different traits, including chloroplast traits, may be needed.