Jian-Wei Liu1, Shau-Fu Li1, Chin-Ting Wu2, Iván A Valdespino3, Jia-Fang Ho1,2, Yeh-Hua Wu1,2, Ho-Ming Chang4, Te-Yu Guu1, Mei-Fang Kao5, Clive Chesson6, Sauren Das7, Hank Oppenheimer8, Ane Bakutis9, Peter Saenger10, Noris Salazar Allen11, Jean W H Yong12, Bayu Adjie13, Ruth Kiew14, Nalini Nadkarni15, Chun-Lin Huang16, Peter Chesson1,17, Chiou-Rong Sheue1,17. 1. Department of Life Sciences & Research Center for Global Change Biology, National Chung Hsing University, Taichung, Taiwan. 2. Department of Biological Resources, National Chiayi University, Chiayi, Taiwan. 3. Departamento de Botánica, Facultad de Ciencias Naturales, Exactas y Tecnología, Universidad de Panamá; Sistema Nacional de Investigación (SNI), SENACYT, Panama, Panama. 4. Endemic Species Research Institute, Jiji Town, Taiwan. 5. TAI Herbarium, National Taiwan University, Taipei, Taiwan. 6. 6 Barker Way, Valley View, S.A., Australia. 7. Agricultural and Ecological Research Unit, Indian Statistical Institute, Kolkata, India. 8. Maui Nui Plant Extinction Prevention Program, Maui, USA. 9. Molokai Plant Extinction Prevention Program, Molokai, USA. 10. Centre for Coastal Management, Southern Cross University, Lismore, Australia. 11. Smithsonian Tropical Research Institute, Panama, Panama. 12. Department of Biosystems and Technology, Swedish University of Agricultural Sciences, Alnarp, Sweden. 13. Bali Botanic Garden, Indonesia. 14. Forest Research Institute Malaysia, Kepong, Malaysia. 15. Department of Biology, University of Utah, Salt Lake City, USA. 16. National Museum of Natural Science, Taichung, Taiwan. 17. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, USA.
Abstract
PREMISE: Unique among vascular plants, some species of Selaginella have single giant chloroplasts in their epidermal or upper mesophyll cells (monoplastidy, M), varying in structure between species. Structural variants include several forms of bizonoplast with unique dimorphic ultrastructure. Better understanding of these structural variants, their prevalence, environmental correlates and phylogenetic association, has the potential to shed new light on chloroplast biology unavailable from any other plant group. METHODS: The chloroplast ultrastructure of 76 Selaginella species was studied with various microscopic techniques. Environmental data for selected species and subgeneric relationships were compared against chloroplast traits. RESULTS: We delineated five chloroplast categories: ME (monoplastidy in a dorsal epidermal cell), MM (monoplastidy in a mesophyll cell), OL (oligoplastidy), Mu (multiplastidy, present in the most basal species), and RC (reduced or vestigial chloroplasts). Of 44 ME species, 11 have bizonoplasts, cup-shaped (concave upper zone) or bilobed (basal hinge, a new discovery), with upper zones of parallel thylakoid membranes varying subtly between species. Monoplastidy, found in 49 species, is strongly shade associated. Bizonoplasts are only known in deep-shade species (<2.1% full sunlight) of subgenus Stachygynandrum but in both the Old and New Worlds. CONCLUSIONS: Multiplastidic chloroplasts are most likely basal, implying that monoplastidy and bizonoplasts are derived traits, with monoplastidy evolving at least twice, potentially as an adaptation to low light. Although there is insufficient information to understand the adaptive significance of the numerous structural variants, they are unmatched in the vascular plants, suggesting unusual evolutionary flexibility in this ancient plant genus.
PREMISE: Unique among vascular plants, some species of Selaginella have single giant chloroplasts in their epidermal or upper mesophyll cells (monoplastidy, M), varying in structure between species. Structural variants include several forms of bizonoplast with unique dimorphic ultrastructure. Better understanding of these structural variants, their prevalence, environmental correlates and phylogenetic association, has the potential to shed new light on chloroplast biology unavailable from any other plant group. METHODS: The chloroplast ultrastructure of 76 Selaginella species was studied with various microscopic techniques. Environmental data for selected species and subgeneric relationships were compared against chloroplast traits. RESULTS: We delineated five chloroplast categories: ME (monoplastidy in a dorsal epidermal cell), MM (monoplastidy in a mesophyll cell), OL (oligoplastidy), Mu (multiplastidy, present in the most basal species), and RC (reduced or vestigial chloroplasts). Of 44 ME species, 11 have bizonoplasts, cup-shaped (concave upper zone) or bilobed (basal hinge, a new discovery), with upper zones of parallel thylakoid membranes varying subtly between species. Monoplastidy, found in 49 species, is strongly shade associated. Bizonoplasts are only known in deep-shade species (<2.1% full sunlight) of subgenus Stachygynandrum but in both the Old and New Worlds. CONCLUSIONS: Multiplastidic chloroplasts are most likely basal, implying that monoplastidy and bizonoplasts are derived traits, with monoplastidy evolving at least twice, potentially as an adaptation to low light. Although there is insufficient information to understand the adaptive significance of the numerous structural variants, they are unmatched in the vascular plants, suggesting unusual evolutionary flexibility in this ancient plant genus.
Authors: Eftychios Frangedakis; Masaki Shimamura; Juan Carlos Villarreal; Fay-Wei Li; Marta Tomaselli; Manuel Waller; Keiko Sakakibara; Karen S Renzaglia; Péter Szövényi Journal: New Phytol Date: 2020-09-15 Impact factor: 10.151