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Research article2020Peer reviewedOpen access

Gigantic chloroplasts, including bizonoplasts, are common in shade-adapted species of the ancient vascular plant family Selaginellaceae

Liu, Jian-Wei; Li, Shau-Fu; Wu, Chin-Ting; Valdespino, Ivan A.; Ho, Jia-Fang; Wu, Yeh-Hua; Chang, Ho-Ming; Guu, Te-Yu; Kao, Mei-Fang; Chesson, Clive; Das, Sauren; Oppenheimer, Hank; Bakutis, Ane; Saenger, Peter; Allen, Noris; Yong, Jean W. H.; Adjie, Bayu; Kiew, Ruth; Nadkarni, Nalini; Huang, Chun-Lin;
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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.

Keywords

bilobed chloroplast; chloroplast diversity; cup-shaped chloroplast; monoplastidy; shade-adapted Selaginella; Selaginellaceae; Stachygynandrum; ultrastructure

Published in

American Journal of Botany
2020, Volume: 107, number: 4, pages: 562-576

    UKÄ Subject classification

    Evolutionary Biology
    Botany
    Biological Systematics

    Publication identifier

    DOI: https://doi.org/10.1002/ajb2.1455

    Permanent link to this page (URI)

    https://res.slu.se/id/publ/103964