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

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

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Pages (from-to)562-576
Number of pages15
JournalAmerican journal of botany
Volume107
Issue number4
DOIs
StatePublished - Apr 1 2020

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Keywords

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

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Plant Science

Cite this

Liu, J. W., Li, S. F., Wu, C. T., Valdespino, I. A., Ho, J. F., Wu, Y. H., Chang, H. M., Guu, T. Y., Kao, M. F., Chesson, C., Das, S., Oppenheimer, H., Bakutis, A., Saenger, P., Salazar Allen, N., Yong, J. W. H., Adjie, B., Kiew, R., Nadkarni, N., ... Sheue, C. R. (2020). Gigantic chloroplasts, including bizonoplasts, are common in shade-adapted species of the ancient vascular plant family Selaginellaceae. American journal of botany, 107(4), 562-576. https://doi.org/10.1002/ajb2.1455