A variation on chloroplast development: the bizonoplast and photosynthetic efficiency in the deep-shade plant Selaginella erythropus

Chiou Rong Sheue, Jian Wei Liu, Jia Fang Ho, Ai Wen Yao, Yeh Hua Wu, Sauren Das, Chi Chu Tsai, Hsiu An Chu, Maurice S B Ku, Peter Chesson

Research output: Contribution to journalArticle

8 Citations (Scopus)

Abstract

PREMISE OF THE STUDY: Chloroplast development and structure are highly conserved in vascular plants, but the bizonoplast of Selaginella is a notable exception. In the shade plant S. erythropus, each dorsal epidermal cell contains one bizonoplast, while other cells have normal chloroplasts. Our quest was to (1) determine the origin of bizonoplasts, (2) explore developmental plasticity, and (3) correlate developmental changes with photosynthetic activity to provide insights unavailable in other green plants with more constrained development.•

METHODS: Bizonoplast development was studied in juvenile prostrate and older erect shoots of S. erythropus. Plastid plasticity was studied in plants cultivated under different light conditions. Chlorophyll fluorescence was measured and correlated with photosynthetic activity.•

KEY RESULTS: The bizonoplast originates from a proplastid, forming a distinctive upper zone rapidly after exposure to low light. In the prostrate shoots, the proplastid develops through early stages only. When the shoot becomes erect, the proplastid soon develops into a mature bizonoplast. Erect shoots have significantly higher photosynthetic efficiency than prostrate shoots. No bizonoplasts were found in the plants growing in high light, where 2-4 spheroidal chloroplasts formed, or with light from below.•

CONCLUSIONS: The upper zone develops above a normal-looking chloroplast structure to produce a bizonoplast. Bizonoplast developmental plasticity suggests that regular lamellar structure and monoplastidy are adaptations to deep shade environments. Such novel variation in S. erythropus is in stark contrast to known plastid development in other vascular plants, possibly reflecting retention of developmental flexibility in the basal clade, Lycophyta, to which it belongs.

Original languageEnglish (US)
Pages (from-to)500-511
Number of pages12
JournalAmerican Journal of Botany
Volume102
Issue number4
DOIs
StatePublished - Apr 1 2015

Fingerprint

Selaginellaceae
Chloroplasts
chloroplast
shade
chloroplasts
shoot
shoots
plasticity
Light
Plastids
plastid
vascular plant
vascular plants
plastids
Blood Vessels
Viridiplantae
Selaginella
Chlorophyll
chlorophyll
fluorescence

Keywords

  • cup-shaped
  • erect shoot
  • microphyll
  • monoplastidy
  • photosynthesis
  • plasticity
  • plastid
  • Selaginellaceae
  • ultrastructure
  • upper zone

ASJC Scopus subject areas

  • Medicine(all)

Cite this

A variation on chloroplast development : the bizonoplast and photosynthetic efficiency in the deep-shade plant Selaginella erythropus. / Sheue, Chiou Rong; Liu, Jian Wei; Ho, Jia Fang; Yao, Ai Wen; Wu, Yeh Hua; Das, Sauren; Tsai, Chi Chu; Chu, Hsiu An; Ku, Maurice S B; Chesson, Peter.

In: American Journal of Botany, Vol. 102, No. 4, 01.04.2015, p. 500-511.

Research output: Contribution to journalArticle

Sheue, Chiou Rong ; Liu, Jian Wei ; Ho, Jia Fang ; Yao, Ai Wen ; Wu, Yeh Hua ; Das, Sauren ; Tsai, Chi Chu ; Chu, Hsiu An ; Ku, Maurice S B ; Chesson, Peter. / A variation on chloroplast development : the bizonoplast and photosynthetic efficiency in the deep-shade plant Selaginella erythropus. In: American Journal of Botany. 2015 ; Vol. 102, No. 4. pp. 500-511.
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abstract = "PREMISE OF THE STUDY: Chloroplast development and structure are highly conserved in vascular plants, but the bizonoplast of Selaginella is a notable exception. In the shade plant S. erythropus, each dorsal epidermal cell contains one bizonoplast, while other cells have normal chloroplasts. Our quest was to (1) determine the origin of bizonoplasts, (2) explore developmental plasticity, and (3) correlate developmental changes with photosynthetic activity to provide insights unavailable in other green plants with more constrained development.•METHODS: Bizonoplast development was studied in juvenile prostrate and older erect shoots of S. erythropus. Plastid plasticity was studied in plants cultivated under different light conditions. Chlorophyll fluorescence was measured and correlated with photosynthetic activity.•KEY RESULTS: The bizonoplast originates from a proplastid, forming a distinctive upper zone rapidly after exposure to low light. In the prostrate shoots, the proplastid develops through early stages only. When the shoot becomes erect, the proplastid soon develops into a mature bizonoplast. Erect shoots have significantly higher photosynthetic efficiency than prostrate shoots. No bizonoplasts were found in the plants growing in high light, where 2-4 spheroidal chloroplasts formed, or with light from below.•CONCLUSIONS: The upper zone develops above a normal-looking chloroplast structure to produce a bizonoplast. Bizonoplast developmental plasticity suggests that regular lamellar structure and monoplastidy are adaptations to deep shade environments. Such novel variation in S. erythropus is in stark contrast to known plastid development in other vascular plants, possibly reflecting retention of developmental flexibility in the basal clade, Lycophyta, to which it belongs.",
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author = "Sheue, {Chiou Rong} and Liu, {Jian Wei} and Ho, {Jia Fang} and Yao, {Ai Wen} and Wu, {Yeh Hua} and Sauren Das and Tsai, {Chi Chu} and Chu, {Hsiu An} and Ku, {Maurice S B} and Peter Chesson",
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AU - Sheue, Chiou Rong

AU - Liu, Jian Wei

AU - Ho, Jia Fang

AU - Yao, Ai Wen

AU - Wu, Yeh Hua

AU - Das, Sauren

AU - Tsai, Chi Chu

AU - Chu, Hsiu An

AU - Ku, Maurice S B

AU - Chesson, Peter

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N2 - PREMISE OF THE STUDY: Chloroplast development and structure are highly conserved in vascular plants, but the bizonoplast of Selaginella is a notable exception. In the shade plant S. erythropus, each dorsal epidermal cell contains one bizonoplast, while other cells have normal chloroplasts. Our quest was to (1) determine the origin of bizonoplasts, (2) explore developmental plasticity, and (3) correlate developmental changes with photosynthetic activity to provide insights unavailable in other green plants with more constrained development.•METHODS: Bizonoplast development was studied in juvenile prostrate and older erect shoots of S. erythropus. Plastid plasticity was studied in plants cultivated under different light conditions. Chlorophyll fluorescence was measured and correlated with photosynthetic activity.•KEY RESULTS: The bizonoplast originates from a proplastid, forming a distinctive upper zone rapidly after exposure to low light. In the prostrate shoots, the proplastid develops through early stages only. When the shoot becomes erect, the proplastid soon develops into a mature bizonoplast. Erect shoots have significantly higher photosynthetic efficiency than prostrate shoots. No bizonoplasts were found in the plants growing in high light, where 2-4 spheroidal chloroplasts formed, or with light from below.•CONCLUSIONS: The upper zone develops above a normal-looking chloroplast structure to produce a bizonoplast. Bizonoplast developmental plasticity suggests that regular lamellar structure and monoplastidy are adaptations to deep shade environments. Such novel variation in S. erythropus is in stark contrast to known plastid development in other vascular plants, possibly reflecting retention of developmental flexibility in the basal clade, Lycophyta, to which it belongs.

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