Leaf development in the single-cell C4 system in Bienertia sinuspersici: expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions

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Authors

  • María Valeria Lara
  • Sascha Offermann
  • Monica Smith
  • Thomas W Okita
  • Carlos Santiago Andreo
  • Gerald E Edwards

Research Organisations

External Research Organisations

  • Centro de Estudios Fotosintéticos y Bioquímicos
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Details

Original languageEnglish
Pages (from-to)593-610
Number of pages18
JournalPlant physiology
Volume148
Issue number1
Publication statusPublished - Sept 2008

Abstract

Bienertia sinuspersici performs C(4) photosynthesis in individual chlorenchyma cells by the development of two cytoplasmic domains (peripheral and central) with dimorphic chloroplasts, an arrangement that spatially separates the fixation of atmospheric CO(2) into C(4) acids and the donation of CO(2) from C(4) acids to Rubisco in the C(3) cycle. In association with the formation of these cytoplasmic domains during leaf maturation, developmental stages were analyzed for the expression of a number of photosynthetic genes, including Rubisco small and large subunits and key enzymes of the C(4) cycle. Early in development, Rubisco subunits and Gly decarboxylase and Ser hydroxymethyltransferase of the glycolate pathway accumulated more rapidly than enzymes associated with the C(4) cycle. The levels of pyruvate,Pi dikinase and phosphoenolpyruvate carboxylase were especially low until spatial cytoplasmic domains developed and leaves reached maturity, indicating a developmental transition toward C(4) photosynthesis. In most cases, there was a correlation between the accumulation of mRNA transcripts and the respective peptides, indicating at least partial control of the development of photosynthesis at the transcriptional level. During growth under moderate light, when branches containing mature leaves were enclosed in darkness for 1 month, spatial domains were maintained and there was high retention of a number of photosynthetic peptides, including Rubisco subunits and pyruvate,Pi dikinase, despite a reduction in transcript levels. When plants were transferred from moderate to low light conditions for 1 month, there was a striking shift of the central cytoplasmic compartment toward the periphery of chlorenchyma cells; the mature leaves showed strong acclimation with a shade-type photosynthetic response to light while retaining C(4) features indicative of low photorespiration. These results indicate a progressive development of C(4) photosynthesis with differences in the control mechanisms for the expression of photosynthetic genes and peptide synthesis during leaf maturation and in response to light conditions.

Keywords

    Carbon Dioxide/metabolism, Carbon Isotopes/metabolism, Chenopodiaceae/cytology, Chlorophyll/metabolism, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Light, Peptides/metabolism, Photosynthesis, Plant Leaves/cytology, Plant Proteins/metabolism, Water/metabolism

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Leaf development in the single-cell C4 system in Bienertia sinuspersici: expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions. / Lara, María Valeria; Offermann, Sascha; Smith, Monica et al.
In: Plant physiology, Vol. 148, No. 1, 09.2008, p. 593-610.

Research output: Contribution to journalArticleResearchpeer review

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title = "Leaf development in the single-cell C4 system in Bienertia sinuspersici: expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions",
abstract = "Bienertia sinuspersici performs C(4) photosynthesis in individual chlorenchyma cells by the development of two cytoplasmic domains (peripheral and central) with dimorphic chloroplasts, an arrangement that spatially separates the fixation of atmospheric CO(2) into C(4) acids and the donation of CO(2) from C(4) acids to Rubisco in the C(3) cycle. In association with the formation of these cytoplasmic domains during leaf maturation, developmental stages were analyzed for the expression of a number of photosynthetic genes, including Rubisco small and large subunits and key enzymes of the C(4) cycle. Early in development, Rubisco subunits and Gly decarboxylase and Ser hydroxymethyltransferase of the glycolate pathway accumulated more rapidly than enzymes associated with the C(4) cycle. The levels of pyruvate,Pi dikinase and phosphoenolpyruvate carboxylase were especially low until spatial cytoplasmic domains developed and leaves reached maturity, indicating a developmental transition toward C(4) photosynthesis. In most cases, there was a correlation between the accumulation of mRNA transcripts and the respective peptides, indicating at least partial control of the development of photosynthesis at the transcriptional level. During growth under moderate light, when branches containing mature leaves were enclosed in darkness for 1 month, spatial domains were maintained and there was high retention of a number of photosynthetic peptides, including Rubisco subunits and pyruvate,Pi dikinase, despite a reduction in transcript levels. When plants were transferred from moderate to low light conditions for 1 month, there was a striking shift of the central cytoplasmic compartment toward the periphery of chlorenchyma cells; the mature leaves showed strong acclimation with a shade-type photosynthetic response to light while retaining C(4) features indicative of low photorespiration. These results indicate a progressive development of C(4) photosynthesis with differences in the control mechanisms for the expression of photosynthetic genes and peptide synthesis during leaf maturation and in response to light conditions.",
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author = "Lara, {Mar{\'i}a Valeria} and Sascha Offermann and Monica Smith and Okita, {Thomas W} and Andreo, {Carlos Santiago} and Edwards, {Gerald E}",
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volume = "148",
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Download

TY - JOUR

T1 - Leaf development in the single-cell C4 system in Bienertia sinuspersici

T2 - expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions

AU - Lara, María Valeria

AU - Offermann, Sascha

AU - Smith, Monica

AU - Okita, Thomas W

AU - Andreo, Carlos Santiago

AU - Edwards, Gerald E

PY - 2008/9

Y1 - 2008/9

N2 - Bienertia sinuspersici performs C(4) photosynthesis in individual chlorenchyma cells by the development of two cytoplasmic domains (peripheral and central) with dimorphic chloroplasts, an arrangement that spatially separates the fixation of atmospheric CO(2) into C(4) acids and the donation of CO(2) from C(4) acids to Rubisco in the C(3) cycle. In association with the formation of these cytoplasmic domains during leaf maturation, developmental stages were analyzed for the expression of a number of photosynthetic genes, including Rubisco small and large subunits and key enzymes of the C(4) cycle. Early in development, Rubisco subunits and Gly decarboxylase and Ser hydroxymethyltransferase of the glycolate pathway accumulated more rapidly than enzymes associated with the C(4) cycle. The levels of pyruvate,Pi dikinase and phosphoenolpyruvate carboxylase were especially low until spatial cytoplasmic domains developed and leaves reached maturity, indicating a developmental transition toward C(4) photosynthesis. In most cases, there was a correlation between the accumulation of mRNA transcripts and the respective peptides, indicating at least partial control of the development of photosynthesis at the transcriptional level. During growth under moderate light, when branches containing mature leaves were enclosed in darkness for 1 month, spatial domains were maintained and there was high retention of a number of photosynthetic peptides, including Rubisco subunits and pyruvate,Pi dikinase, despite a reduction in transcript levels. When plants were transferred from moderate to low light conditions for 1 month, there was a striking shift of the central cytoplasmic compartment toward the periphery of chlorenchyma cells; the mature leaves showed strong acclimation with a shade-type photosynthetic response to light while retaining C(4) features indicative of low photorespiration. These results indicate a progressive development of C(4) photosynthesis with differences in the control mechanisms for the expression of photosynthetic genes and peptide synthesis during leaf maturation and in response to light conditions.

AB - Bienertia sinuspersici performs C(4) photosynthesis in individual chlorenchyma cells by the development of two cytoplasmic domains (peripheral and central) with dimorphic chloroplasts, an arrangement that spatially separates the fixation of atmospheric CO(2) into C(4) acids and the donation of CO(2) from C(4) acids to Rubisco in the C(3) cycle. In association with the formation of these cytoplasmic domains during leaf maturation, developmental stages were analyzed for the expression of a number of photosynthetic genes, including Rubisco small and large subunits and key enzymes of the C(4) cycle. Early in development, Rubisco subunits and Gly decarboxylase and Ser hydroxymethyltransferase of the glycolate pathway accumulated more rapidly than enzymes associated with the C(4) cycle. The levels of pyruvate,Pi dikinase and phosphoenolpyruvate carboxylase were especially low until spatial cytoplasmic domains developed and leaves reached maturity, indicating a developmental transition toward C(4) photosynthesis. In most cases, there was a correlation between the accumulation of mRNA transcripts and the respective peptides, indicating at least partial control of the development of photosynthesis at the transcriptional level. During growth under moderate light, when branches containing mature leaves were enclosed in darkness for 1 month, spatial domains were maintained and there was high retention of a number of photosynthetic peptides, including Rubisco subunits and pyruvate,Pi dikinase, despite a reduction in transcript levels. When plants were transferred from moderate to low light conditions for 1 month, there was a striking shift of the central cytoplasmic compartment toward the periphery of chlorenchyma cells; the mature leaves showed strong acclimation with a shade-type photosynthetic response to light while retaining C(4) features indicative of low photorespiration. These results indicate a progressive development of C(4) photosynthesis with differences in the control mechanisms for the expression of photosynthetic genes and peptide synthesis during leaf maturation and in response to light conditions.

KW - Carbon Dioxide/metabolism

KW - Carbon Isotopes/metabolism

KW - Chenopodiaceae/cytology

KW - Chlorophyll/metabolism

KW - Gene Expression Regulation, Developmental

KW - Gene Expression Regulation, Plant

KW - Light

KW - Peptides/metabolism

KW - Photosynthesis

KW - Plant Leaves/cytology

KW - Plant Proteins/metabolism

KW - Water/metabolism

U2 - 10.1104/pp.108.124008

DO - 10.1104/pp.108.124008

M3 - Article

C2 - 18667722

VL - 148

SP - 593

EP - 610

JO - Plant physiology

JF - Plant physiology

SN - 0032-0889

IS - 1

ER -

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