Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species

Ronan Sulpice, Hirofumi Ishihara, Armin Schlereth, Gregory R. Cawthray, Beatrice Encke, Patrick Giavalisco, Alexander Ivakov, Stéphanie Arrivault, Ricarda Jost, Nicole Krohn, John Kuo, Etienne Laliberté, Stuart J. Pearse, John A. Raven, Wolf Rüdiger Scheible, François Teste, Erik J. Veneklaas, Mark Stitt, Hans Lambers

Research output: Contribution to journalArticle

46 Citations (Scopus)

Abstract

Proteaceae species in south-western Australia occur on phosphorus- (P) impoverished soils. Their leaves contain very low P levels, but have relatively high rates of photosynthesis. We measured ribosomal RNA (rRNA) abundance, soluble protein, activities of several enzymes and glucose 6-phosphate (Glc6P) levels in expanding and mature leaves of six Proteaceae species in their natural habitat. The results were compared with those for Arabidopsis thaliana. Compared with A.thaliana, immature leaves of Proteaceae species contained very low levels of rRNA, especially plastidic rRNA. Proteaceae species showed slow development of the photosynthetic apparatus ('delayed greening'), with young leaves having very low levels of chlorophyll and Calvin-Benson cycle enzymes. In mature leaves, soluble protein and Calvin-Benson cycle enzyme activities were low, but Glc6P levels were similar to those in A.thaliana. We propose that low ribosome abundance contributes to the high P efficiency of these Proteaceae species in three ways: (1) less P is invested in ribosomes; (2) the rate of growth and, hence, demand for P is low; and (3) the especially low plastidic ribosome abundance in young leaves delays formation of the photosynthetic machinery, spreading investment of P in rRNA. Although Calvin-Benson cycle enzyme activities are low, Glc6P levels are maintained, allowing their effective use.

Original languageEnglish
Pages (from-to)1276-1298
Number of pages23
JournalPlant, Cell & Environment
Volume37
Issue number6
Early online date23 Dec 2013
DOIs
Publication statusPublished - 2014

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Proteaceae
Phosphorus
Photosynthesis
Glucose-6-Phosphate
ribosomal RNA
Ribosomal RNA
phosphorus
glucose 6-phosphate
Ribosomes
Calvin cycle
ribosomes
leaves
Enzymes
enzyme activity
Western Australia
South Australia
Chlorophyll
Arabidopsis
Ecosystem
Proteins

Cite this

Sulpice, Ronan ; Ishihara, Hirofumi ; Schlereth, Armin ; Cawthray, Gregory R. ; Encke, Beatrice ; Giavalisco, Patrick ; Ivakov, Alexander ; Arrivault, Stéphanie ; Jost, Ricarda ; Krohn, Nicole ; Kuo, John ; Laliberté, Etienne ; Pearse, Stuart J. ; Raven, John A. ; Scheible, Wolf Rüdiger ; Teste, François ; Veneklaas, Erik J. ; Stitt, Mark ; Lambers, Hans. / Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. In: Plant, Cell & Environment. 2014 ; Vol. 37, No. 6. pp. 1276-1298.
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abstract = "Proteaceae species in south-western Australia occur on phosphorus- (P) impoverished soils. Their leaves contain very low P levels, but have relatively high rates of photosynthesis. We measured ribosomal RNA (rRNA) abundance, soluble protein, activities of several enzymes and glucose 6-phosphate (Glc6P) levels in expanding and mature leaves of six Proteaceae species in their natural habitat. The results were compared with those for Arabidopsis thaliana. Compared with A.thaliana, immature leaves of Proteaceae species contained very low levels of rRNA, especially plastidic rRNA. Proteaceae species showed slow development of the photosynthetic apparatus ('delayed greening'), with young leaves having very low levels of chlorophyll and Calvin-Benson cycle enzymes. In mature leaves, soluble protein and Calvin-Benson cycle enzyme activities were low, but Glc6P levels were similar to those in A.thaliana. We propose that low ribosome abundance contributes to the high P efficiency of these Proteaceae species in three ways: (1) less P is invested in ribosomes; (2) the rate of growth and, hence, demand for P is low; and (3) the especially low plastidic ribosome abundance in young leaves delays formation of the photosynthetic machinery, spreading investment of P in rRNA. Although Calvin-Benson cycle enzyme activities are low, Glc6P levels are maintained, allowing their effective use.",
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Sulpice, R, Ishihara, H, Schlereth, A, Cawthray, GR, Encke, B, Giavalisco, P, Ivakov, A, Arrivault, S, Jost, R, Krohn, N, Kuo, J, Laliberté, E, Pearse, SJ, Raven, JA, Scheible, WR, Teste, F, Veneklaas, EJ, Stitt, M & Lambers, H 2014, 'Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species' Plant, Cell & Environment, vol. 37, no. 6, pp. 1276-1298. https://doi.org/10.1111/pce.12240

Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. / Sulpice, Ronan; Ishihara, Hirofumi; Schlereth, Armin; Cawthray, Gregory R.; Encke, Beatrice; Giavalisco, Patrick; Ivakov, Alexander; Arrivault, Stéphanie; Jost, Ricarda; Krohn, Nicole; Kuo, John; Laliberté, Etienne; Pearse, Stuart J.; Raven, John A.; Scheible, Wolf Rüdiger; Teste, François; Veneklaas, Erik J.; Stitt, Mark; Lambers, Hans.

In: Plant, Cell & Environment, Vol. 37, No. 6, 2014, p. 1276-1298.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species

AU - Sulpice, Ronan

AU - Ishihara, Hirofumi

AU - Schlereth, Armin

AU - Cawthray, Gregory R.

AU - Encke, Beatrice

AU - Giavalisco, Patrick

AU - Ivakov, Alexander

AU - Arrivault, Stéphanie

AU - Jost, Ricarda

AU - Krohn, Nicole

AU - Kuo, John

AU - Laliberté, Etienne

AU - Pearse, Stuart J.

AU - Raven, John A.

AU - Scheible, Wolf Rüdiger

AU - Teste, François

AU - Veneklaas, Erik J.

AU - Stitt, Mark

AU - Lambers, Hans

PY - 2014

Y1 - 2014

N2 - Proteaceae species in south-western Australia occur on phosphorus- (P) impoverished soils. Their leaves contain very low P levels, but have relatively high rates of photosynthesis. We measured ribosomal RNA (rRNA) abundance, soluble protein, activities of several enzymes and glucose 6-phosphate (Glc6P) levels in expanding and mature leaves of six Proteaceae species in their natural habitat. The results were compared with those for Arabidopsis thaliana. Compared with A.thaliana, immature leaves of Proteaceae species contained very low levels of rRNA, especially plastidic rRNA. Proteaceae species showed slow development of the photosynthetic apparatus ('delayed greening'), with young leaves having very low levels of chlorophyll and Calvin-Benson cycle enzymes. In mature leaves, soluble protein and Calvin-Benson cycle enzyme activities were low, but Glc6P levels were similar to those in A.thaliana. We propose that low ribosome abundance contributes to the high P efficiency of these Proteaceae species in three ways: (1) less P is invested in ribosomes; (2) the rate of growth and, hence, demand for P is low; and (3) the especially low plastidic ribosome abundance in young leaves delays formation of the photosynthetic machinery, spreading investment of P in rRNA. Although Calvin-Benson cycle enzyme activities are low, Glc6P levels are maintained, allowing their effective use.

AB - Proteaceae species in south-western Australia occur on phosphorus- (P) impoverished soils. Their leaves contain very low P levels, but have relatively high rates of photosynthesis. We measured ribosomal RNA (rRNA) abundance, soluble protein, activities of several enzymes and glucose 6-phosphate (Glc6P) levels in expanding and mature leaves of six Proteaceae species in their natural habitat. The results were compared with those for Arabidopsis thaliana. Compared with A.thaliana, immature leaves of Proteaceae species contained very low levels of rRNA, especially plastidic rRNA. Proteaceae species showed slow development of the photosynthetic apparatus ('delayed greening'), with young leaves having very low levels of chlorophyll and Calvin-Benson cycle enzymes. In mature leaves, soluble protein and Calvin-Benson cycle enzyme activities were low, but Glc6P levels were similar to those in A.thaliana. We propose that low ribosome abundance contributes to the high P efficiency of these Proteaceae species in three ways: (1) less P is invested in ribosomes; (2) the rate of growth and, hence, demand for P is low; and (3) the especially low plastidic ribosome abundance in young leaves delays formation of the photosynthetic machinery, spreading investment of P in rRNA. Although Calvin-Benson cycle enzyme activities are low, Glc6P levels are maintained, allowing their effective use.

KW - Banksia

KW - Carbon metabolism

KW - Delayed greening

KW - Glucose 6-phosphate

KW - Hakea

KW - PPUE

KW - Rubisco

KW - Shikimate dehydrogenase

U2 - 10.1111/pce.12240

DO - 10.1111/pce.12240

M3 - Article

VL - 37

SP - 1276

EP - 1298

JO - Plant, Cell and Environment.

JF - Plant, Cell and Environment.

SN - 0140-7791

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ER -