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

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 - Plant Cell Environ. (2014)

Bottom Line: The results were compared with those for Arabidopsis 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.

View Article: PubMed Central - PubMed

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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Anatomy and morphology of selected Proteaceae species used in this study. Top left: Cross section of a mature leaf of Banksia menziesii, showing a double epidermis, stomatal crypts, mesophyll (fluorescing red), sclerenchyma and a thick midrib. Top right: Cross section of an old leaf of B. menziesii, showing a double epidermis, stomatal crypts that are covered with trichomes, mesophyll, sclerenchymatic fibres and vascular tissue. Bottom left: Habitat photo of Hakea flabellifolia, showing dark green previous years’ foliage and yellow young expanding leaves (photo: Marion L. Cambridge). Bottom right: Habitat photo of Banksia attenuata, showing dark green previous years’ foliage and yellow young expanding leaves; both were used for gas-exchange measurements presented in Lambers et al. (2012b) (photo: Marion L. Cambridge).
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fig01: Anatomy and morphology of selected Proteaceae species used in this study. Top left: Cross section of a mature leaf of Banksia menziesii, showing a double epidermis, stomatal crypts, mesophyll (fluorescing red), sclerenchyma and a thick midrib. Top right: Cross section of an old leaf of B. menziesii, showing a double epidermis, stomatal crypts that are covered with trichomes, mesophyll, sclerenchymatic fibres and vascular tissue. Bottom left: Habitat photo of Hakea flabellifolia, showing dark green previous years’ foliage and yellow young expanding leaves (photo: Marion L. Cambridge). Bottom right: Habitat photo of Banksia attenuata, showing dark green previous years’ foliage and yellow young expanding leaves; both were used for gas-exchange measurements presented in Lambers et al. (2012b) (photo: Marion L. Cambridge).

Mentions: Leaves of all six Proteaceae species showed very high values for leaf mass per unit area (LMA) and leaf dry matter content (LDMC) compared with those of A. thaliana (Table 1). This is accounted for by the large proportion of sclerenchymatic tissue in the leaf blade as well as a very thick midrib (Fig. 1). The leaf of B. menziesii had a double epidermis (Fig. 1), which is common for this genus (Swart 1988; Edwards et al. 2000; Mast & Givnish 2002; Jordan et al. 2005). Leaf thickness was calculated from these primary data, showing values for young leaves of 222–600 μm and for mature leaves of 504–780 μm, in the same range as described based on microscopic observations (Hassiotou et al. 2009; Lambers et al. 2012b) or using digital callipers (Hassiotou et al. 2010).


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

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 - Plant Cell Environ. (2014)

Anatomy and morphology of selected Proteaceae species used in this study. Top left: Cross section of a mature leaf of Banksia menziesii, showing a double epidermis, stomatal crypts, mesophyll (fluorescing red), sclerenchyma and a thick midrib. Top right: Cross section of an old leaf of B. menziesii, showing a double epidermis, stomatal crypts that are covered with trichomes, mesophyll, sclerenchymatic fibres and vascular tissue. Bottom left: Habitat photo of Hakea flabellifolia, showing dark green previous years’ foliage and yellow young expanding leaves (photo: Marion L. Cambridge). Bottom right: Habitat photo of Banksia attenuata, showing dark green previous years’ foliage and yellow young expanding leaves; both were used for gas-exchange measurements presented in Lambers et al. (2012b) (photo: Marion L. Cambridge).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4260170&req=5

fig01: Anatomy and morphology of selected Proteaceae species used in this study. Top left: Cross section of a mature leaf of Banksia menziesii, showing a double epidermis, stomatal crypts, mesophyll (fluorescing red), sclerenchyma and a thick midrib. Top right: Cross section of an old leaf of B. menziesii, showing a double epidermis, stomatal crypts that are covered with trichomes, mesophyll, sclerenchymatic fibres and vascular tissue. Bottom left: Habitat photo of Hakea flabellifolia, showing dark green previous years’ foliage and yellow young expanding leaves (photo: Marion L. Cambridge). Bottom right: Habitat photo of Banksia attenuata, showing dark green previous years’ foliage and yellow young expanding leaves; both were used for gas-exchange measurements presented in Lambers et al. (2012b) (photo: Marion L. Cambridge).
Mentions: Leaves of all six Proteaceae species showed very high values for leaf mass per unit area (LMA) and leaf dry matter content (LDMC) compared with those of A. thaliana (Table 1). This is accounted for by the large proportion of sclerenchymatic tissue in the leaf blade as well as a very thick midrib (Fig. 1). The leaf of B. menziesii had a double epidermis (Fig. 1), which is common for this genus (Swart 1988; Edwards et al. 2000; Mast & Givnish 2002; Jordan et al. 2005). Leaf thickness was calculated from these primary data, showing values for young leaves of 222–600 μm and for mature leaves of 504–780 μm, in the same range as described based on microscopic observations (Hassiotou et al. 2009; Lambers et al. 2012b) or using digital callipers (Hassiotou et al. 2010).

Bottom Line: The results were compared with those for Arabidopsis 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.

View Article: PubMed Central - PubMed

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.

Show MeSH