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

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.

Lipid Biosynthesis and Protein Concentration Respond Uniquely to Phosphate Supply during Leaf Development in Highly Phosphorus-Efficient Hakea prostrata

“…Given that the majority of total RNA is rRNA, the change in RNA concentration during leaf development in these glasshousegrown seedlings resembled the decrease in rRNA that was found between young and mature leaves of H. prostrata in the field (Sulpice et al, 2014).…”

“…Their young leaves have especially low levels of plastidic rRNA and a very low photosynthetic capacity. As the leaves develop, the levels of plastidic rRNA increase, concomitant with an increase in photosynthetic capacity, while their cytosolic rRNA levels decline (Sulpice et al, 2014).…”

“…use P-mining strategies to acquire inorganic phosphate (Pi; Shane et al, 2003;Shane and Lambers, 2005;Lambers et al, 2012a), but they also use leaf P very efficiently. They achieve this efficiency by allocating P to mesophyll cells rather than to epidermal cells (Shane et al, 2004;Lambers et al, 2015), as is common for other dicotyledons (Conn and Gilliham, 2010), by extensively replacing phospholipids by galactolipids and sulfolipids during leaf development (Lambers et al, 2012b) and by operating at very low ribosomal RNA (rRNA) levels in their leaves (Sulpice et al, 2014). The low abundance of rRNA economizes on P and also decreases the rate of protein synthesis and the resulting demand for P. In addition, many southwestern Australian Proteaceae spp.…”

“…Here, we address the question of how this trait may contribute to the high P-use efficiency of a southwestern Australian Proteaceae species, Hakea prostrata. This is one of six Proteaceae species we previously studied in their natural habitat (Lambers et al, 2012b;Sulpice et al, 2014). Here, we analyzed changes in lipid profiles and the levels of transcripts encoding lipid remodeling enzymes during leaf development in glasshouse-grown H. prostrata plants.…”

“…are adapted to severely phosphorus (P)-impoverished soils and operate at very low leaf P status without compromising rates of photosynthesis (Denton et al, 2007;Lambers et al, 2012b;Sulpice et al, 2014). A large number of these species are endemic to the South West Australian Floristic Region, which features highly weathered, P-impoverished soils (Hopper, 2009;Laliberté et al, 2012;Hayes et al, 2014).…”