Proteaceae from severely phosphorus‐impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus‐use‐efficiency

Abstract

SummaryProteaceae species in south-western Australia occur on severely phosphorus (P)-impoverished soils. They have very low leaf P concentrations, but relatively fast rates of photosynthesis, thus exhibiting extremely high photosynthetic phosphorus-use-efficiency (PPUE). Although the mechanisms underpinning their high PPUE remain unknown, one possibility is that these species may be able to replace phospholipids with nonphospholipids during leaf development, without compromising photosynthesis.For six Proteaceae species, we measured soil and leaf P concentrations and rates of photosynthesis of both young expanding and mature leaves. We also assessed the investment in galactolipids, sulfolipids and phospholipids in young and mature leaves, and compared these results with those on Arabidopsis thaliana, grown under both P-sufficient and P-deficient conditions.In all Proteaceae species, phospholipid levels strongly decreased during leaf development, whereas those of galactolipids and sulfolipids strongly increased. Photosynthetic rates increased from young to mature leaves. This shows that these species extensively replace phospholipids with nonphospholipids during leaf development, without compromising photosynthesis. A considerably less pronounced shift was observed in A. thaliana.Our results clearly show that a low investment in phospholipids, relative to nonphospholipids, offers a partial explanation for a high photosynthetic rate per unit leaf P in Proteaceae adapted to P-impoverished soils.

A Shoot-Specific Hypoxic Response of Arabidopsis Sheds Light on the Role of the Phosphate-Responsive Transcription Factor PHOSPHATE STARVATION RESPONSE1

“…Phosphate deficiency in plants originates from poor fertilization of the soil in agriculture but also occurs in natural environments (Yang and Finnegan, 2010;Plaxton and Tran, 2011;Lambers et al, 2012). Phosphate is one of the macronutrients required for plant growth and is specifically important for energy transfer (i.e.…”

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

“…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. show delayed greening (Lambers et al, 2012b). Their young leaves have especially low levels of plastidic rRNA and a very low photosynthetic capacity.…”

“…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.…”

“…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).…”

Low-Phosphate Induction of Plastidal Stromules Is Dependent on Strigolactones But Not on the Canonical Strigolactone Signaling Component MAX2

“…Phosphate is essential for cell function as it is required for the production of phospholipids, energy production, and regulation of protein activity, and much of the plant's phosphate is stored in the phospholipids of the cell membranes. When phosphate availability is limiting for the plant cell, phosphor may be mobilized from membrane phospholipids, in which case the lipids are replaced by galactolipids derived from plastids (Tjellström et al, 2008;Lambers et al, 2012). This exchange of lipids between the plastid and other membranes occurs via the endoplasmic reticulum (ER) through plastid ER membrane contact sites (Dörmann and Benning, 2002;Tjellström et al, 2008), and indeed this frequency of these contact sites is increased under low Pi conditions (Tjellström et al, 2008).…”