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

Abstract

ORCID IDs: 0000-0002-6113-9570 (R.S.); 0000-0002-4118-2272 (H.L.); 0000-0002-3819-6358 (R.J.).Hakea prostrata (Proteaceae) is adapted to severely phosphorus-impoverished soils and extensively replaces phospholipids during leaf development. We investigated how polar lipid profiles change during leaf development and in response to external phosphate supply. Leaf size was unaffected by a moderate increase in phosphate supply. However, leaf protein concentration increased by more than 2-fold in young and mature leaves, indicating that phosphate stimulates protein synthesis. Orthologs of known lipid-remodeling genes in Arabidopsis (Arabidopsis thaliana) were identified in the H. prostrata transcriptome. Their transcript profiles in young and mature leaves were analyzed in response to phosphate supply alongside changes in polar lipid fractions. In young leaves of phosphate-limited plants, phosphatidylcholine/phosphatidylethanolamine and associated transcript levels were higher, while phosphatidylglycerol and sulfolipid levels were lower than in mature leaves, consistent with low photosynthetic rates and delayed chloroplast development. Phosphate reduced galactolipid and increased phospholipid concentrations in mature leaves, with concomitant changes in the expression of only four H. prostrata genes, GLYCEROPHOSPHODIESTER PHOSPHODIESTERASE1, N-METHYLTRANSFERASE2, NONSPECIFIC PHOSPHOLIPASE C4, and MONOGALACTOSYLDIACYLGLYCEROL3. Remarkably, phosphatidylglycerol levels decreased with increasing phosphate supply and were associated with lower photosynthetic rates. Levels of polar lipids with highly unsaturated 32:x (x = number of double bonds in hydrocarbon chain) and 34:x acyl chains increased. We conclude that a regulatory network with a small number of central hubs underpins extensive phospholipid replacement during leaf development in H. prostrata. This hardwired regulatory framework allows increased photosynthetic phosphorus use efficiency and growth in a low-phosphate environment. This may have rendered H. prostrata lipid metabolism unable to adjust to higher internal phosphate concentrations.

Single-gene resolution of locally adaptive genetic variation in Mexican maize

“…Variation in lipid composition has been linked with multiple environmental factors (32; 33; 34; 35; 36; 37), is associated with variation in flowering time (38), and population genetic analysis suggests that lipid metabolic pathways may have been important in local adaptation to highland regions in Mexico and South America (31). We thus compared our results to a QTL analysis of G × E for phospholipid metabolites in Mexican highland maize (39).…”

Biodiversity hotspots and Ocbil theory

“…de Campos et al (2013) x Hakea prostrata (Proteaceae) Kuppusamy et al (2014) x x global Phylogenetic ecology of foliar N and P and N:P Mediterranean-type ecosystems Stock and Verboom (2012) x x x Many species Lambers et al (2010) x Various species Oliveira et al (2015) Plant Soil (2012) 6 (e) Complex seed biology, germination strategies…”

Plant phospholipases D and C and their diverse functions in stress responses

“…Amino acid sequences among the six NPCs vary with an exceptionally high identity of 84.7% between NPC4 and NPC5. Additionally, five NPC orthologues were recently identified in rice [141], three in Proteaceae (Hakea prostrata) [142], and a phylogenetic analysis revealed some NPC families in evolutionarily distinct plant species [143]. NPCs possess a phosphoesterase domain necessary for esterase activity and three unknown domains highly conserved with a bacterial (Mycobacterium tuberculosis) PC-PLC.…”