Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition

• Published in: Plant, cell and environment Vol. 42; no. 6; pp. 1987 - 2002
• Main Authors: Ryan, Megan H., Kaur, Parwinder, Nazeri, Nazanin K., Clode, Peta L., Keeble‐Gagnère, Gabriel, Doolette, Ashlea L., Smernik, Ronald J., Van Aken, Olivier, Nicol, Dion, Maruyama, Hayato, Ezawa, Tatsuhiro, Lambers, Hans, Millar, A. Harvey, Appels, Rudi
• Format: Journal Article
• Language: English
• Published: United States Wiley Subscription Services, Inc 01.06.2019
• Subjects: Agricultural and Veterinary sciences; Agricultural Biotechnology; Agricultural Sciences; Biologi; Biological Sciences; Biological Transport; Bioteknologi med applikationer på växter och djur; Botanik; Botany; Cell culture; cortex; crops; ecosystem services; Fertilizers; Gene expression; gene expression regulation; Gene Expression Regulation, Plant; Genes; genome assembly; Genomes; Homeostasis; Homology; inorganic phosphorus; Lantbruksvetenskap och veterinärmedicin; Magnesium; Magnesium - metabolism; Natural Sciences; Naturvetenskap; NMR; Nuclear magnetic resonance; nuclear magnetic resonance spectroscopy; phosphorous efficient crops; Phosphorus; Phosphorus - metabolism; Plant Biotechnology; Plant Biotechnology (including Forest Biotechnology); Plant Roots - cytology; Plant Roots - genetics; Plant Roots - metabolism; Plastids; Plastids - metabolism; potassium; Potassium - metabolism; Roots; Seedlings; Seedlings - cytology; Seedlings - metabolism; Sodium; Sodium - metabolism; Soil - chemistry; Spectroscopy; Transcriptome; Transmission electron microscopy; transporters; Trifolium - genetics; Trifolium - growth & development; Trifolium - metabolism; Trifolium subterraneum; Vacuoles; Vacuoles - metabolism; Växtbioteknologi; Växtbioteknologi (Här ingår: Skogsbioteknologi); X-radiation; X-ray microanalysis; nuclear magnetic resonance spectroscopy; X-ray microanalysis; phosphorous efficient crops; vacuoles; roots; plastids
• ISSN: 0140-7791; 1365-3040; 1365-3040
• DOI: 10.1111/pce.13531

Crops with improved uptake of fertilizer phosphorus (P) would reduce P losses and confer environmental benefits. We examined how P‐sufficient 6‐week‐old soil‐grown Trifolium subterraneum plants, and 2‐week‐old seedlings in solution culture, accumulated P in roots after inorganic P (Pi) addition. In contrast to our expectation that vacuoles would accumulate excess P, after 7 days, X‐ray microanalysis showed that vacuolar [P] remained low (<12 mmol kg−1). However, in the plants after P addition, some cortex cells contained globular structures extraordinarily rich in P (often >3,000 mmol kg−1), potassium, magnesium, and sodium. Similar structures were evident in seedlings, both before and after P addition, with their [P] increasing threefold after P addition. Nuclear magnetic resonance (NMR) spectroscopy showed seedling roots accumulated Pi following P addition, and transmission electron microscopy (TEM) revealed large plastids. For seedlings, we demonstrated that roots differentially expressed genes after P addition using RNAseq mapped to the T. subterraneum reference genome assembly and transcriptome profiles. Among the most up‐regulated genes after 4 hr was TSub_g9430.t1, which is similar to plastid envelope Pi transporters (PHT4;1, PHT4;4): expression of vacuolar Pi‐transporter homologs did not change. We suggest that subcellular P accumulation in globular structures, which may include plastids, aids cytosolic Pi homeostasis under high‐P availability. We examined clover roots after inorganic phosphorus (Pi) addition. Although vacuolar P concentration was unchanged, unexpectedly, P accumulated in intracellular globular structures and genes similar to plastid envelope Pi transporters were up‐regulated. The structures likely aid cytosolic Pi homeostasis.