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

Megan H Ryan, Parwinder Kaur, Nazanin K Nazeri, Peta L Clode, Gabriel Keeble-Gagnère, Ashlea L Doolette, Ronald J Smernik, Olivier Van Aken, Dion Nicol, Hayato Maruyama, Tatsuhiro Ezawa, Hans Lambers, A Harvey Millar, Rudi Appels

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Abstract

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.

Original languageEnglish
Pages (from-to)1987-2002
JournalPlant, Cell & Environment
Volume42
Issue number6
Early online date8 Feb 2019
DOIs
Publication statusPublished - Jun 2019

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