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

Research output: Contribution to journalArticle

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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Seedlings
Phosphorus
Plastids
plastids
phosphorus
Trifolium subterraneum
seedlings
transporters
genome assembly
Trifolium
Electron Probe Microanalysis
phosphorus fertilizers
Fertilizers
Vacuoles
Transmission Electron Microscopy
Transcriptome
transcriptome
ecosystem services
Magnesium
Genes

Cite this

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. / Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition. In: Plant, Cell & Environment. 2019 ; Vol. 42, No. 6. pp. 1987-2002.
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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.",
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Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition. / 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.

In: Plant, Cell & Environment, Vol. 42, No. 6, 06.2019, p. 1987-2002.

Research output: Contribution to journalArticle

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AU - Kaur, Parwinder

AU - Nazeri, Nazanin K

AU - Clode, Peta L

AU - Keeble-Gagnère, Gabriel

AU - Doolette, Ashlea L

AU - Smernik, Ronald J

AU - Van Aken, Olivier

AU - Nicol, Dion

AU - Maruyama, Hayato

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AU - Lambers, Hans

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AU - Appels, Rudi

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AB - 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.

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JO - Plant, Cell and Environment.

JF - Plant, Cell and Environment.

SN - 0140-7791

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