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

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...

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Published inPlant, 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
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Published United States Wiley Subscription Services, Inc 01.06.2019
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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. 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.
AbstractList 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.
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.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.
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 ). However, in the plants after P addition, some cortex cells contained globular structures extraordinarily rich in P (often >3,000 mmol kg ), 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.
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.
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.
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.
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.
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.
Author Keeble‐Gagnère, Gabriel
Maruyama, Hayato
Ryan, Megan H.
Clode, Peta L.
Ezawa, Tatsuhiro
Van Aken, Olivier
Lambers, Hans
Millar, A. Harvey
Appels, Rudi
Smernik, Ronald J.
Doolette, Ashlea L.
Kaur, Parwinder
Nazeri, Nazanin K.
Nicol, Dion
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  organization: The University of Western Australia
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  organization: The University of Western Australia
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  organization: Hokkaido University
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  organization: The University of Western Australia
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  surname: Appels
  fullname: Appels, Rudi
  organization: University of Melbourne, Bioscience
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Copyright 2019 John Wiley & Sons Ltd
2019 John Wiley & Sons Ltd.
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Issue 6
Keywords nuclear magnetic resonance spectroscopy
X-ray microanalysis
phosphorous efficient crops
vacuoles
roots
plastids
Language English
License 2019 John Wiley & Sons Ltd.
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Snippet Crops with improved uptake of fertilizer phosphorus (P) would reduce P losses and confer environmental benefits. We examined how P‐sufficient 6‐week‐old...
Crops with improved uptake of fertilizer phosphorus (P) would reduce P losses and confer environmental benefits. We examined how P-sufficient 6-week-old...
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crossref
wiley
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 1987
SubjectTerms 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
Title Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpce.13531
https://www.ncbi.nlm.nih.gov/pubmed/30734927
https://www.proquest.com/docview/2227653650
https://www.proquest.com/docview/2197891519
https://www.proquest.com/docview/2253256890
https://lup.lub.lu.se/record/4cdafe06-3df2-495c-990a-b9a561c7de0e
oai:portal.research.lu.se:publications/4cdafe06-3df2-495c-990a-b9a561c7de0e
Volume 42
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