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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 LU ; Nicol, Dion and Maruyama, Hayato , et al. (2019) In Plant, Cell and Environment 42(6). p.1987-2002
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... (More)


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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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
nuclear magnetic resonance spectroscopy, phosphorous efficient crops, plastids, roots, vacuoles, X-ray microanalysis
in
Plant, Cell and Environment
volume
42
issue
6
pages
1987 - 2002
publisher
Wiley-Blackwell
external identifiers
  • scopus:85063451102
  • pmid:30734927
ISSN
0140-7791
DOI
10.1111/pce.13531
language
English
LU publication?
yes
id
4cdafe06-3df2-495c-990a-b9a561c7de0e
date added to LUP
2019-04-11 11:05:56
date last changed
2024-06-11 08:41:26
@article{4cdafe06-3df2-495c-990a-b9a561c7de0e,
  abstract     = {{<p><br>
                                                         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 (&lt;12 mmol kg                             <br>
                            <sup>−1</sup><br>
                                                         ). However, in the plants after P addition, some cortex cells contained globular structures extraordinarily rich in P (often &gt;3,000 mmol kg                             <br>
                            <sup>−1</sup><br>
                                                         ), 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.                         <br>
                        </p>}},
  author       = {{Ryan, Megan H. and Kaur, Parwinder and Nazeri, Nazanin K. and Clode, Peta L. and Keeble-Gagnère, Gabriel and Doolette, Ashlea L. and Smernik, Ronald J. and Van Aken, Olivier and Nicol, Dion and Maruyama, Hayato and Ezawa, Tatsuhiro and Lambers, Hans and Millar, A. Harvey and Appels, Rudi}},
  issn         = {{0140-7791}},
  keywords     = {{nuclear magnetic resonance spectroscopy; phosphorous efficient crops; plastids; roots; vacuoles; X-ray microanalysis}},
  language     = {{eng}},
  number       = {{6}},
  pages        = {{1987--2002}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Plant, Cell and Environment}},
  title        = {{Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition}},
  url          = {{http://dx.doi.org/10.1111/pce.13531}},
  doi          = {{10.1111/pce.13531}},
  volume       = {{42}},
  year         = {{2019}},
}