Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: An adaptation improving phosphorus-use efficiency

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Abstract

Plants allocate nutrients to specific leaf cell types; eudicots are thought to predominantly allocate phosphorus (P) to epidermal/bundle sheath cells. However, three Proteaceae species have been shown to preferentially allocate P to mesophyll cells instead. These Proteaceae species are highly adapted to P-impoverished habitats, with exceptionally high photosynthetic P-use efficiencies (PPUE). We hypothesized that preferential allocation of P to photosynthetic mesophyll cells is an important trait in species adapted to extremely P-impoverished habitats, contributing to their high PPUE. We used elemental X-ray mapping to determine leaf cell-specific nutrient concentrations for 12 Proteaceae species, from habitats of strongly contrasting soil P concentrations, in Australia, Brazil, and Chile. We found that only species from extremely P-impoverished habitats preferentially allocated P to photosynthetic mesophyll cells, suggesting it has evolved as an adaptation to their extremely P-impoverished habitat and that it is not a family-wide trait. Our results highlight the possible role of soil P in driving the evolution of ecologically relevant nutrient allocation patterns and that these patterns cannot be generalized across families. Furthermore, preferential allocation of P to photosynthetic cells may provide new and exciting strategies to improve PPUE in crop species.

Original languageEnglish
Pages (from-to)605-619
JournalPlant Cell and Environment
Volume41
Issue number3
DOIs
Publication statusPublished - Mar 2018

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Proteaceae
Phosphorus
Ecosystem
Mesophyll Cells
phosphorus
habitats
mesophyll
Food
cells
Soil
Chile
bundle sheath cells
nutrients
Brazil
X-Rays
leaves
soil
X-radiation
nutrient content
crops

Cite this

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title = "Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: An adaptation improving phosphorus-use efficiency",
abstract = "Plants allocate nutrients to specific leaf cell types; eudicots are thought to predominantly allocate phosphorus (P) to epidermal/bundle sheath cells. However, three Proteaceae species have been shown to preferentially allocate P to mesophyll cells instead. These Proteaceae species are highly adapted to P-impoverished habitats, with exceptionally high photosynthetic P-use efficiencies (PPUE). We hypothesized that preferential allocation of P to photosynthetic mesophyll cells is an important trait in species adapted to extremely P-impoverished habitats, contributing to their high PPUE. We used elemental X-ray mapping to determine leaf cell-specific nutrient concentrations for 12 Proteaceae species, from habitats of strongly contrasting soil P concentrations, in Australia, Brazil, and Chile. We found that only species from extremely P-impoverished habitats preferentially allocated P to photosynthetic mesophyll cells, suggesting it has evolved as an adaptation to their extremely P-impoverished habitat and that it is not a family-wide trait. Our results highlight the possible role of soil P in driving the evolution of ecologically relevant nutrient allocation patterns and that these patterns cannot be generalized across families. Furthermore, preferential allocation of P to photosynthetic cells may provide new and exciting strategies to improve PPUE in crop species.",
keywords = "Calcium accumulation, Cell-type-specific distribution, Elemental analysis, Scanning electron microscopy, X-ray microanalysis",
author = "Hayes, {Patrick E.} and Clode, {Peta L.} and Oliveira, {Rafael S.} and Hans Lambers",
year = "2018",
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language = "English",
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journal = "Plant, Cell and Environment.",
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T1 - Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells

T2 - An adaptation improving phosphorus-use efficiency

AU - Hayes, Patrick E.

AU - Clode, Peta L.

AU - Oliveira, Rafael S.

AU - Lambers, Hans

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AB - Plants allocate nutrients to specific leaf cell types; eudicots are thought to predominantly allocate phosphorus (P) to epidermal/bundle sheath cells. However, three Proteaceae species have been shown to preferentially allocate P to mesophyll cells instead. These Proteaceae species are highly adapted to P-impoverished habitats, with exceptionally high photosynthetic P-use efficiencies (PPUE). We hypothesized that preferential allocation of P to photosynthetic mesophyll cells is an important trait in species adapted to extremely P-impoverished habitats, contributing to their high PPUE. We used elemental X-ray mapping to determine leaf cell-specific nutrient concentrations for 12 Proteaceae species, from habitats of strongly contrasting soil P concentrations, in Australia, Brazil, and Chile. We found that only species from extremely P-impoverished habitats preferentially allocated P to photosynthetic mesophyll cells, suggesting it has evolved as an adaptation to their extremely P-impoverished habitat and that it is not a family-wide trait. Our results highlight the possible role of soil P in driving the evolution of ecologically relevant nutrient allocation patterns and that these patterns cannot be generalized across families. Furthermore, preferential allocation of P to photosynthetic cells may provide new and exciting strategies to improve PPUE in crop species.

KW - Calcium accumulation

KW - Cell-type-specific distribution

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KW - Scanning electron microscopy

KW - X-ray microanalysis

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