Accumulation of phosphorus and calcium in different cells protects the phosphorus-hyperaccumulator Ptilotus exaltatus from phosphorus toxicity in high-phosphorus soils

Ye, Daihua; Clode, Peta L.; Hammer, Timothy A.; Pang, Jiayin; Lambers, Hans; Ryan, Megan H.

doi:10.1016/j.chemosphere.2020.128438

Cited by 11 publications

(10 citation statements)

References 55 publications

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“…More recently, however, several studies have indicated that selective accumulation of Ca arises from the ability of cells to take up Ca (i.e., expression of both Ca 2+ ‐permeable ion channels in the plasma membrane and Ca 2+ transporters in the tonoplast; Hayes et al, 2018 ; Storey and Leigh, 2004 ), where it can accumulate to high concentrations (>700 mM in Rhodes grass). This selective accumulation of Ca could be linked: (i) to the allocation of Ca and P in different cell types, thus avoiding the precipitation of calcium phosphate that would reduce the availability of both nutrients and impact on the cellular process (P and Ca allocated to different cell types; Conn & Gilliham, 2010 ; Hayes et al, 2018 , 2019 , Ye et al, 2021 ) or (ii) to osmotic balance in specific cell types. The present study supports both assumptions: (i) P and Ca were localized in different cells (P‐allocating epidermal and mesophyll cells did not accumulate Ca; see below) and (ii) high Ca concentration in bundle sheath cells may compensate for the low Na in the cells and thus contribute to charge and osmotic balance (Figures 2 and 3 ).…”

Section: Discussionmentioning

confidence: 99%

Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C₄ monocotyledonous halophyte

Clode

Taniguchi

et al. 2022

Plant Cell & Environment

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Halophytes accumulate and sequester high concentrations of salt in vacuoles while maintaining lower levels of salt in the cytoplasm. The current data on cellular and subcellular partitioning of salt in halophytes are, however, limited to only a few dicotyledonous C 3 species. Using cryo-scanning electron microscopy X-ray microanalysis, we assessed the concentrations of Na, Cl, K, Ca, Mg, P and S in various cell types within the leaf-blades of a monocotyledonous C 4 halophyte, Rhodes grass (Chloris gayana). We also linked, for the first time, elemental concentrations in chloroplasts of mesophyll and bundle sheath cells to their ultrastructure and photosynthetic performance of plants grown in nonsaline and saline (200 mM NaCl) conditions. Na and Cl accumulated to the highest levels in xylem parenchyma and epidermal cells, but were maintained at lower concentrations in photosynthetically active mesophyll and bundle sheath cells. Concentrations of Na and Cl in chloroplasts of mesophyll and bundle sheath cells were lower than in their respective vacuoles. No ultrastructural changes were observed in either mesophyll or bundle sheath chloroplasts, and photosynthetic activity was maintained in saline conditions. Salinity tolerance in Rhodes grass is related to specific cellular Na and Cl distributions in leaf tissues, and the ability to regulate Na and Cl concentrations in chloroplasts.bundle sheath cells, C 4 plant, cellular distribution, cryo-SEM X-ray microanalysis, mesophyll cells, Rhodes grass (Chloris gayana), salinity tolerance, transmission electron microscopy, xylem parenchyma | INTRODUCTIONSoil salinity is one of the most significant environmental factors limiting yields of crops and forages (Hillel, 2000). High salt concentration decreases the osmotic potential in the rhizosphere reducing the capacity of roots to take up water. To cope with low soil water potential induced by salt, plant tissues need to adjust osmotically for maintaining a total solute concentration greater than that in the external solution (Flowers et al., 2015). In halophytes (salttolerant plants) and in salt-tolerant nonhalophyte crops (e.g., barley),

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Section: Discussionmentioning

confidence: 99%

Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C₄ monocotyledonous halophyte

Clode

Taniguchi

et al. 2022

Plant Cell & Environment

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“…from Ye et al . (2021), were not included. However, the four data points that deviate from the rest in the first column are Hordeum leporinum Link and Hordeum vulgare L. from Chapin III & Bieleski (1982).…”

Section: Methodsmentioning

confidence: 99%

“…P-hyperaccumulating outlier species, Ptilotus exaltatus 'Joey' (Mulla Mulla) and Kennedia prostrata R.Br. from Ye et al (2021), were not included. However, the four data points that deviate from the rest in the first column are Hordeum leporinum Link and Hordeum vulgare L. from Chapin III & Bieleski (1982).…”

Section: Relationships Among Leaf P Fractionsmentioning

confidence: 99%

Phosphorus fractions in leaves

et al. 2022

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Leaf phosphorus (P) comprises four major fractions: inorganic phosphate (P i ), nucleic acids, phospholipids, P-containing metabolites and a residual fraction. In this review paper, we investigated whether allocation of P fractions varies among groups of terrestrial vascular plants, and is indicative of a species' strategy to use P efficiently. We found that as leaf total P concentration increases, the P i fraction increases the most, without a plateau, while other fractions plateau. Variability of the concentrations of leaf P fractions is greatest among families > species(family) > regions > plant life forms. The percentage of total P allocated to nucleic acid-P (20-35%) and lipid-P (14-34%) varies less among families/species. High photosynthetic P-use efficiency is associated with low concentrations of all P fractions, and preferential allocation of P to metabolite-P and mesophyll cells. Sequential resorption of P from senescing leaves starts with P i , followed by metabolite-P, and then other organic P fractions. Allocation of P to leaf P fractions varies with season. Leaf phytate concentrations vary considerably among species, associated with variation in photosynthesis and defence. Plasticity of P allocation to its fractions is important for acclimation to low soil P availability, and species-specific P allocation is needed for cooccurrence with other species.

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“…However, most studies that examined the functions of Ca in photosynthesis focused on its signaling role (Hirschi, 2004;McAinsh & Pittman, 2009), and not on how it might interact with other mineral elements. Calcium and P, for example, are rarely co-localized in high concentrations, presumably to prevent the deleterious precipitation of Ca-phosphates (Conn & Gilliham, 2010;Guilherme Pereira et al, 2018;Hayes et al, 2018;Ye et al, 2021).…”

Section: Soil-indifferent Hakeamentioning

confidence: 99%

Phosphorus toxicity, not deficiency, explains the calcifuge habit of phosphorus‐efficient Proteaceae

Pereira

Hayes

Clode

et al. 2021

Physiologia Plantarum

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The calcifuge habit of plants is commonly explained in terms of high soil pH and its effects on nutrient availability, particularly that of phosphorus (P). However, most Proteaceae that occur on nutrient-impoverished soils in south-western Australia are calcifuge, despite their ability to produce cluster-roots, which effectively mobilize soil P and micronutrients. We hypothesize that the mechanism explaining the calcifuge habit in Proteaceae is their sensitivity to P and calcium (Ca), and that soil-indifferent species are less sensitive to the interaction of these nutrients. In this study, we analyzed growth, gas-exchange rate, and chlorophyll fluorescence of two soil-indifferent and four calcifuge Hakea and Banksia (Proteaceae) species from south-western Australia, across a range of P and Ca concentrations in hydroponic solution. We observed Ca-enhanced P toxicity in all analyzed species, but to different extents depending on distribution type and genus. Increasing P supply enhanced plant growth, leaf biomass, and photosynthetic rates of soil-indifferent species in a pattern largely independent of Ca supply. In contrast, positive physiological responses to increasing [P] in calcifuges were either absent or limited to low Ca supply, indicating that calcifuges were far more sensitive to Ca-enhanced P toxicity. In calcifuge Hakeas, we attributed this to higher leaf [P], and in calcifuge Banksias to lower leaf zinc concentration. These differences help to explain these species' contrasting sensitivity to Ca-enhanced P toxicity and account for the exclusion of most Proteaceae from calcareous habitats. We surmise that Ca-enhanced P toxicity is a major factor explaining the calcifuge habit of Proteaceae, and, possibly, other P-sensitive plants.

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Accumulation of phosphorus and calcium in different cells protects the phosphorus-hyperaccumulator Ptilotus exaltatus from phosphorus toxicity in high-phosphorus soils

Cited by 11 publications

References 55 publications

Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C₄ monocotyledonous halophyte

Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C₄ monocotyledonous halophyte

Phosphorus fractions in leaves

Phosphorus toxicity, not deficiency, explains the calcifuge habit of phosphorus‐efficient Proteaceae

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Accumulation of phosphorus and calcium in different cells protects the phosphorus-hyperaccumulator Ptilotus exaltatus from phosphorus toxicity in high-phosphorus soils

Cited by 11 publications

References 55 publications

Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C4 monocotyledonous halophyte

Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C4 monocotyledonous halophyte

Phosphorus fractions in leaves

Phosphorus toxicity, not deficiency, explains the calcifuge habit of phosphorus‐efficient Proteaceae

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Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C₄ monocotyledonous halophyte

Salt tolerance in relation to elemental concentrations in leaf cell vacuoles and chloroplasts of a C₄ monocotyledonous halophyte