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Although significant intraspecific variation in photosynthetic phosphorus (P) use efficiency (PPUE) has been shown in numerous species, we still know little about the biochemical basis for differences in PPUE among genotypes within a species. Here, we grew two high PPUE and two low PPUE chickpea (Cicer arietinum) genotypes with low P supply in a glasshouse to compare their photosynthesis-related traits, total foliar P concentration ([P]) and chemical P fractions (i.e. inorganic P (Pi), metabolite P, lipid P, nucleic acid P, and residual P). Foliar cell-specific nutrient concentrations including P were characterized using elemental X-ray microanalysis. Genotypes with high PPUE showed lower total foliar [P] without slower photosynthetic rates. No consistent differences in cellular [P] between the epidermis and mesophyll cells occurred across the four genotypes. In contrast, high PPUE was associated with lower allocation to Pi and metabolite P, with PPUE being negatively correlated with the percentage of these two fractions. Furthermore, a lower allocation to Pi and metabolite P was correlated with a greater allocation to nucleic acid P, but not to lipid P. Collectively, our results suggest that a different allocation to foliar P fractions, rather than preferential P allocation to specific leaf tissues, underlies the contrasting PPUE among chickpea genotypes., (© The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

Ptilotus exaltatus accumulates phosphorus (P) to > 40 mg g -1 without toxicity symptoms, while Kennedia prostrata is intolerant of increased P supply. What physiological mechanisms underlie this difference and protect P. exaltatus from P toxicity? Ptilotus exaltatus and K. prostrata were grown in a sandy soil with low-P, high-P and P-pulse treatments. Both species hyperaccumulated P (>20 mg g -1 ) under high-P and P-pulse treatments; shoot dry weight was unchanged for P. exaltatus, but decreased by >50% for K. prostrata. Under high-P, in young fully-expanded leaves, both species accumulated P predominantly as inorganic P. However, P. exaltatus preferentially allocated P to mesophyll cells and stored calcium (Ca) as occasional crystals in specific lower mesophyll cells, separate from P, while K. prostrata preferentially allocated P to epidermal and spongy mesophyll cells, but co-located P and Ca in palisade mesophyll cells where granules with high [P] and [Ca] were evident. Mesophyll cellular [P] correlated positively with [potassium] for both species, and negatively with [sulfur] for P. exaltatus. Thus, P. exaltatus tolerated a very high leaf [inorganic P] (17 mg g -1 ), associated with P and Ca allocation to different cell types and formation of Ca crystals, thereby avoiding deleterious precipitation of Ca 3 (PO 4 ) 2 . It also showed enhanced [potassium] and decreased [sulfur] to balance high cellular [P]. Phosphorus toxicity in K. prostrata arose from co-location of Ca and P in palisade mesophyll cells. This study advances understanding of leaf physiological mechanisms for high P tolerance in a P-hyperaccumulator and indicates P. exaltatus as a promising candidate for P-phytoextraction., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2020 Elsevier Ltd. All rights reserved.)

Over 650 Proteaceae occur in south-western Australia, contributing to the region's exceptionally high biodiversity. Most Proteaceae occur exclusively on severely nutrient-impoverished, acidic soils (calcifuge), whilst only few also occur on young, calcareous soils (soil-indifferent), higher in calcium (Ca) and phosphorus (P). The calcifuge habit of Proteaceae is explained by Ca-enhanced P toxicity, putatively linked to the leaf cell-specific allocation of Ca and P. Separation of these elements is essential to avoid the deleterious precipitation of Ca-phosphate. We used quantitative X-ray microanalysis to determine leaf cell-specific nutrient concentrations of two calcifuge and two soil-indifferent Proteaceae grown in hydroponics at a range of Ca and P concentrations. Calcium enhanced the preferential allocation of P to palisade mesophyll (PM) cells under high P conditions, without a significant change in whole leaf [P]. Calcifuges showed a greater PM [P] compared with soil-indifferent species, corresponding to their greater sensitivity. This study advances our mechanistic understanding of Ca-enhanced P toxicity, supporting the proposed model, and demonstrating its role in the calcifuge distribution of Proteaceae. This furthers our understanding of nutrient interactions at the cellular level and highlights its importance to plant functioning., (© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

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&#95;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., (© 2019 John Wiley & Sons Ltd.)

Many Proteaceae are highly phosphorus (P)-sensitive and occur exclusively on old nutrient-impoverished acidic soils (calcifuge), whilst a few also occur on young calcareous soils (soil-indifferent) that are higher in available calcium (Ca) and P. Calcium increases the severity of P-toxicity symptoms, but its underlying mechanisms are unknown. We propose that Ca-enhanced P toxicity explains the calcifuge habit of most Proteaceae. Four calcifuge and four soil-indifferent Proteaceae from South-Western Australia were grown in hydroponics, at a range of P and Ca concentrations. Calcium increased the severity of P-toxicity symptoms in all species. Calcifuge Proteaceae were more sensitive to Ca-enhanced P toxicity than soil-indifferent ones. Calcifuges shared these traits: low leaf zinc concentration ([Zn]), low Zn allocation to leaves, low leaf [Zn]:[P], low root : shoot ratio, and high seed P content, compared with soil-indifferent species. This is the first demonstration of Ca-enhanced P toxicity across multiple species. Calcium-enhanced P toxicity provides an explanation for the calcifuge habit of most Proteaceae and is critical for the management of this iconic Australian family. This study represents a major advance towards an understanding of the physiological mechanisms of P toxicity and its role in the distribution of Proteaceae., (© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.)

To study mechanism underpinning the calcifuge habit of some Lupinus species, especially under low-phosphorus (P) conditions, Lupinus species that were likely to respond differently to calcium (Ca) availability were assembled, and the sensitivity to Ca under a low-P supply was assessed. Seven Lupinus species (9 genotypes, L. albus L. cv Kiev, L. albus L. P26766, L. angustifolius L. cv Mandelup, L. angustifolius L. P26723, L. luteus L. cv Pootalong, L. hispanicus ssp. bicolor Boiss. and Reut. P22999, L. pilosus Murr. P27440, L. cosentinii Guss. P27225, and L. atlanticus Gladst. P27219) were grown hydroponically at 10 or 6000 μM Ca. Leaf symptoms, gas exchange and biomass were recorded; leaf and root nutrient concentrations were analysed, and the leaf cell types in which Ca and P accumulated were determined using elemental X-ray microanalyses. Calcium toxicity was demonstrated for L. angustifolius P26723, L. hispanicus ssp. bicolor. P22999, and L. cosentinii P27225, whereas the other species were tolerant of a high Ca supply under low-P conditions. In addition, genotypic differences in Ca toxicity were found within L. angustifolius. Most Ca accumulated in the mesophyll cells in all species, whereas most P was located in epidermal cells., (© 2018 John Wiley & Sons Ltd.)

Plants allocate nutrients to specific leaf cell types, with commelinoid monocots preferentially allocating phosphorus (P) to the mesophyll and calcium (Ca) to the epidermis, whereas the opposite is thought to occur in eudicots. However, Proteaceae from severely P-impoverished habitats present the same P-allocation pattern as monocots. This raises the question of whether preferential P allocation to mesophyll cells is a phylogenetically conserved trait, exclusive to commelinoid monocots and a few Proteaceae, or a trait that has evolved multiple times to allow plants to cope with very low soil P availability. We analysed the P-allocation patterns of 16 species from 10 genera, eight families and six orders within three major clades of eudicots across different P-impoverished environments in Australia and Brazil, using elemental X-ray mapping to quantitatively determine leaf cell-specific nutrient concentrations. Many of the analysed species showed P-allocation patterns that differed substantially from that expected for eudicots. Instead, P-allocation patterns were strongly associated with the P availability in the natural habitat of the species, suggesting a convergent evolution of P-allocation patterns at the cellular level, with P limitation as selective pressure and without a consistent P-allocation pattern within eudicots. Here, we show that most eudicots from severely P-impoverished environments preferentially allocated P to their mesophyll. We surmise that this preferential P allocation to photosynthetically active cells might contribute to the very high photosynthetic P-use efficiency of species adapted to P-impoverished habitats., (© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.)

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., (© 2018 John Wiley & Sons Ltd.)

The Jurien Bay dune chronosequence in south‐western Australia's biodiversity hotspot comprises sites differing in nutrient availability, with phosphorus (P) availability declining strongly with increasing soil age. We have explored the exceptionally high photosynthetic P‐use efficiency (PPUE) of Proteaceae in this region, triggering the question what the PPUE of co‐occurring species in other families might be along the Jurien Bay chronosequence.We explored how traits associated with PPUE, photosynthetic nitrogen (N)‐use efficiency (PNUE) and leaf respiration might converge along the chronosequence, and whether Proteaceae and non‐Proteaceae species differ in leaf traits associated with nutrient use.Seven to 10 species were sampled at three sites differing in nutrient availability (ranging from N‐ to P‐limited). Measurements of leaf light‐saturated photosynthesis and dark respiration were integrated with measurements of total N and P concentration in both mature and senesced leaves, and leaf mass per unit area (LMA).Contrary to what is known for other chronosequences, rates of photosynthesis and respiration did not decrease with increasing soil age and LMA along the Jurien Bay chronosequence. However, they increased when expressed per unit leaf P. Both N and P were used much more efficiently for photosynthesis on nutrient‐poor sites, in both Proteaceae and non‐Proteaceae species. Proteaceae had the fastest rate of photosynthesis per unit leaf P, followed by species that preferentially allocate P to mesophyll cells, rather than epidermal cells.Synthesis. Our results show that with declining soil P availability, photosynthetic P‐use efficiency of all investigated species from different families increased. Plants growing on the oldest, most nutrient‐impoverished soils exhibited similar rates of CO2 exchange as plants growing on more nutrient‐rich younger soils, and extraordinarily high photosynthetic P‐use efficiency. This indicates convergence in leaf traits related to photosynthetic nutrient use on severely P‐impoverished sites. [ABSTRACT FROM AUTHOR]