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Nonmycorrhizal cluster root-forming species enhance the phosphorus (P) acquisition of mycorrhizal neighbours in P-impoverished megadiverse systems. However, whether mycorrhizal plants facilitate the defence of nonmycorrhizal plants against soil-borne pathogens, in return and via their symbiosis, remains unknown. We characterised growth and defence-related compounds in Banksia menziesii (nonmycorrhizal) and Eucalyptus todtiana (ectomycorrhizal, ECM) seedlings grown either in monoculture or mixture in a multifactorial glasshouse experiment involving ECM fungi and native oomycete pathogens. Roots of B. menziesii had higher levels of phytohormones (salicylic and jasmonic acids, jasmonoyl-isoleucine and 12-oxo-phytodienoic acid) than E. todtiana which further activated a salicylic acid-mediated defence response in roots of B. menziesii, but only in the presence of ECM fungi. We also found that B. menziesii induced a shift in the defence strategy of E. todtiana, from defence-related secondary metabolites (phenolic and flavonoid) towards induced phytohormone response pathways. We conclude that ECM fungi play a vital role in the interactions between mycorrhizal and nonmycorrhizal plants in a severely P-impoverished environment, by introducing a competitive component within the facilitation interaction between the two plant species with contrasting nutrient-acquisition strategies. This study sheds light on the interplay between beneficial and detrimental soil microbes that shape plant-plant interaction in severely nutrient-impoverished ecosystems., (© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.)

Background and Aims: Soils in south-western Australia are severely phosphorus (P) impoverished, and plants in this region have evolved a variety of P-acquisition strategies. Phosphorus acquisition by Adenanthos cygnorum (Proteaceae) is facilitated by P-mobilizing neighbours which allows it to extend its range of habitats. However, we do not know if other Adenanthos species also exhibit a strategy based on facilitation for P acquisition in P-impoverished environments., Methods: We collected leaf and soil samples of Adenanthosbarbiger, A. cuneatus, A.meisneri,A. obovatus, A. sericeus and Adenanthos sp. Whicher Range (G.J. Keighery 9736) growing in their natural habitats at different locations within the severely P-limited megadiverse environment of south-western Australia. Hydroponic experiments were conducted to collect the carboxylates exuded by cluster roots. Pot experiments in soil were carried out to measure rhizosheath phosphatase activity., Key Results: We found no evidence for facilitation of P uptake in any of the studied Adenanthos species. Like most Proteaceae, A. cuneatus, A. meisneri, A. obovatus, A. sericeus and Adenanthos sp. Whicher Range (G.J. Keighery 9736) expressed P-mining strategies, including the formation of cluster roots. Cluster roots of A. obovatus were less effective than those of the other four Adenanthos species. In contrast to what is known for most Proteaceae, we found no cluster roots for A. barbiger. This species probably expressed a post-fire P-acquisition strategy. All Adenanthos species used P highly efficiently for photosynthesis, like other Proteaceae in similar natural habitats., Conclusions: Adenanthos is the first genus of Proteaceae found to express multiple P-acquisition strategies. The diversity of P-acquisition strategies in these Proteaceae, coupled with similarly diverse strategies in Fabaceae and Myrtaceae, demonstrates that caution is needed in making family- or genus-wide extrapolations about the strategies exhibited in severely P-impoverished megadiverse ecosystems., (© The Author(s) 2024. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

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 co-occurrence with other species., (© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.)

Plants respond to soil phosphorus (P) availability by adjusting leaf P among inorganic P (Pi) and organic P fractions (nucleic acids, phospholipids, small metabolites and a residual fraction). We tested whether phylogenetically divergent plants in a biodiversity hotspot similarly adjust leaf P allocation in response to P limitation by sampling along a 2 Myr chronosequence in southwestern Australia where nitrogen (N) limitation transitions to P limitation with increasing soil age. Total P and N, and P allocated to five chemical fractions were determined for photosynthetic organs from Melaleuca systena (Myrtaceae), Acacia rostellifera (Fabaceae) and Hakea prostrata (Proteaceae). Soil characteristics were also determined. Acacia rostellifera maintained phyllode total P and N concentrations at c. 0.5 and 16 mg g -1 DW, respectively, with a constant P-allocation pattern along the chronosequence. H. prostrata leaves allocated less P to Pi, phospholipids and nucleic acids with increasing soil age, while leaf N concentration was constant. M. systena had the greatest variation in allocating leaf P, whereas leaf N concentration decreased 20% along the chronosequence. Variation in P-allocation patterns was only partially conserved among species along the chronosequence. Such variation could have an impact on species distribution and contribute to species richness in P-limited environments., (© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.)

Phosphorus (P) fertilisers, made from rock phosphate, are used to attain high crop yields. However, rock phosphate is a finite resource and excessive P fertilisers pollute our environment, stressing the need for more P-efficient crops. Some Proteaceae have evolved in extremely P-impoverished environments. One of their adaptations is to curtail the abundance of ribosomal RNA, and thus protein, and tightly control the acquisition and assimilation of nitrogen (N) and sulfur. This differs fundamentally from plants that evolved in environments where N limits plant productivity, but is likely common in many species that evolved in P-impoverished landscapes. Here, we scrutinise the relevance of these responses towards developing P-efficient crops, focusing on plant species where 'P is in the driver's seat'., (Copyright © 2018 Elsevier Ltd. All rights reserved.)

Hakea prostrata (Proteaceae) has evolved in extremely phosphorus (P)-impoverished habitats. Unlike species that evolved in P-richer environments, it tightly controls its nitrogen (N) acquisition, matching its low protein concentration, and thus limiting its P requirement for ribosomal RNA (rRNA). Protein is a major sink for sulfur (S), but the link between low protein concentrations and S metabolism in H. prostrata is unknown, although this is pivotal for understanding this species' supreme adaptation to P-impoverished soils. Plants were grown at different sulfate supplies for 5 wk and used for nutrient and metabolite analyses. Total S content in H. prostrata was unchanged with increasing S supply, in sharp contrast with species that typically evolved in environments where P is not a major limiting nutrient. Unlike H. prostrata, other plants typically store excess available sulfate in vacuoles. Like other species, S-starved H. prostrata accumulated arginine, lysine and O-acetylserine, indicating S deficiency. Hakea prostrata tightly controls its S acquisition to match its low protein concentration and low demand for rRNA, and thus P, the largest organic P pool in leaves. We conclude that the tight control of S acquisition, like that of N, helps H. prostrata to survive in P-impoverished environments., (© 2017 The Authors. New Phytologist © 2017 New Phytologist Trust.)

Hakea prostrata (Proteaceae) has evolved in an extremely phosphorus (P)-limited environment. This species exhibits an exceptionally low ribosomal RNA (rRNA) and low protein and nitrogen (N) concentration in its leaves. Little is known about the N requirement of this species and its link to P metabolism, despite this being the key to understanding how it functions with a minimal P budget. H. prostrata plants were grown with various N supplies. Metabolite and elemental analyses were performed to determine its N requirement. H. prostrata maintained its organ N content and concentration at a set point, independent of a 25-fold difference nitrate supplies. This is in sharp contrast to plants that are typically studied, which take up and store excess nitrate. Plants grown without nitrate had lower leaf chlorophyll and carotenoid concentrations, indicating N deficiency. However, H. prostrata plants at low or high nitrate availability had the same photosynthetic pigment levels and hence were not physiologically compromised by the treatments. The tight control of nitrate acquisition in H. prostrata retains protein at a very low level, which results in a low demand for rRNA and P. We surmise that the constrained nitrate acquisition is an adaptation to severely P-impoverished soils., (© 2016 John Wiley & Sons Ltd.)

Hakea prostrata (Proteaceae) is adapted to severely phosphorus-impoverished soils and extensively replaces phospholipids during leaf development. We investigated how polar lipid profiles change during leaf development and in response to external phosphate supply. Leaf size was unaffected by a moderate increase in phosphate supply. However, leaf protein concentration increased by more than 2-fold in young and mature leaves, indicating that phosphate stimulates protein synthesis. Orthologs of known lipid-remodeling genes in Arabidopsis (Arabidopsis thaliana) were identified in the H. prostrata transcriptome. Their transcript profiles in young and mature leaves were analyzed in response to phosphate supply alongside changes in polar lipid fractions. In young leaves of phosphate-limited plants, phosphatidylcholine/phosphatidylethanolamine and associated transcript levels were higher, while phosphatidylglycerol and sulfolipid levels were lower than in mature leaves, consistent with low photosynthetic rates and delayed chloroplast development. Phosphate reduced galactolipid and increased phospholipid concentrations in mature leaves, with concomitant changes in the expression of only four H. prostrata genes, GLYCEROPHOSPHODIESTER PHOSPHODIESTERASE1, N-METHYLTRANSFERASE2, NONSPECIFIC PHOSPHOLIPASE C4, and MONOGALACTOSYLDIACYLGLYCEROL3. Remarkably, phosphatidylglycerol levels decreased with increasing phosphate supply and were associated with lower photosynthetic rates. Levels of polar lipids with highly unsaturated 32:x (x = number of double bonds in hydrocarbon chain) and 34:x acyl chains increased. We conclude that a regulatory network with a small number of central hubs underpins extensive phospholipid replacement during leaf development in H. prostrata. This hard-wired regulatory framework allows increased photosynthetic phosphorus use efficiency and growth in a low-phosphate environment. This may have rendered H. prostrata lipid metabolism unable to adjust to higher internal phosphate concentrations., (© 2014 American Society of Plant Biologists. All Rights Reserved.)

In common with many plants native to low P soils, jarrah (Eucalyptus marginata) develops toxicity symptoms upon exposure to elevated phosphorus (P). Jarrah plants can establish arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) associations, along with a non-colonizing symbiosis described recently. AM colonization is known to influence the pattern of expression of genes required for P uptake of host plants and our aim was to investigate this phenomenon in relation to P sensitivity. Therefore, we examined the effect on hosts of the presence of AM and ECM fungi in combination with toxic pulses of P and assessed possible correlations between the induced tolerance and the shoot P concentration. The P transport dynamics of AM (Rhizophagus irregularis and Scutellospora calospora), ECM (Scleroderma sp.), non-colonizing symbiosis (Austroboletus occidentalis), dual mycorrhizal (R. irregularis and Scleroderma sp.), and non-mycorrhizal (NM) seedlings were monitored following two pulses of P. The ECM and A. occidentalis associations significantly enhanced the shoot P content of jarrah plants growing under P-deficient conditions. In addition, S. calospora, A. occidentalis, and Scleroderma sp. all stimulated plant growth significantly. All inoculated plants had significantly lower phytotoxicity symptoms compared to NM controls 7 days after addition of an elevated P dose (30 mg P kg(-1) soil). Following exposure to toxicity-inducing levels of P, the shoot P concentration was significantly lower in R. irregularis-inoculated and dually inoculated plants compared to NM controls. Although all inoculated plants had reduced toxicity symptoms and there was a positive linear relationship between rank and shoot P concentration, the protective effect was not necessarily explained by the type of fungal association or the extent of mycorrhizal colonization.

Plant adaptations associated with a high efficiency of phosphorus (P) acquisition can be used to increase productivity and sustainability in a world with a growing population and decreasing rock phosphate reserves. White lupin (Lupinus albus) produces cluster roots that release carboxylates to efficiently mobilize P from P-sorbing soils. It has been hypothesized that an increase in the activity of the alternative oxidase (AOX) would allow for the mitochondrial oxidation of NAD(P)H produced during citrate synthesis in cluster roots at a developmental stage when there is a low demand for ATP. We used the oxygen-isotope fractionation technique to study the in vivo respiratory activities of the cytochrome oxidase pathway (COP) and the alternative oxidase pathway (AOP) in different root sections of white lupins grown hydroponically with and without P. In parallel, AOX protein levels and internal carboxylate concentrations were determined in cluster and non-cluster roots. Higher in vivo AOP activity was measured in cluster roots when malate and citrate concentrations were also high, thus confirming our hypothesis. AOX protein levels were not always correlated with in vivo AOP activity, suggesting post-translational regulation of AOX., (© 2013 John Wiley & Sons Ltd.)

Recent studies have identified genotypic variation in phosphorus (P) efficiency, but rarely have the underlying mechanisms been described at the molecular level. We demonstrate that the highly P-efficient wheat (Triticum aestivum L.) cultivar Chinese 80-55 maintains higher inorganic phosphate (Pi ) concentrations in all organs upon Pi withdrawal in combination with higher Pi acquisition in the presence of Pi when compared with the less-efficient cultivar Machete. These findings correlated with differential organ-specific expression of Pi transporters TaPHT1;2, TaPHT1;5, TaPHT1;8, TaPHT2;1 and H(+) -ATPase TaHa1. Observed transcript level differences between the cultivars suggest that higher de novo phospholipid biosynthetic activities in Pi -limited elongating basal leaf sections are another crucial adaptation in Chinese 80-55 for sustaining growth upon Pi withdrawal. These activities may be supported through enhanced breakdown of starch in Chinese 80-55 stems as suggested by higher TaGPho1 transcript levels. Chinese 80-55 fine roots on the other hand show strong suppression of transcripts involved in glycolysis, transcriptional regulation and ribosomal activities. Our work reveals major differences in the way the two contrasting cultivars allocate Pi and organic P compounds between source and sink tissues and in the acclimation of their metabolism to changes in Pi availability., (© 2013 John Wiley & Sons Ltd.)

Limitation of grain crop productivity by phosphorus (P) is widespread and will probably increase in the future. Enhanced P efficiency can be achieved by improved uptake of phosphate from soil (P-acquisition efficiency) and by improved productivity per unit P taken up (P-use efficiency). This review focuses on improved P-use efficiency, which can be achieved by plants that have overall lower P concentrations, and by optimal distribution and redistribution of P in the plant allowing maximum growth and biomass allocation to harvestable plant parts. Significant decreases in plant P pools may be possible, for example, through reductions of superfluous ribosomal RNA and replacement of phospholipids by sulfolipids and galactolipids. Improvements in P distribution within the plant may be possible by increased remobilization from tissues that no longer need it (e.g. senescing leaves) and reduced partitioning of P to developing grains. Such changes would prolong and enhance the productive use of P in photosynthesis and have nutritional and environmental benefits. Research considering physiological, metabolic, molecular biological, genetic and phylogenetic aspects of P-use efficiency is urgently needed to allow significant progress to be made in our understanding of this complex trait., (© 2012 The Authors. New Phytologist © 2012 New Phytologist Trust.)

Background and Aims Pinus massoniana: Lamb. is an important conifer forestry species in south China, but soil fertility has declined over time in monoculture plantations. Knowledge about how P. massoniana uses phosphorus (P) by distributing it among five biochemical fractions and how intercropping with broadleaf Castanopsis hystrix alters that pattern may inform long-term plantation management. Methods: We studied a single P. massoniana plantation that was split in half into a monoculture and a P. massoniana / C. hystrix intercropped plantation 25 years after establishment. We measured photosynthesis and leaf concentrations of total P, P allocated to five chemical fractions and total nitrogen (N). We also measured soil N concentrations. Results: Intercropping C. hystrix with 25-year-old P. massoniana for a further 34 years had no significant impact on P. massoniana total stem volume, although intercropped P. massoniana trees were 5 m taller. Intercropping with C. hystrix increased timber biomass due to the additional C. hystrix stems. Growth of C. hystrix was likely more limited by P than that of P. massoniana in both plantations. Total P concentration and its allocation among fractions declined with increasing leaf age, but differed in the two species. Leaf P-resorption efficiency in intercropped P. massoniana was 79%, which was about 15% greater than that in P. massoniana monoculture and in the intercropped C. hystrix. The greater P-resorption efficiency in intercropped P. massoniana than in monoculture was due to greater mobilization of P from all fractions, except phospholipids. Bulk soil N concentration was 50% greater in the intercropped plantation than in monoculture. Conclusion: Adding C. hystrix to an P. massoniana plantation was effective at increasing wood yield without compromising productivity of P. massoniana. [ABSTRACT FROM AUTHOR]

Background and aims: In extremely low-phosphorus (P) environments, most Proteaceae exude carboxylates from cluster roots. These carboxylates mobilise inorganic P which leads to a relatively high leaf manganese concentration ([Mn]). However, we found that Adenanthos cygnorum (Proteaceae) in a low-P habitat did not invariably have a high leaf [Mn] in south-western Australia. We aimed to explore how A. cygnorum acquires P in severely P-impoverished habitats. Methods: We determined soil P concentrations and leaf [Mn] of A. cygnorum growing within 1 m and more than 10 m away from other large Proteaceae. We also grew plants in a glasshouse to determine its root carboxylate exudation and rhizosheath phosphatase activity. Results: Adenanthos cygnorum did not produce functional cluster roots. It depended on carboxylates released by a P-mobilising neighbour, Banksia attenuata (Proteaceae), to acquire P when growing in severely P-impoverished soil (< 8 mg P kg− 1 dry soil). In slightly less P-impoverished soil (> 11 mg P kg− 1 dry soil), phosphatases released by A. cygnorum hydrolysed sufficient organic P that was relatively mobile. Conclusion: The reliance on facilitation of P acquisition in A cygnorum depended strongly on location. We demonstrated the exudation of phosphatases, which mobilise inorganic P; this P was adequate for growth when there was sufficient organic P in soil. Facilitation of P acquisition by B. attenuata allowed A. cygnorum to extend its range into severely P-impoverished habitats where it cannot exist without facilitation. This knowledge provides a better understanding of the diversity of P-acquisition strategies in severely P-impoverished environments. [ABSTRACT FROM AUTHOR]

Hakea prostrata R.Br. (Proteaceae) shows a 'delayed greening' strategy of leaf development characterised by reddish young leaves that become green as they mature. This trait may contribute to efficient use of phosphorus (P) during leaf development by first investing P in the development of leaf structure followed by maturation of the photosynthetic machinery. In this study, we investigated the properties of delayed greening in a highly P-efficient species to enhance our understanding of the ecological significance of this trait as a nutrient-saving and photoprotective strategy. In glasshouse-grown plants, we assessed foliar pigments, fatty acids and nutrient composition across five leaf developmental stages. Young leaves had higher concentrations of anthocyanin, P, nitrogen (N), copper (Cu), xanthophyll-cycle pigments and saturated fatty acids than mature leaves. As leaves developed, the concentration of anthocyanins decreased, whereas that of chlorophyll and the double bond index of fatty acids increased. In mature leaves, ~60% of the fatty acids was α-linolenic acid (C18:3 n-3). Mature leaves also had higher concentrations of aluminium (Al), calcium (Ca) and manganese (Mn) than young leaves. We conclude that delayed greening in H. prostrata is a strategy that saves P as well as N and Cu through sequential allocation of these resources, first to cell production and structural development, and then to supplement chloroplast development. This strategy also protects young leaves against photodamage and oxidative stress during leaf expansion under high-light conditions. Hakea prostrata (Proteaceae) shows delayed greening during leaf development. This strategy is linked to nutrient-use efficiency. We show that delayed greening helps H. prostrata to save nutrients through sequential allocation of these resources first to cell production and structural development and then to chloroplast development. Delayed greening also offers photoprotection to young leaves during early leaf expansion. [ABSTRACT FROM AUTHOR]