1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 73, 2022
  5. Article

Annual Review of Plant Biology

Volume 73, 2022

Phosphorus Acquisition and Utilization in Plants

Abstract

Tremendous progress has been made on molecular aspects of plant phosphorus (P) nutrition, often without heeding information provided by soil scientists, ecophysiologists, and crop physiologists. This review suggests ways to integrate information from different disciplines.

When soil P availability is very low, P-mobilizing strategies are more effective than mycorrhizal strategies. Soil parameters largely determine how much P roots can acquire from P-impoverished soil, and kinetic properties of P transporters are less important. Changes in the expression of P transporters avoid P toxicity.

Plants vary widely in photosynthetic P-use efficiency, photosynthesis per unit leaf P. The challenge is to discover what the trade-offs are of different patterns of investment in P fractions. Less investment may save P, but are costs incurred? Are these costs acceptable for crops? These questions can be resolved only by the concerted action of scientists working at both molecular and physiological levels, rather than pursuing these problems independently.

Keyword(s): carboxylates, manganese, phosphorus toxicity, phosphorus-acquisition efficiency, phosphorus-use efficiency, silicon
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-102720-125738
2022-05-20
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-102720-125738.html?itemId=/content/journals/10.1146/annurev-arplant-102720-125738&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abbott LK, Robson AD, De Boer G. 1984. The effect of phosphorus on the formation of hyphae in soil by the vesicular-arbuscular mycorrhizal fungus Glomus fasciculatum. New Phytol 97:437–46
     [Google Scholar]
  2. 2.
    Abrahão A, de Britto Costa P, Teodoro GS, Lambers H, Nascimento DL et al. 2020. Vellozioid roots allow for habitat specialization among rock- and soil-dwelling Velloziaceae in campos rupestres. Funct. Ecol. 34:442–57
     [Google Scholar]
  3. 3.
    Abrahão A, Ryan MH, Laliberté E, Oliveira RS, Lambers H. 2018. Phosphorus- and nitrogen-acquisition strategies in two Bossiaea species (Fabaceae) along retrogressive soil chronosequences in south-western Australia. Physiol. Plant 163:323–43
     [Google Scholar]
  4. 4.
    Ahanger MA, Bhat JA, Siddiqui MH, Rinklebe J, Ahmad P 2020. Integration of silicon and secondary metabolites in plants: a significant association in stress tolerance. J. Exp. Bot. 71:6758–74
     [Google Scholar]
  5. 5.
    Albornoz FE, Burgess TI, Lambers H, Etchells H, Laliberté E. 2017. Native soilborne pathogens equalize differences in competitive ability between plants of contrasting nutrient-acquisition strategies. J. Ecol. 105:549–57
     [Google Scholar]
  6. 6.
    Alkarawi HH, Zotz G. 2014. Phytic acid in green leaves of herbaceous plants—temporal variation in situ and response to different nitrogen/phosphorus fertilizing regimes. AoB Plants 6:plu048
     [Google Scholar]
  7. 7.
    Anderson G, Williams EG, Moir JO 1974. A comparison of the sorption of inorganic orthophosphate and inositol hexaphosphate by six acid soils. J. Soil Sci. 25:51–62
     [Google Scholar]
  8. 8.
    Andersson MX, Larsson KE, Tjellström H, Liljenberg C, Sandelius AS. 2005. Phosphate-limited oat. J. Biol. Chem. 280:27578–86
     [Google Scholar]
  9. 9.
    Andersson MX, Stridh MH, Larsson KE, Liljenberg C, Sandelius AS. 2003. Phosphate-deficient oat replaces a major portion of the plasma membrane phospholipids with the galactolipid digalactosyldiacylglycerol. FEBS Lett 537:128–32
     [Google Scholar]
  10. 10.
    Asher CJ, Loneragan JF. 1967. Response of plants to phosphate concentration in solution culture: I. Growth and phosphorus content. Soil Sci 103:225–33
     [Google Scholar]
  11. 11.
    Bahl J, Francke B, Monéger R 1976. Lipid composition of envelopes, prolamellar bodies and other plastid membranes in etiolated, green and greening wheat leaves. Planta 129:193–201
     [Google Scholar]
  12. 12.
    Barber SA. 1962. A diffusion and mass-flow concept of soil nutrient availability. Soil Sci 93:39–49
     [Google Scholar]
  13. 13.
    Barrow NJ. 2017. The effects of pH on phosphate uptake from the soil. Plant Soil 410:401–10
     [Google Scholar]
  14. 14.
    Barrow NJ. 2021. Comparing two theories about the nature of soil phosphate. Eur. J. Soil Sci. 72:679–85
     [Google Scholar]
  15. 15.
    Barrow NJ, Sen A, Roy N, Debnath A. 2021. The soil phosphate fractionation fallacy. Plant Soil 459:1–11
     [Google Scholar]
  16. 16.
    Berzelius JJ. 1814. An Attempt to Establish a Pure Scientific System of Mineralogy: by the Application of the Electro-Chemical Theory and the Chemical Proportions, transl J. Black. Edinburgh, UK: R. Baldwin
     [Google Scholar]
  17. 17.
    Bieleski RL. 1968. Effect of phosphorus deficiency on levels of phosphorus compounds in Spirodela. Plant Physiol 43:1309–16
     [Google Scholar]
  18. 18.
    Bieleski RL. 1973. Phosphate pools, phosphate transport, and phosphate availability. Annu. Rev. Plant Physiol. 24:225–52
     [Google Scholar]
  19. 19.
    Blake RE, Walter LM. 1999. Kinetics of feldspar and quartz dissolution at 70–80°C and near-neutral pH: effects of organic acids and NaCl. Geochim. Cosmochim. Acta 63:2043–59
     [Google Scholar]
  20. 20.
    Bolland MDA. 1997. Comparative phosphorus requirement of four lupin species. J. Plant Nutr. 20:1239–53
     [Google Scholar]
  21. 21.
    Braun-Blanquet J. 1949. Übersicht der Pflanzengesellschaften rätiens (II). Vegetatio 1:129–46
     [Google Scholar]
  22. 22.
    Bray AW, Oelkers EH, Bonneville S, Wolff-Boenisch D, Potts NJ et al. 2015. The effect of pH, grain size, and organic ligands on biotite weathering rates. Geochim. Cosmochim. Acta 164:127–45
     [Google Scholar]
  23. 23.
    Breeze VG, Wild A, Hopper MJ, Jones LHP. 1984. The uptake of phosphate by plants from flowing nutrient solution. II. Growth of Lolium perenne L. at constant phosphate concentrations. J. Exp. Bot. 35:1210–21
     [Google Scholar]
  24. 24.
    Breshears DD, Fontaine JB, Ruthrof KX, Field JP, Feng X et al. 2021. Underappreciated plant vulnerabilities to heat waves. New Phytol 231:32–39
     [Google Scholar]
  25. 25.
    Brundrett MC. 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77
     [Google Scholar]
  26. 26.
    Bulgarelli RG, De Oliveira VH, de Andrade SAL. 2020. Arbuscular mycorrhizal symbiosis alters the expression of PHT1 phosphate transporters in roots and nodules of P-starved soybean plants. Theor. Exp. Plant Physiol. 32:243–53
     [Google Scholar]
  27. 27.
    Cade-Menun BJ. 2017. Characterizing phosphorus forms in cropland soils with solution 31P-NMR: past studies and future research needs. Chem. Biol. Technol. Agric. 4:19
     [Google Scholar]
  28. 28.
    Cama J, Ganor J. 2006. The effects of organic acids on the dissolution of silicate minerals: a case study of oxalate catalysis of kaolinite dissolution. Geochim. Cosmochim. Acta 70:2191–209
     [Google Scholar]
  29. 29.
    Chang SC, Jackson ML. 1957. Fraction of soil forms of phosphorus. Soil Sci 84:133–44
     [Google Scholar]
  30. 30.
    Cheong BE, Beine-Golovchuk O, Gorka M, Ho WWH, Martinez-Seidel F et al. 2021. Arabidopsis REI-LIKE proteins activate ribosome biogenesis during cold acclimation. Sci. Rep 11:2410Arabidopsis may buffer fluctuating protein translation by recruiting preexisting nontranslating ribosomes upon stress-induced increased demands before increased de novo synthesis.
     [Google Scholar]
  31. 31.
    Chiou T-J, Lin S-I. 2011. Signaling network in sensing phosphate availability in plants. Annu. Rev. Plant Biol. 62:185–206
     [Google Scholar]
  32. 32.
    Clarkson DT, Hanson JB. 1980. The mineral nutrition of higher plants. Annu. Rev. Plant Physiol. 31:239–98
     [Google Scholar]
  33. 33.
    Clarkson DT, Scattergood CB. 1982. Growth and phosphate transport in barley and tomato plants during the development of, and recovery from, phosphate-stress. J. Exp. Bot. 33:865–75
     [Google Scholar]
  34. 34.
    Colwell JD. 1965. An automatic procedure for the determination of phosphorus in sodium hydrogen carbonate extract of soil. Chem. Ind. 10:893–95
     [Google Scholar]
  35. 35.
    Cong W-F, Suriyagoda LDB, Lambers H. 2020. Tightening the phosphorus cycle through phosphorus-efficient crop genotypes. Trends Plant Sci 25:967–75
     [Google Scholar]
  36. 36.
    Conn S, Gilliham M. 2010. Comparative physiology of elemental distributions in plants. Ann. Bot. 105:1081–102
     [Google Scholar]
  37. 37.
    Coskun D, Deshmukh R, Sonah H, Menzies JG, Reynolds O et al. 2019. The controversies of silicon's role in plant biology. New Phytol 221:67–85
     [Google Scholar]
  38. 38.
    Cowan AK. 2006. Phospholipids as plant growth regulators. Plant Growth Regul 48:97–109
     [Google Scholar]
  39. 39.
    de Campos MCR, Pearse SJ, Oliveira RS, Lambers H. 2013. Downregulation of net phosphorus-uptake capacity is inversely related to leaf phosphorus-resorption proficiency in four species from a phosphorus-impoverished environment. Ann. Bot. 111:445–54
     [Google Scholar]
  40. 40.
    de Tombeur F, Cornelis J-T, Lambers H. 2021. Silicon mobilisation by root-released carboxylates. Trends Plant Sci 26:1116–25
     [Google Scholar]
  41. 41.
    de Tombeur F, Laliberté E, Lambers H, Faucon M-P, Zemunik G et al. 2021. A shift from phenol to silica-based leaf defences during long-term soil and ecosystem development. Ecol. Lett. 24:984–95
     [Google Scholar]
  42. 42.
    de Tombeur F, Roux P, Cornelis J-T. 2021. Silicon dynamics through the lens of soil-plant-animal interactions: perspectives for agricultural practices. Plant Soil 467:1–28
     [Google Scholar]
  43. 43.
    de Tombeur F, Turner BL, Laliberté E, Lambers H, Mahy G et al. 2020. Plants sustain the terrestrial silicon cycle during ecosystem retrogression. Science 369:1245–48
     [Google Scholar]
  44. 44.
    Debona D, Rodrigues FA, Datnoff LE. 2017. Silicon's role in abiotic and biotic plant stresses. Annu. Rev. Phytopathol. 55:85–107
     [Google Scholar]
  45. 45.
    Dechassa N, Schenk MK, Claassen N, Steingrobe B 2003. Phosphorus efficiency of cabbage (Brassica oleraceae L. var. capitata), carrot (Daucus carota L.), and potato (Solanum tuberosum L.). Plant Soil 250:215–24
     [Google Scholar]
  46. 46.
    Denton MD, Veneklaas EJ, Freimoser FM, Lambers H. 2007. Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus. Plant Cell Environ 30:1557–65
     [Google Scholar]
  47. 47.
    Dissanayaka DMSB, Ghahremani M, Siebers M, Wasaki J, Plaxton WC 2020. Recent insights into the metabolic adaptations of phosphorus-deprived plants. J. Exp. Bot. 72:199–223
     [Google Scholar]
  48. 48.
    Doolette AL, Smernik RJ. 2016. Phosphorus speciation of dormant grapevine (Vitis vinifera L.) canes in the Barossa Valley, South Australia. Aust. J. Grape Wine Res. 22:462–68
     [Google Scholar]
  49. 49.
    Dörmann P, Benning C. 2002. Galactolipids rule in seed plants. Trends Plant Sci 7:112–18
     [Google Scholar]
  50. 50.
    Dunlop J, Bowling DJF. 1978. Uptake of phosphate by white clover. II. The effect of pH on the electrogenic phosphate pump. J. Exp. Bot. 29:1147–53
     [Google Scholar]
  51. 51.
    Epstein E. 1999. Silicon. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:641–64
     [Google Scholar]
  52. 52.
    Epstein E. 2009. Silicon: its manifold roles in plants. Ann. Appl. Biol. 155:155–60
     [Google Scholar]
  53. 53.
    Epstein E, Bloom AJ. 2005. Mineral Nutrition of Plants: Principles and Perspectives Sunderland, MA: Sinauer
  54. 54.
    García-López AM, Recena R, Delgado A 2021. The adsorbent capacity of growing media does not constrain myo-inositol hexakiphosphate hydrolysis but its use as a phosphorus source by plants. Plant Soil 459:277–88Sorption of phytate P in soil restricts its use by plants because of the sorption of P after phytate hydrolysis.
     [Google Scholar]
  55. 55.
    Gardner WK, Parbery DG, Barber DA. 1981. Proteoid root morphology and function in Lupinus albus. Plant Soil 60:143–47
     [Google Scholar]
  56. 56.
    Gardner WK, Parbery DG, Barber DA. 1982. The acquisition of phosphorus by Lupinus albus L. II. The effect of varying phosphorus supply and soil type on some characteristics of the soil/root interface. Plant Soil 68:33–41
     [Google Scholar]
  57. 57.
    Ghahremani M, Tran H, Biglou SG, O'Gallagher B, She Y-M, Plaxton WC 2019. A glycoform of the secreted purple acid phosphatase AtPAP26 co-purifies with a mannose-binding lectin (AtGAL1) upregulated by phosphate-starved Arabidopsis. Plant Cell Environ 42:1139–57
     [Google Scholar]
  58. 58.
    Green DG, Ferguson WS, Warder FG 1973. Accumulation of toxic levels of phosphorus in the leaves of phosphorus-deficient barley. Can. J. Plant Sci. 53:241–46
     [Google Scholar]
  59. 59.
    Griffiths M, York LM. 2020. Targeting root ion uptake kinetics to increase plant productivity and nutrient use efficiency. Plant Physiol 182:1854–68
     [Google Scholar]
  60. 60.
    Groves RH, Keraitis K. 1976. Survival and growth of seedlings of three sclerophyll species at high levels of phosphorus and nitrogen. Aust. J. Bot. 24:681–90
     [Google Scholar]
  61. 61.
    Grundon NJ. 1972. Mineral nutrition of some Queensland heath plants. J. Ecol. 60:171–81
     [Google Scholar]
  62. 62.
    Gu C, Dam T, Hart SC, Turner BL, Chadwick OA et al. 2020. Quantifying uncertainties in sequential chemical extraction of soil phosphorus using XANES spectroscopy. Environ. Sci. Technol. 54:2257–67
     [Google Scholar]
  63. 63.
    Guilherme Pereira C, Clode PL, Oliveira RS, Lambers H 2018. Eudicots from severely phosphorus-impoverished environments preferentially allocate phosphorus to their mesophyll. New Phytol 218:959–73
     [Google Scholar]
  64. 64.
    Guilherme Pereira C, Hayes PE, O'Sullivan O, Weerasinghe L, Clode PL et al. 2019. Trait convergence in photosynthetic nutrient-use efficiency along a 2-million year dune chronosequence in a global biodiversity hotspot. J. Ecol. 107:2006–23
     [Google Scholar]
  65. 65.
    Güsewell S, Schroth MH. 2017. How functional is a trait? Phosphorus mobilization through root exudates differs little between Carex species with and without specialized dauciform roots. New Phytol 215:1438–50
     [Google Scholar]
  66. 66.
    Hagen CE, Hopkins HT. 1955. Ionic species in orthophosphate absorption by barley roots. Plant Physiol 30:193–99
     [Google Scholar]
  67. 67.
    Han Z, Shi J, Pang J, Yan L, Finnegan PM, Lambers H 2021. Foliar nutrient allocation patterns in Banksia attenuata and Banksia sessilis differing in growth rate and adaptation to low-phosphorus habitats. Ann. Bot. 128:419–30
     [Google Scholar]
  68. 68.
    Hawkesford MJ, Cakmak I, Coskun D, De Kok LJ, Lambers H et al. 2022. Functions of macronutrients. Marschner's Mineral Nutrition of Plants Z Rengel, I Cakmak, PJ White London: Elsevier. , 4th ed.. In press
    [Google Scholar]
  69. 69.
    Hawkins H-J, Cramer MD, Mesjasz-Przybylowicz J, Przybylowicz W, Louw E, O'Brien C. 2008. Prevention and amelioration of phosphorus toxicity in Proteaceae grown on previously fertilised land. Acta Hort 869:37–46
     [Google Scholar]
  70. 70.
    Hawkins H-J, Hettasch H, Mesjasz-Przybylowicz J, Przybylowicz W, Cramer MD 2008. Phosphorus toxicity in the Proteaceae: a problem in post-agricultural lands. Sci. Hort. 117:357–65
     [Google Scholar]
  71. 71.
    Hayes PE, Clode PL, Guilherme Pereira C, Lambers H 2019. Calcium modulates leaf cell-specific phosphorus allocation in Proteaceae from south-western Australia. J. Exp. Bot. 70:3995–4009Phosphorus sensitivity is enhanced by preferential P allocation to mesophyll and aggravated by Ca displacing more P to mesophyll cells.
     [Google Scholar]
  72. 72.
    Hayes PE, Clode PL, Oliveira RS, Lambers H. 2018. Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency. Plant Cell Environ 41:605–19
     [Google Scholar]
  73. 73.
    Hayes PE, Guilherme Pereira C, Clode PL, Lambers H 2019. Calcium-enhanced phosphorus-toxicity in calcifuge and soil-indifferent Proteaceae along the Jurien Bay chronosequence. New Phytol 221:764–77
     [Google Scholar]
  74. 74.
    Hayes PE, Nge FJ, Cramer MD, Finnegan PM, Fu P et al. 2021. Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus-impoverished landscapes. Plant Soil 462:67–88
     [Google Scholar]
  75. 75.
    Hayes PE, Turner BL, Lambers H, Laliberté E. 2014. Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J. Ecol. 102:396–410
     [Google Scholar]
  76. 76.
    Hedin LO, Vitousek PM, Matson PA. 2003. Nutrient losses over four million years of tropical forest development. Ecology 84:2231–55
     [Google Scholar]
  77. 77.
    Hedley MJ, Stewart JWB, Chauhan BS. 1982. Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci. Soc. Am. J. 46:970–76
     [Google Scholar]
  78. 78.
    Hellebust JA, Bidwell RGS. 1963. Protein turnover in wheat and snapdragon leaves: preliminary investigations. Can. J. Bot. 41:969–83
     [Google Scholar]
  79. 79.
    Hodson MJ, Evans DE. 2020. Aluminium–silicon interactions in higher plants: an update. J. Exp. Bot. 71:6719–29
     [Google Scholar]
  80. 80.
    Hübel F, Beck E. 1993. In-situ determination of the P-relations around the primary root of maize with respect to inorganic and phytate-P. Plant Soil 157:1–9
     [Google Scholar]
  81. 81.
    Jaffré T. 1979. Accumulation du manganèse par les Protéacées de Nouvelle-Calédonie. C. R. Acad. Sci. 289:425–28
     [Google Scholar]
  82. 82.
    Johnston AE, Poulton PR. 2019. Phosphorus in agriculture: a review of results from 175 years of research at Rothamsted, UK. J. Environ. Qual. 48:1133–44
     [Google Scholar]
  83. 83.
    Jouhet J, Maréchal E, Baldan B, Bligny R, Joyard J, Block MA 2004. Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J. Cell Biol. 167:863–74
     [Google Scholar]
  84. 84.
    Kanda H, Kasukabe Y, Fujita H, Washino T, Tachibana S 1994. Effect of low root temperature on ribonucleic acid concentrations in figleaf gourd and cucumber roots differing in tolerance to chilling temperature. J. Jap. Soc. Hort. Sci. 63:611–18
     [Google Scholar]
  85. 85.
    Kobayashi T. 2011. Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptability in yeast. Cell. Mol. Life Sci. 68:1395–403
     [Google Scholar]
  86. 86.
    Konoplenko MA, Güsewell S, Veselkin DV. 2017. Taxonomic and ecological patterns in root traits of Carex (Cyperaceae). Plant Soil 420:37–48
     [Google Scholar]
  87. 87.
    Kuerban M, Jiao W, Pang J, Jing J, Qiu L-J et al. 2020. Targeting low-phytate soybean genotypes without compromising desirable phosphorus-acquisition traits. Front. Genet. 11:574547
     [Google Scholar]
  88. 88.
    Kuppusamy T, Giavalisco P, Arvidsson S, Sulpice R, Stitt M et al. 2014. Lipid biosynthesis and protein concentration respond uniquely to phosphate supply during leaf development in highly phosphorus-efficient Hakea prostrata. Plant Physiol 166:1891–911
     [Google Scholar]
  89. 89.
    Lagace TA, Ridgway ND. 2013. The role of phospholipids in the biological activity and structure of the endoplasmic reticulum. Biochim. Biophys. Acta Mol. Cell Res. 1833:2499–510
     [Google Scholar]
  90. 90.
    Lambers H, Albornoz FE, Arruda AJ, Barker T, Finnegan PM et al. 2019. Nutrient-acquisition strategies. A Jewel in the Crown of a Global Biodiversity Hotspot H Lambers 227–48 Perth, Aust: Kwongan Found., West. Aust. Nat. Club
     [Google Scholar]
  91. 91.
    Lambers H, Albornoz FE, Kotula L, Laliberté E, Ranathunge K et al. 2018. How belowground interactions contribute to the coexistence of mycorrhizal and non-mycorrhizal species in severely phosphorus-impoverished hyperdiverse ecosystems. Plant Soil 424:11–34
     [Google Scholar]
  92. 92.
    Lambers H, Barrow NJ. 2020. P2O5, K2O, CaO, MgO, and basic cations: pervasive use of references to molecules that do not exist in soil. Plant Soil 452:1–4
     [Google Scholar]
  93. 93.
    Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E et al. 2012. Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. New Phytol 196:1098–108Highly P-efficient Proteaceae replace phospholipids by sulfolipids and galactolipids during leaf development but exhibit rapid rates of photosynthesis.
     [Google Scholar]
  94. 94.
    Lambers H, Clode PL, Hawkins H, Laliberté E, Oliveira RS et al. 2015. Metabolic adaptations of the non-mycotrophic Proteaceae to soils with low phosphorus availability. Annual Plant Reviews, Vol. 48: Phosphorus Metabolism in Plants WC Plaxton, H Lambers 289–336 Chichester, UK: Wiley & Sons
     [Google Scholar]
  95. 95.
    Lambers H, Guilherme Pereira C, Wright IJ, Bellingham PJ, Bentley LP et al. 2021. Leaf manganese concentrations as a tool to assess belowground plant functioning in phosphorus-impoverished environments. Plant Soil 461:43–61
     [Google Scholar]
  96. 96.
    Lambers H, Hayes PE, Laliberté E, Oliveira RS, Turner BL. 2015. Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci 20:83–90
     [Google Scholar]
  97. 97.
    Lambers H, Juniper D, Cawthray GR, Veneklaas EJ, Martínez-Ferri E. 2002. The pattern of carboxylate exudation in Banksia grandis (Proteaceae) is affected by the form of phosphate added to the soil. Plant Soil 238:111–22
     [Google Scholar]
  98. 98.
    Lambers H, Oliveira RS. 2019. Plant Physiological Ecology Cham, Switz: Springer. , 3rd ed..
  99. 99.
    Lambers H, Plaxton WC 2015. Phosphorus: back to the roots. Annual Plant Reviews, Vol. 48: Phosphorus Metabolism in Plants WC Plaxton, H Lambers 3–22 Chichester, UK: Wiley & Sons
     [Google Scholar]
  100. 100.
    Lambers H, Raven JA, Shaver GR, Smith SE. 2008. Plant nutrient-acquisition strategies change with soil age. Trends Ecol. Evol. 23:95–103
     [Google Scholar]
  101. 101.
    Lamont B. 1982. Mechanisms for enhancing nutrient uptake in plants, with particular reference to Mediterranean South Africa and Western Australia. Bot. Rev. 48:597–689
     [Google Scholar]
  102. 102.
    Liu J, Samac DA, Bucciarelli B, Allan DL, Vance CP 2005. Signaling of phosphorus deficiency-induced gene expression in white lupin requires sugar and phloem transport. Plant J 41:257–68
     [Google Scholar]
  103. 103.
    López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L. 2014. Phosphate nutrition: improving low-phosphate tolerance in crops. Annu. Rev. Plant Biol. 65:95–123
     [Google Scholar]
  104. 104.
    Lopez FB, Fort A, Tadini L, Probst AV, McHale M et al. 2021. Gene dosage compensation of rRNA transcript levels in Arabidopsis thaliana lines with reduced ribosomal gene copy number. Plant Cell 33:1135–50
     [Google Scholar]
  105. 105.
    Lott JNA, Bojarski M, Kolasa J, Batten GD, Campbell LC. 2009. A review of the phosphorus content of dry cereal and legume crops of the world. Int. J. Agric. Res. Gov. Ecol. 8:351–70
     [Google Scholar]
  106. 106.
    Lugli LF, Andersen KM, Aragão LEOC, Cordeiro AL, Cunha HFV et al. 2020. Multiple phosphorus acquisition strategies adopted by fine roots in low-fertility soils in Central Amazonia. Plant Soil 450:49–63
     [Google Scholar]
  107. 107.
    Mai W, Xue X, Feng G, Yang R, Tian C 2019. Arbuscular mycorrhizal fungi—15-fold enlargement of the soil volume of cotton roots for phosphorus uptake in intensive planting conditions. Eur. J. Soil Biol. 90:31–35
     [Google Scholar]
  108. 108.
    Marshall RS, Vierstra RD. 2018. Autophagy: the master of bulk and selective recycling. Annu. Rev. Plant Biol. 69:173–208
     [Google Scholar]
  109. 109.
    Martinez-Seidel F, Beine-Golovchuk O, Hsieh Y-C, Kopka J. 2020. Systematic review of plant ribosome heterogeneity and specialization. Front. Plant Sci. 11:948Plants allocate large amounts of resources to the production of ribosomes, which turn out to be subject to extensive regulation.
     [Google Scholar]
  110. 110.
    Matusick G, Ruthrof KX, Brouwers NC, Dell B, Hardy GSJ 2013. Sudden forest canopy collapse corresponding with extreme drought and heat in a mediterranean-type eucalypt forest in southwestern Australia. Eur. J. For. Res. 132:497–510
     [Google Scholar]
  111. 111.
    Matzek V, Vitousek PM. 2009. N:P stoichiometry and protein:RNA ratios in vascular plants: an evaluation of the growth-rate hypothesis. Ecol. Lett. 12:765–71
     [Google Scholar]
  112. 112.
    McLaren TI, Smernik RJ, Simpson RJ, McLaughlin MJ, McBeath TM et al. 2016. The chemical nature of organic phosphorus that accumulates in fertilized soils of a temperate pasture as determined by solution 31P NMR spectroscopy. J. Plant Nutr. Soil Sci. 10:27–38
     [Google Scholar]
  113. 113.
    McQuillan M, Smernik RJ, Doolette AL. 2020. Partitioning of phosphorus between biochemical and storage compounds in leaves follows a consistent pattern across four Australian genera growing in native settings. Plant Soil 454:57–75To scrutinize leaf P fractions, 31P-NMR identifies P molecules; improving the preservation of sampled material will make this a powerful technique.
     [Google Scholar]
  114. 114.
    Mimura T, Dietz KJ, Kaiser W, Schramm MJ, Kaiser G, Heber U 1990. Phosphate transport across biomembranes and cytosolic phosphate homeostasis in barley leaves. Planta 180:139–46
     [Google Scholar]
  115. 115.
    Moir J, Jordan P, Moot D, Lucas R 2016. Phosphorus response and optimum pH ranges of twelve pasture legumes grown in an acid upland New Zealand soil under glasshouse conditions. J. Soil Sci. Plant Nutr. 16:438–60
     [Google Scholar]
  116. 116.
    Muchhal US, Raghothama KG. 1999. Transcriptional regulation of plant phosphate transporters. PNAS 96:5868–72
     [Google Scholar]
  117. 117.
    Narang RA, Bruene A, Altmann T. 2000. Analysis of phosphate acquisition efficiency in different Arabidopsis accessions. Plant Physiol 124:1786–99
     [Google Scholar]
  118. 118.
    Nelson CJ, Alexova R, Jacoby RP, Millar AH. 2014. Proteins with high turnover rate in barley leaves estimated by proteome analysis combined with in planta isotope labeling. Plant Physiol 166:91–108Barley leaf proteins turn over at 100-fold different rates; those related to photosynthesis are among those that turn over fastest.
     [Google Scholar]
  119. 119.
    Newton I, Hooke R. 1675. Isaac Newton Letter to Robert Hooke, 5 February 1675. Simon Gratz Collection Historical Society of Pennsylvania Philadelphia: https://digitallibrary.hsp.org/index.php/Detail/objects/9792
  120. 120.
    Nge FJ, Cambridge ML, Ellsworth DS, Zhong H, Lambers H. 2020. Cluster roots are common in Daviesia and allies (Mirbelioids; Fabaceae). J. R. Soc. W. Austr. 103:111–18
     [Google Scholar]
  121. 121.
    Nichols DG, Beardsell DV. 1981. Interactions of calcium, nitrogen and potassium with phosphorus on the symptoms of toxicity in Grevillea cv. ‘Poorinda Firebird. ’. Plant Soil 61:437–45
     [Google Scholar]
  122. 122.
    Nussaume L, Kanno S, Javot H, Marin E, Nakanishi TM, Thibaud M-C 2011. Phosphate import in plants: focus on the PHT1 transporters. Front. Plant Sci. 2:83
     [Google Scholar]
  123. 123.
    Nye PH. 1966. The effect of the nutrient intensity and buffering power of a soil, and the absorbing power, size and root hairs of a root, on nutrient absorption by diffusion. Plant Soil 25:81–105
     [Google Scholar]
  124. 124.
    Nye PH, Tinker PB. 1977. Solute Movement in the Soil-Root System Oxford, UK: Blackwell
  125. 125.
    Pang J, Ruchi B, Zhao H, Bansal R, Bohuon E et al. 2018. The carboxylate-releasing phosphorus-mobilising strategy could be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–29
     [Google Scholar]
  126. 126.
    Pang J, Wen Z, Kidd D, Ryan MH, Yu R et al. 2021. Advances in understanding plant root uptake of phosphorus. Understanding and Improving Crop Root Function PJ Gregory 321–72 Cambridge, UK: Burleigh Dodds Sci. Publ.
     [Google Scholar]
  127. 127.
    Parfitt RL. 1979. The availability of P from phosphate-goethite bridging complexes. Desorption and uptake by ryegrass. Plant Soil 53:55–65
     [Google Scholar]
  128. 128.
    Pate JS, Bell TL. 1999. Application of the ecosystem mimic concept to the species-rich Banksia woodlands of Western Australia. Agrofor. Syst. 45:303–41
     [Google Scholar]
  129. 129.
    Paungfoo-Lonhienne C, Lonhienne TGA, Mudge SR, Schenk PM, Christie M et al. 2010. DNA is taken up by root hairs and pollen, and stimulates root and pollen tube growth. Plant Physiol 153:799–805
     [Google Scholar]
  130. 130.
    Pierre WH, Parker FW. 1927. Soil phosphorus studies: II. The concentration of organic and inorganic phosphorus in the soil solution and soil extracts and the availibility of the organic phosphorus to plants. Soil Sci 24:119–28
     [Google Scholar]
  131. 131.
    Preuss CP, Huang CY, Tyerman SD. 2011. Proton-coupled high-affinity phosphate transport revealed from heterologous characterization in Xenopus of barley-root plasma membrane transporter, HvPHT1;1. Plant Cell Environ 34:681–89
     [Google Scholar]
  132. 132.
    Raboy V 2007. Seed phosphorus and the development of low-phytate crops. Inositol Phosphates: Linking Agriculture and the Environment BL Turner, AE Richardson, EJ Mullaney 111–32 Wallingford, UK: CABI
     [Google Scholar]
  133. 133.
    Rae AL, Jarmey JM, Mudge SR, Smith FW. 2004. Over-expression of a high-affinity phosphate transporter in transgenic barley plants does not enhance phosphate uptake rates. Funct. Plant Biol. 31:141–48
     [Google Scholar]
  134. 134.
    Raghothama KG. 1999. Phosphate acquisition. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:665–93
     [Google Scholar]
  135. 135.
    Raven JA. 2018. The potential effect of low cell osmolarity on cell function through decreased concentration of enzyme substrates. J. Exp. Bot. 69:4667–73
     [Google Scholar]
  136. 136.
    Raven JA, Lambers H, Smith SE, Westoby M. 2018. Costs of acquiring phosphorus by vascular land plants: patterns and implications for plant coexistence. New Phytol 217:1420–27
     [Google Scholar]
  137. 137.
    Reef R, Ball MC, Feller IC, Lovelock CE 2010. Relationship between RNA:DNA ratio, growth and elemental stoichiometry in mangrove trees. Funct. Ecol. 24:1064–72
     [Google Scholar]
  138. 138.
    Rees TAV, Raven JA 2021. The maximum growth rate hypothesis is correct for eukaryotic photosynthetic organisms, but not cyanobacteria. New Phytol 230:601–11
     [Google Scholar]
  139. 139.
    Rengel Z, Cakmak I, White PJ, eds. 2022. Marschner's Mineral Nutrition of Plants London: Elsevier. , 4th ed..
  140. 140.
    Roberts JKM. 1984. Study of plant metabolism in vivo using NMR spectroscopy. Annu. Rev. Plant Physiol. 35:375–86
     [Google Scholar]
  141. 141.
    Rossiter RC. 1952. Phosphorus toxicity in subterranean clover and oats grown on Muchea sand, and the modifying effects of lime and nitrate-nitrogen. Aust. J. Agric. Res. 3:227–43
     [Google Scholar]
  142. 142.
    Sadowski PG, Groen AJ, Dupree P, Lilley KS. 2008. Sub-cellular localization of membrane proteins. Proteomics 8:3991–4011
     [Google Scholar]
  143. 143.
    Sakano K. 1990. Proton/phosphate stoichiometry in uptake of inorganic phosphate by cultured cells of Catharanthus roseus (L.) G. Don. Plant Physiol 93:479–83
     [Google Scholar]
  144. 144.
    Salih KJ, Duncan O, Li L, O'Leary B, Fenske R et al. 2020. Impact of oxidative stress on the function, abundance, and turnover of the Arabidopsis 80S cytosolic ribosome. Plant J 103:128–39
     [Google Scholar]
  145. 145.
    Salih KJ, Duncan O, Li L, Trösch J, Millar AH 2020. The composition and turnover of the Arabidopsis thaliana 80S cytosolic ribosome. Biochem. J. 477:3019–32
     [Google Scholar]
  146. 146.
    Schubert S, Steffens D, Ashraf I. 2020. Is occluded phosphate plant-available?. J. Plant Nutr. Soil Sci. 183:338–44
     [Google Scholar]
  147. 147.
    Sentenac H, Grignon C. 1985. Effect of pH on orthophosphate uptake by corn roots. Plant Physiol 77:136–41
     [Google Scholar]
  148. 148.
    Shane MW, Cawthray GR, Cramer MD, Kuo J, Lambers H. 2006. Specialized ‘dauciform’ roots of Cyperaceae are structurally distinct, but functionally analogous with ‘cluster’ roots. Plant Cell Environ 29:1989–99
     [Google Scholar]
  149. 149.
    Shane MW, Lambers H. 2005. Cluster roots: a curiosity in context. Plant Soil 274:101–25
     [Google Scholar]
  150. 150.
    Shane MW, Lambers H. 2006. Systemic suppression of cluster-root formation and net P-uptake rates in Grevillea crithmifolia at elevated P supply: a proteacean with resistance for developing symptoms of ‘P toxicity. ’. J. Exp. Bot. 57:413–23
     [Google Scholar]
  151. 151.
    Shane MW, McCully ME, Lambers H. 2004. Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). J. Exp. Bot. 55:1033–44
     [Google Scholar]
  152. 152.
    Shane MW, Szota C, Lambers H. 2004. A root trait accounting for the extreme phosphorus sensitivity of Hakea prostrata (Proteaceae). Plant Cell Environ 27:991–1004
     [Google Scholar]
  153. 153.
    Shi J, Strack D, Albornoz F, Han Z, Lambers H 2020. Differences in investment and functioning of cluster roots account for different distributions between Banksia attenuata and B. sessilis, with contrasting life history. Plant Soil 447:85–98
     [Google Scholar]
  154. 154.
    Silberbush M, Barber SA. 1983. Sensitivity of simulated phosphorus uptake to parameters used by a mechanistic-mathematical model. Plant Soil 74:93–100
     [Google Scholar]
  155. 155.
    Smith RJ, Hopper SD, Shane MW. 2011. Sand-binding roots in Haemodoraceae: global survey and morphology in a phylogenetic context. Plant Soil 348:453–70
     [Google Scholar]
  156. 156.
    Smith SE, Anderson IC, Smith FA 2015. Mycorrhizal associations and P acquisition: from cells to ecosystems. Annual Plant Reviews, Vol. 48: Phosphorus Metabolism in Plants WC Plaxton, H Lambers 409–40 Chichester, UK: Wiley & Sons
     [Google Scholar]
  157. 157.
    Smith SE, Smith FA. 2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62:227–50
     [Google Scholar]
  158. 158.
    Smyth TJ, Sanchez PA. 1980. Effects of lime, silicate, and phosphorus applications to an oxisol on phosphorus sorption and ion retention. Soil Sci. Soc. Am. J. 44:500–5
     [Google Scholar]
  159. 159.
    Song A, Xue G, Cui P, Fan F, Liu H et al. 2016. The role of silicon in enhancing resistance to bacterial blight of hydroponic- and soil-cultured rice. Sci. Rep. 6:24640
     [Google Scholar]
  160. 160.
    Sprent JI. 1999. Nitrogen fixation and growth of non-crop legume species in diverse environments. Perspect. Plant Ecol. Evol. Syst. 2:149–62
     [Google Scholar]
  161. 161.
    Sterner R, Elser J. 2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere Princeton, NJ: Princeton Univ. Press
  162. 162.
    Stevens TJ, Arkin IT. 2000. Do more complex organisms have a greater proportion of membrane proteins in their genomes?. Proteins 39:417–20
     [Google Scholar]
  163. 163.
    Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B et al. 2014. Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant Cell Environ 37:1276–98Highly P-efficient Proteaceae exhibit very low levels of ribosomal RNA yet exhibit high activities of photosynthetic enzymes and photosynthesis.
     [Google Scholar]
  164. 164.
    Syers JK, Johnston AE, Curtin D. 2008. Changing concepts of the behavior of soil and fertilizer phosphorus and reconciling these with agronomic information. Efficiency of Soil and Fertilizer Phosphorus Use: Reconciling Changing Concepts of Soil Phosphorus Behaviour with Agronomic Information15–26 Rome: FAO
     [Google Scholar]
  165. 165.
    Tachibana S. 1987. Effect of root temperature on the concentration of various forms of phosphorus in cucumber and figleaf gourd plants. Bull. Fac. Agric. Mie Univ. 74:1–8
     [Google Scholar]
  166. 166.
    Takagi D, Miyagi A, Tazoe Y, Suganami M, Kawai-Yamada M et al. 2020. Phosphorus toxicity disrupts Rubisco activation and reactive oxygen species defence systems by phytic acid accumulation in leaves. Plant Cell Environ 43:2033–53Phosphorus toxicity involves the accumulation of phytic acid, which sequesters metals needed for Cu/Zn-type superoxide dismutase and thus triggers lipid peroxidation.
     [Google Scholar]
  167. 167.
    Teodoro GS, Lambers H, Nascimento DL, de Britto Costa P, Flores-Borges DNA et al. 2019. Specialized roots of Velloziaceae weather quartzite rock while mobilizing phosphorus using carboxylates. Funct. Ecol. 33:762–73
     [Google Scholar]
  168. 168.
    Teste FP, Laliberté E, Lambers H, Auer Y, Kramer S, Kandeler E. 2016. Mycorrhizal fungal biomass and scavenging declines in phosphorus-impoverished soils during ecosystem retrogression. Soil Biol. Biochem. 92:119–32
     [Google Scholar]
  169. 169.
    Thibaud M-C, Arrighi J-F, Bayle V, Chiarenza S, Creff A et al. 2010. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64:775–89
     [Google Scholar]
  170. 170.
    Thomas GW. 1992. In defense of observations and measurements. Soil Sci. Soc. Am. J. 56:1979
     [Google Scholar]
  171. 171.
    Tian Q, Yang L, Ma P, Zhou H, Liu N et al. 2020. Belowground-mediated and phase-dependent processes drive nitrogen-evoked community changes in grasslands. J. Ecol. 108:1874–87N deposition enhances P limitation of grassland productivity, enhancing expression of carboxylate-releasing P-mobilizing strategies, which increase leaf Mn concentrations.
     [Google Scholar]
  172. 172.
    Tivendale ND, Hanson AD, Henry CS, Hegeman AD, Millar AH. 2020. Enzymes as parts in need of replacement—and how to extend their working life. Trends Plant Sci 25:661–69
     [Google Scholar]
  173. 173.
    Tjellström H, Hellgren LI, Wieslander Å, Sandelius AS. 2010. Lipid asymmetry in plant plasma membranes: phosphate deficiency-induced phospholipid replacement is restricted to the cytosolic leaflet. FASEB J 24:1128–38
     [Google Scholar]
  174. 174.
    Treseder KK, Allen MF. 2002. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol 155:507–15
     [Google Scholar]
  175. 175.
    Troll R. 1980. Johann Wolfgang von Goethe: poet-scientist. Am. Biol. Teach. 42:55–60
     [Google Scholar]
  176. 176.
    Turner BL, Hayes PE, Laliberté E. 2018. A climosequence of chronosequences in southwestern Australia. Eur. J. Soil Sci. 69:69–85
     [Google Scholar]
  177. 177.
    Turner BL, Romero TE. 2009. Short-term changes in extractable inorganic nutrients during storage of tropical rain forest soils. Soil Sci. Soc. Am. J. 73:1972–79
     [Google Scholar]
  178. 178.
    Ullrich CI, Novacky AJ. 1990. Extra- and intracellular pH and membrane potential changes induced by K+, Cl−, H2PO4−, and NO3− uptake and fusicoccin in root hairs of Limnobium stoloniferum. Plant Physiol 94:1561–67
     [Google Scholar]
  179. 179.
    Ullrich-Eberius CI, Novacky A, Fischer E, Lüttge U. 1981. Relationship between energy-dependent phosphate uptake and the electrical membrane potential in Lemna gibba G1. Plant Physiol 67:797–801
     [Google Scholar]
  180. 180.
    Ullrich-Eberius CI, Novacky A, Van Bel AJE 1984. Phosphate uptake in Lemna gibba G1: energetics and kinetics. Planta 161:46–52
     [Google Scholar]
  181. 181.
    van't Padje A, Oyarte Galvez L, Klein M, Hink MA, Postma M et al. 2020. Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies. ISME J 15:435–49
     [Google Scholar]
  182. 182.
    Varadachari C, Barman AK, Ghosh K. 1994. Weathering of silicate minerals by organic acids II. Nature of residual products. Geoderma 61:251–68
     [Google Scholar]
  183. 183.
    Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE et al. 2012. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–20
     [Google Scholar]
  184. 184.
    Wen Z, Pang J, Tueux G, Liu Y, Shen J et al. 2020. Contrasting patterns in biomass allocation, root morphology and mycorrhizal symbiosis for phosphorus acquisition among 20 chickpea genotypes differing in amount of rhizosheath carboxylates. Funct. Ecol. 34:1311–24
     [Google Scholar]
  185. 185.
    Wilson DN, Doudna Cate JH. 2012. The structure and function of the eukaryotic ribosome. Cold Spring Harbor Perspect. Biol. 4:a011536
     [Google Scholar]
  186. 186.
    Wolf AM, Baker DE. 1985. Comparisons of soil test phosphorus by Olsen, Bray P1, Mehlich I and Mehlich III methods. Commun. Soil Sci. Plant Anal. 16:467–84
     [Google Scholar]
  187. 187.
    Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z et al. 2004. The worldwide leaf economics spectrum. Nature 428:821–27
     [Google Scholar]
  188. 188.
    Wu P, Ma L, Hou X, Wang M, Wu Y et al. 2003. Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132:1260–71
     [Google Scholar]
  189. 189.
    Xu X, Zhu T, Nikonorova N, De Smet I. 2019. Phosphorylation-mediated signalling in plants. Annual Plant Reviews Online JA Roberts 909–32 Chichester, UK: Wiley & Sons
     [Google Scholar]
  190. 190.
    Yan L, Zhang X, Han Z, Lambers H, Finnegan PM. 2019. Responses of foliar phosphorus fractions to soil age are diverse along a 2 Myr dune chronosequence. New Phytol 223:1621–33
     [Google Scholar]
  191. 191.
    Yan Y, Wan B, Liu F, Tan W, Liu M, Feng X. 2014. Adsorption-desorption of myo-inositol hexakisphosphate on hematite. Soil Sci 179:476–85
     [Google Scholar]
  192. 192.
    Yang S-Y, Huang T-K, Kuo H-F, Chiou T-J. 2017. Role of vacuoles in phosphorus storage and remobilization. J. Exp. Bot. 68:3045–55
     [Google Scholar]
  193. 193.
    Yu R-P, Lambers H, Callaway RM, Wright AJ, Li L 2021. Belowground facilitation and trait matching: two or three to tango?. Trends Plant Sci 26:1227–35
     [Google Scholar]
  194. 194.
    Yu R-P, Li X-X, Xiao Z-H, Lambers H, Li L 2020. Phosphorus facilitation and covariation of root traits in steppe species. New Phytol 226:1285–98
     [Google Scholar]
  195. 195.
    Zemunik G, Turner BL, Lambers H, Laliberté E. 2015. Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat. Plants 1:15050
     [Google Scholar]
  196. 196.
    Zhou Y, Sarker U, Neumann G, Ludewig U. 2019. The LaCEP1 peptide modulates cluster root morphology in Lupinus albus. Physiol. Plant 166:525–37
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-102720-125738
Loading
Phosphorus Acquisition and Utilization in Plants
Annual Review of Plant Biology 73, 17 (2022); https://doi.org/10.1146/annurev-arplant-102720-125738
/content/journals/10.1146/annurev-arplant-102720-125738
/content/journals/10.1146/annurev-arplant-102720-125738
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error