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Contrasting phosphorus sensitivity of two Australian native monocots adapted to different habitats

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Abstract

Aims

Contrasting nutrient-acquisition strategies would explain why species differ in their distribution in relation to soil phosphorus (P) availability, promoting diversity. However, what drives the differential distribution of plant species with the same P-acquisition strategy remains poorly understood.

Methods

We selected two Haemodoraceae species, Anigozanthos flavidus and Macropidia fuliginosa, to investigate physiological responses in non-mycorrhizal monocots adapted to different edaphic habitats that vary in P availability. Plants were grown in nutrient solution in large tanks at a range of P concentrations (0, 0.1, 1, 10 µM P). After seven months, we measured growth, photosynthetic rate, net P-uptake capacity, and leaf [P].

Results

Fresh weights of A. flavidus plants were highest at 1 µM P and lowest at 0 µM P. Fresh weights of M. fuliginosa plants were lowest at 10 µM P compared with those at other P levels. Rates of P uptake by A. flavidus showed a steady decline with increasing P level during growth from 0 to 1 µM P, and then a sharp decline from 1 to 10 µM P. Rates of P uptake in M. fuliginosa did not differ among growth P levels, except between 0 and 1 µM P. Both species showed a drastic increase in the concentration of both total P and inorganic P at 10 µM P.

Conclusions

The results support our hypothesis that A. flavidus is efficient in down-regulating its P-uptake capacity, while M. fuliginosa is not. Thus, partly explaining the narrower and wider distribution of these species.

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Data availability

Data will be archived in Dryad upon paper acceptance.

References

  • Abrahão A, Lambers H, Sawaya A, Mazzafera P, Oliveira RS (2014) Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176:345–355

    Article  PubMed  Google Scholar 

  • Brundrett MC, Abbott LK (1991) Roots of jarrah forest plants. I. Mycorrhizal associations of shrubs and herbaceous plants. Aust J Bot 39:445–457

    Article  Google Scholar 

  • Cakmak I, Marschner H (1987) Mechanism of phosphorus-induced zinc deficiency in cotton. III. Changes in physiological availability of zinc in plants Is mail. Physiol Plant 70:13–20

    Article  CAS  Google Scholar 

  • Conn S, Gilliham M (2010) Comparative physiology of elemental distributions in plants. Ann Bot-London 105:1081–1102

    Article  CAS  Google Scholar 

  • Cowling RM, Witkowski ETF, Milewski AV, Newbey KR (1994) Taxonomic, edaphic and biological aspects of narrow plant endemism on matched sites in mediterranean South Africa and Australia. J Biogeogr 21:651–664

    Article  Google Scholar 

  • 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-London 111:445–454

    Article  CAS  Google Scholar 

  • Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107:207–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Epstein AJ, Bloom E (2005) Mineral nutrition of plants: Principles and perspectives, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Gao J, Wang F, Ranathunge K, Arruda AJ, Cawthray GR, Clode PL, He X, Leopold M, Roessner U, Rupasinghe T et al (2020) Edaphic niche characterization of four Proteaceae reveals unique calcicole physiology linked to hyper‐endemism of Grevillea thelemanniana. New Phytol 228: 869-883

  • Groves RH, Keraitis K (1976) Survival and growth of seedlings of three sclerophyll species at high levels of phosphorus and nitrogen. Aust J Bot 24:681–690

    Article  Google Scholar 

  • Grundon NJ (1972) Mineral nutrition of some Queensland heath plants. J Ecol 60:171–181

    Article  CAS  Google Scholar 

  • Handreck KA (1997a) Phosphorus requirements of Australian native plants. Soil Res 35:241–290

    Article  Google Scholar 

  • Handreck K (1997b) Phosphorus needs of some Australian plants. Society for Growing Australian. http://anpsa.org.au/APOL8/dec97-4.html

  • 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 Hortic-Amsterdam 117:357–365

    Article  CAS  Google Scholar 

  • Hayes P, 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

    Article  CAS  Google Scholar 

  • Hayes PE, Clode PL, Guilherme Pereira C, Lambers H (2019a) Calcium modulates leaf cell-specific phosphorus allocation in Proteaceae from south-western Australia. J Exp Bot 70:3995–4009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes PE, Guilherme Pereira C, Clode PL, Lambers H (2019b) Calcium-enhanced phosphorus toxicity in calcifuge and soil‐indifferent Proteaceae along the Jurien Bay chronosequence. New Phytol 221:764–777

    Article  CAS  PubMed  Google Scholar 

  • Hopper S (1993) Kangaroo paws and catspaws: a natural history and field guide. Department of Conservation and Land Management, Perth

    Google Scholar 

  • Hopper SD, Campbell NA (1977) A multivariate morphometric study of species relationships in kangaroo paws (Anigozanthos Labill. and Macropidia Drumm. ex. Harv.: Haemodoraceae). Aust J Bot 25:523–544

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P, Heiberger RM (2012) Multcomp: simultaneous inference for general linear hypotheses. R package version, 1.2–13. Retrieved from http://CRAN.R-project.org/package=multcomp

  • Hulshof CM, Spasojevic MJ (2020) The edaphic control of plant diversity. Global Ecol Biogeogr 29:1634–1650

    Article  Google Scholar 

  • Irving GCJ, Bouma D (1984) Phosphorus compounds measured in a rapid and simple leaf test for the assessment of the phosphorus status of subterranean clover. Aust J Exp Agr 24:213–218

    Article  Google Scholar 

  • Lambers H (2014) Plant life on the sandplains in southwest Australia: a global biodiversity hotspot. University of Western Australia Publishing, Crawley

    Google Scholar 

  • Lambers H, Oliveira RS (2019) Plant physiological ecology, 3rd edn. Springer, Cham. https://doi.org/10.1007/978-3-030-29639-1

  • Lambers H, Plaxton WC (2015) "Phosphorus: back to the roots. In ‘Annual plant reviews. Vol. 48: Phosphorus metabolism in plants’." (2015): 3-22

  • Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261

    Article  CAS  Google Scholar 

  • Lambers H, Raven J, Shaver G, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    Article  PubMed  Google Scholar 

  • Lambers H, Brundrett M, Raven J, Hopper S (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 348:1–2

    Google Scholar 

  • Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible W, Stitt M, Teste F, Turner BL (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 196:1098–1108

    Article  CAS  PubMed  Google Scholar 

  • Lambers H, Clode PL, Hawkins H, Laliberté E, Oliveira RS, Reddell P, Shane MW, Stitt M, Weston P (2015) Metabolic adaptations of the non-mycotrophic Proteaceae to soils with low phosphorus availability. Annu Plant Rev Online 48:289–335

    CAS  Google Scholar 

  • Latimer AM, Silander JA, Cowling RM (2005) Neutral ecological theory reveals isolation and rapid speciation in a biodiversity hot spot. Science 309:1722–1725

    Article  CAS  PubMed  Google Scholar 

  • Lazarina M, Kallimanis AS, Dimopoulos P, Psaralexi M, Michailidou D-E, Sgardelis SP (2019) Patterns and drivers of species richness and turnover of neo-endemic and palaeo-endemic vascular plants in a Mediterranean hotspot: the case of Crete, Greece. J Biol Res-Thessaloniki 26:12

    Article  Google Scholar 

  • Leopold M, Zhong H (2019) The soils of the Alison Baird Reserve. In: Lambers H (ed) A jewel in the crown of a global biodiversity hotspot. Kwongan Foundation and the Western Australian Naturalists’ Club Inc, Perth, pp 49–57

    Google Scholar 

  • Marschner P (ed) (2012) Marschner’s mineral nutrition of higher plants, 3rd edn. Academic, London

  • Motomizu S, Wakimoto T, Tôei K (1983) Spectrophotometric determination of phosphate in river waters with molybdate and malachite green. Analyst 108:361–367

    Article  CAS  Google Scholar 

  • Mustart PJ, Cowling RM (1993) The role of regeneration stages in the distribution of edaphically restricted fynbos Proteaceae. Ecology 74:1490–1499

    Article  Google Scholar 

  • Myers N, Mittermeier R, Mittermeier C (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Oliveira RS, Galvão HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol 205:1183–1194

    Article  CAS  PubMed  Google Scholar 

  • Ozanne PG, Specht RL (1981) Mineral nutrition of heathlands: phosphorus toxicity. Ecosyst World 9:209–213

    Google Scholar 

  • Pandey CB, Srivastava RC (2009) Plant available phosphorus in homegarden and native forest soils under high rainfall in an equatorial humid tropics. Plant Soil 316:71–80

    Article  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2018) R Core Team (2017) Nlme: linear and nonlinear mixed effects models. R package version 3.1–131. Retrieved from https://cran.r-project.org/web/packages/nlme/nlme.pdf

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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 57:413–423

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shane MW, Cramer MD, Lambers H (2008) Root of edaphically controlled Proteaceae turnover on the Agulhas Plain, South Africa: phosphate uptake regulation and growth. Plant Cell Environ 31:1825–1833

    Article  CAS  PubMed  Google Scholar 

  • Smith RJ, Hopper SD, Shane MW (2011) Sand-binding roots in Haemodoraceae: global survey and morphology in a phylogenetic context. Plant Soil 348:453

    Article  CAS  Google Scholar 

  • Specht RL (1963) Dark Island heath (Ninety-Mile Plain, South Australia). VII. The effect of fertilizers on composition and growth, 1950-60. Aust J Bot 11:67–94

    Article  Google Scholar 

  • Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of P roteaceae species. Plant Cell Environ 37:1276–1298

    Article  CAS  PubMed  Google Scholar 

  • Takagi D, Miyagi A, Tazoe Y, Suganami M, Kawai-Yamada M, Ueda A, Suzuki Y, Noguchi K, Hirotsu N, Makino A (2020) Phosphorus toxicity disrupts Rubisco activation and reactive oxygen species defence systems by phytic acid accumulation in leaves. Plant Cell Environ 43: 2033–2053. https://doi.org/10.1111/pce.13772

  • Willis CK, Cowling RM, Lombard AT (1996) Patterns of endemism in the limestone flora of South African lowland fynbos. Biodivers Conserv 5:55–73

    Article  Google Scholar 

  • Zemunik G, Turner BL, Lambers H, Laliberté E, Coomes DA (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:15050

    Article  CAS  Google Scholar 

  • Zemunik G, Turner BL, Lambers H, Laliberté E (2016) Increasing plant species diversity and extreme species turnover accompany declining soil fertility along a long-term chronosequence in a biodiversity hotspot. J Ecol 104:792–805

    Article  Google Scholar 

  • Zhong H, Zhou J, Azmi A, Arruda AJ, Doolette AL, Smernik RJ, Lambers H (2020) Xylomelum occidentale (Proteaceae) accesses relatively mobile soil organic phosphorus without releasing carboxylates. J Ecol 00: 1– 14. https://doi.org/10.1111/1365-2745.13468

  • Zuur AF, Leno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer Science & Business Media

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Acknowledgements

This work was supported by grant DP0663243 from the Australian Research Council (ARC) to MWS, an ARC Postdoctoral Fellow. We would like to thank Dr Patrick Hayes for helpful comments on the manuscript.

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Authors and Affiliations

  1. School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA, 6009, Australia

    Felipe E. Albornoz, Michael W. Shane & Hans Lambers

Authors
  1. Felipe E. Albornoz
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  2. Michael W. Shane
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  3. Hans Lambers
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Contributions

MWS conducted the experiment and collected data. FEA analysed data and, together with HL, wrote the manuscript.

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Correspondence to Felipe E. Albornoz.

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All authors, with the exception of Dr Shane, who passed away, state that they do not have any conflict of interest in the submission of this manuscript.

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Michael W. Shane is deceased

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Albornoz, F.E., Shane, M.W. & Lambers, H. Contrasting phosphorus sensitivity of two Australian native monocots adapted to different habitats. Plant Soil 461, 151–162 (2021). https://doi.org/10.1007/s11104-020-04760-5

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