Mulling over the mulla mullas: revisiting phosphorus hyperaccumulation in the Australian plant genus Ptilotus (Amaranthaceae)
Timothy A. Hammer A E , Daihua Ye A B , Jiayin Pang C D , Kevin Foster C D , Hans Lambers A C and Megan H. Ryan C DA School of Biological Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B College of Resources, Sichuan Agricultural University, 211 Huimin Road, Chengdu, Sichuan 611130, China.
C The UWA Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
D School of Agriculture and Environment, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
E Corresponding author: timhammer09@gmail.com.
Australian Journal of Botany 68(1) 63-74 https://doi.org/10.1071/BT19188
Submitted: 2019 Nov 30 Accepted: 2020 Apr 12 Published: 6 May 2020
Abstract
Species in the Australian genus Ptilotus (Amaranthaceae) grow well in soils with both very low and very high phosphorus (P) availability; in the latter they hyperaccumulate P. However, it is not known whether this trait is common within Ptilotus, whether it is shared with other genera in the family, or whether it correlates with the wide array of morphologies and ecologies within Ptilotus. We therefore assessed P hyperaccumulation across the morphological, ecological and phylogenetic diversity of Ptilotus. Experiment 1 tested the response of 11 species to added P (0, 50 and 100 mg kg–1), including six species of Ptilotus and the Australian amaranth Gomphrena canescens R.Br. Experiment 2 tested the response of five species – three Ptilotus spp., G. canescens and Kennedia prostrata R.Br. – to added P (5 and 150 mg kg–1) and two pre-harvest P-pulse treatments (5 and 50 mg kg–1). Ptilotus species hyperaccumulated P when grown in high-P soil, but curtailed uptake from a pulse. All Ptilotus species preferentially allocated P to leaves (reaching 73 mg g–1) without development of P toxicity symptoms. Gomphrena canescens and K. prostrata preferentially allocated P to stems and roots, respectively, and suffered P toxicity. The lack of tolerance to high [P] in G. canescens suggests that the likely widespread, or universal, mechanisms for tolerance of high P by Ptilotus are not shared by amaranths. Further research will determine the mechanisms underlying the unusual P physiology of Ptilotus.
Additional keywords: adaptations, plant physiology, plant nutrient acquisition.
References
Alvarez-Manjarrez J, Garibay-Orijel R, Smith ME (2018) Caryophyllales are the main hosts of a unique set of ectomycorrhizal fungi in a Neotropical dry forest. Mycorrhiza 28, 103–115.| Caryophyllales are the main hosts of a unique set of ectomycorrhizal fungi in a Neotropical dry forest.Crossref | GoogleScholarGoogle Scholar | 29181635PubMed |
Aziz T, Lambers H, Nicol D, Ryan MH (2015) Mechanisms for tolerance of very high tissue phosphorus concentrations in Ptilotus polystachyus. Plant, Cell & Environment 38, 790–799.
| Mechanisms for tolerance of very high tissue phosphorus concentrations in Ptilotus polystachyus.Crossref | GoogleScholarGoogle Scholar |
Bolan NM (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant and Soil 134, 189–207.
| A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants.Crossref | GoogleScholarGoogle Scholar |
Boltz DF, Lueck CH (1958) Phosphorus. In ‘Colorimetric determination of non-metals’. (Ed. DF Boltz) pp. 29–46. (Interscience: New York, USA)
Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytologist 154, 275–304.
| Coevolution of roots and mycorrhizas of land plants.Crossref | GoogleScholarGoogle Scholar |
Butterly CR, McNeill AM, Baldock JA, Marschner P (2010) Rapid changes in carbon and phosphorus after rewetting of dry soil. Biology and Fertility of Soils 47, 41–50.
| Rapid changes in carbon and phosphorus after rewetting of dry soil.Crossref | GoogleScholarGoogle Scholar |
Fixen PE, Johnston AM (2012) World fertilizer nutrient reserves: a view to the future. Journal of the Science of Food and Agriculture 92, 1001–1005.
| World fertilizer nutrient reserves: a view to the future.Crossref | GoogleScholarGoogle Scholar | 22415449PubMed |
Gordon H, Haygarth PM, Bardgett RD (2008) Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biology & Biochemistry 40, 302–311.
| Drying and rewetting effects on soil microbial community composition and nutrient leaching.Crossref | GoogleScholarGoogle Scholar |
Hammer T, Davis R, Thiele K (2015) A molecular framework phylogeny for Ptilotus (Amaranthaceae): evidence for the rapid diversification of an arid Australian genus. Taxon 64, 272–285.
| A molecular framework phylogeny for Ptilotus (Amaranthaceae): evidence for the rapid diversification of an arid Australian genus.Crossref | GoogleScholarGoogle Scholar |
Hammer TA, Davis RW, Thiele KR (2018a) A key to Ptilotus (Amaranthaceae) in Western Australia. Nuytsia 29, 217–227.
Hammer TA, Macintyre PD, Nge FJ, Davis RW, Mucina L, Thiele KR (2018b) The noble and the exalted: a multidisciplinary approach to resolving a taxonomic controversy within Ptilotus (Amaranthaceae). Australian Systematic Botany 31, 262–280.
| The noble and the exalted: a multidisciplinary approach to resolving a taxonomic controversy within Ptilotus (Amaranthaceae).Crossref | GoogleScholarGoogle Scholar |
Hammer TA, Zhong X, Colas des Francs-Small C, Nevill PG, Small ID, Thiele KR (2019) Resolving intergeneric relationships in the aervoid clade and the backbone of Ptilotus (Amaranthaceae): evidence from whole plastid genomes and morphology. Taxon 68, 297–314.
| Resolving intergeneric relationships in the aervoid clade and the backbone of Ptilotus (Amaranthaceae): evidence from whole plastid genomes and morphology.Crossref | GoogleScholarGoogle Scholar |
Haug I, Weiß M, Homeier J, Oberwinkler F, Kottke I (2005) Russulaceae and Thelephoraceae form ectomycorrhizas with members of the Nyctaginaceae (Caryophyllales) in the tropical mountain rain forest of southern Ecuador. New Phytologist 165, 923–936.
| Russulaceae and Thelephoraceae form ectomycorrhizas with members of the Nyctaginaceae (Caryophyllales) in the tropical mountain rain forest of southern Ecuador.Crossref | GoogleScholarGoogle Scholar | 15720703PubMed |
Hopper SD (2009) OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil 322, 49–86.
| OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes.Crossref | GoogleScholarGoogle Scholar |
Islam M, Turner DM, Adams MA (1999) Phosphorus availability and the growth, mineral composition and nutritive value of ephemeral forbs and associated perennials from the Pilbara, Western Australia. Australian Journal of Experimental Agriculture 39, 149–159.
| Phosphorus availability and the growth, mineral composition and nutritive value of ephemeral forbs and associated perennials from the Pilbara, Western Australia.Crossref | GoogleScholarGoogle Scholar |
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473, 97–100.
| Ancestral polyploidy in seed plants and angiosperms.Crossref | GoogleScholarGoogle Scholar | 21478875PubMed |
Johnston AE, Poulton PR, Fixen PE, Curtin D (2014) Phosphorus: its efficient use in agriculture. Advances in Agronomy 123, 177–228.
| Phosphorus: its efficient use in agriculture.Crossref | GoogleScholarGoogle Scholar |
Kariman K, Barker SJ, Jost R, Finnegan PM, Tibbett M (2016) Sensitivity of jarrah (Eucalyptus marginata) to phosphate, phosphite, and arsenate pulses as influenced by fungal symbiotic associations. Mycorrhiza 26, 401–415.
| Sensitivity of jarrah (Eucalyptus marginata) to phosphate, phosphite, and arsenate pulses as influenced by fungal symbiotic associations.Crossref | GoogleScholarGoogle Scholar | 26810895PubMed |
Khan AG (1974) The occurrence of mycorrhizas in halophytes, hydrophytes and xerophytes, and of Endogone spores in adjacent soils. Microbiology 81, 7–14.
| The occurrence of mycorrhizas in halophytes, hydrophytes and xerophytes, and of Endogone spores in adjacent soils.Crossref | GoogleScholarGoogle Scholar |
Kooyman RM, Laffan SW, Westoby M (2017) The incidence of low phosphorus soils in Australia. Plant and Soil 412, 143–150.
| The incidence of low phosphorus soils in Australia.Crossref | GoogleScholarGoogle Scholar |
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98, 693–713.
| Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits.Crossref | GoogleScholarGoogle Scholar | 16769731PubMed |
Lambers H, Brundrett MC, Raven JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant and Soil 334, 11–31.
| Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies.Crossref | GoogleScholarGoogle Scholar |
Lodge D, McDowell W, McSwiney C (1994) The importance of nutrient pulses in tropical forests. Trends in Ecology & Evolution 9, 384–387.
| The importance of nutrient pulses in tropical forests.Crossref | GoogleScholarGoogle Scholar |
Nazeri NK, Lambers H, Tibbett M, Ryan MH (2014) Moderating mycorrhizas: arbuscular mycorrhizas modify rhizosphere chemistry and maintain plant phosphorus status within narrow boundaries. Plant, Cell & Environment 37, 911–921.
| Moderating mycorrhizas: arbuscular mycorrhizas modify rhizosphere chemistry and maintain plant phosphorus status within narrow boundaries.Crossref | GoogleScholarGoogle Scholar |
Northcote KH (1979) ‘A factual key for the recognition of Australian soils.’ (Rellim Technical Publications: Coffs Harbour, NSW, Australia)
Oliveira RS, Galvão HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2014) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytologist 205, 1183–1194.
| Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types.Crossref | GoogleScholarGoogle Scholar | 25425486PubMed |
Orians GH, Milewski AV (2007) Ecology of Australia: the effects of nutrient‐poor soils and intense fires. Biological Reviews of the Cambridge Philosophical Society 82, 393–423.
| Ecology of Australia: the effects of nutrient‐poor soils and intense fires.Crossref | GoogleScholarGoogle Scholar | 17624961PubMed |
Pang J, Ryan MH, Tibbett M, Cawthray GR, Siddique KHM, Bolland MDA, Denton MD, Lambers H (2010) Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply. Plant and Soil 331, 241–255.
| Variation in morphological and physiological parameters in herbaceous perennial legumes in response to phosphorus supply.Crossref | GoogleScholarGoogle Scholar |
Ramsey J (2011) Polyploidy and ecological adaptation in wild yarrow. Proceedings of the National Academy of Sciences of the United States of America 108, 7096–7101.
| Polyploidy and ecological adaptation in wild yarrow.Crossref | GoogleScholarGoogle Scholar | 21402904PubMed |
Rayment GE, Lyons D (2011) ‘Soil chemical methods – Australasia.’ (CSIRO Publishing: Melbourne, Vic., Australia)
Ryan MH, Ehrenberg S, Bennett RG, Tibbett M (2009) Putting the P in Ptilotus: a phosphorus-accumulating herb native to Australia. Annals of Botany 103, 901–911.
| Putting the P in Ptilotus: a phosphorus-accumulating herb native to Australia.Crossref | GoogleScholarGoogle Scholar | 19213796PubMed |
Ryan MH, Kaur P, Nazeri NK, Clode PL, Keeble-Gagnère G, Doolette AL, Smernik RJ, Van Aken O, Nicol D, Maruyama H, Ezawa T, Lambers H, Millar AH, Appels R (2019) Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition: P accumulation in globular structures in roots. Plant, Cell & Environment 42, 1987–2002.
| Globular structures in roots accumulate phosphorus to extremely high concentrations following phosphorus addition: P accumulation in globular structures in roots.Crossref | GoogleScholarGoogle Scholar |
Schnitzler J, Barraclough TG, Boatwright JS, Goldblatt P, Manning JC, Powell MP, Rebelo T, Savolainen V (2011) Causes of plant diversification in the Cape biodiversity hotspot of South Africa. Systematic Biology 60, 343–357.
| Causes of plant diversification in the Cape biodiversity hotspot of South Africa.Crossref | GoogleScholarGoogle Scholar | 21362644PubMed |
Searle PL (1984) The berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. A review. Analyst (London) 109, 549–568.
| The berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. A review.Crossref | GoogleScholarGoogle 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’. Journal of Experimental Botany 57, 413–423.
| 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’.Crossref | GoogleScholarGoogle Scholar | 16356944PubMed |
Shane MW, McCully ME, Lambers H (2004) Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae). Journal of Experimental Botany 55, 1033–1044.
| Tissue and cellular phosphorus storage during development of phosphorus toxicity in Hakea prostrata (Proteaceae).Crossref | GoogleScholarGoogle Scholar | 15047760PubMed |
Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, Zheng C, Sankoff D, Depamphilis CW, Wall PK, Soltis PS (2009) Polyploidy and angiosperm diversification. American Journal of Botany 96, 336–348.
| Polyploidy and angiosperm diversification.Crossref | GoogleScholarGoogle Scholar | 21628192PubMed |
Stewart DA, Barlow BA (1976) Infraspecific polyploidy and gynodioecism in Ptilotus obovatus (Amaranthaceae). Australian Journal of Botany 24, 237–248.
| Infraspecific polyploidy and gynodioecism in Ptilotus obovatus (Amaranthaceae).Crossref | GoogleScholarGoogle Scholar |
Suriyagoda LDB, Lambers H, Renton M, Ryan MH (2012) Growth, carboxylate exudates and nutrient dynamics in three herbaceous perennial plant species under low, moderate and high phosphorus supply. Plant and Soil 358, 105–117.
| Growth, carboxylate exudates and nutrient dynamics in three herbaceous perennial plant species under low, moderate and high phosphorus supply.Crossref | GoogleScholarGoogle Scholar |
Suriyagoda LDB, Tibbett M, Edmonds-Tibbet T, Cawthray GR, Ryan MH (2015) Poor regulation of phosphorus uptake and rhizosphere carboxylates in three phosphorus-hyperaccumulating species of Ptilotus. Plant and Soil 402, 145–158.
| Poor regulation of phosphorus uptake and rhizosphere carboxylates in three phosphorus-hyperaccumulating species of Ptilotus.Crossref | GoogleScholarGoogle Scholar |
Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE, Hinchliff CE, Brown JW, Sessa EB, Harmon LJ (2015) Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytologist 207, 454–467.
| Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications.Crossref | GoogleScholarGoogle Scholar | 26053261PubMed |
te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubesová M, Pysek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany 109, 19–45.
| The more the better? The role of polyploidy in facilitating plant invasions.Crossref | GoogleScholarGoogle Scholar | 22040744PubMed |
Tsakalos JL, Renton M, Dobrowolski MP, Feoli E, Macintyre PD, Veneklaas EJ, Mucina L (2018) Community patterns and environmental drivers in hyper-diverse kwongan scrub vegetation of Western Australia. Applied Vegetation Science 21, 694–722.
| Community patterns and environmental drivers in hyper-diverse kwongan scrub vegetation of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nature Reviews. Genetics 18, 411–424.
| The evolutionary significance of polyploidy.Crossref | GoogleScholarGoogle Scholar | 28502977PubMed |
van de Wiel CCM, van der Linden CG, Scholten OE (2016) Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207, 1–22.
| Improving phosphorus use efficiency in agriculture: opportunities for breeding.Crossref | GoogleScholarGoogle Scholar |
Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist 195, 306–320.
| Opportunities for improving phosphorus-use efficiency in crop plants.Crossref | GoogleScholarGoogle Scholar | 22691045PubMed |
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37, 29–38.
| An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method.Crossref | GoogleScholarGoogle Scholar |
Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363.
| Phylogenetic distribution and evolution of mycorrhizas in land plants.Crossref | GoogleScholarGoogle Scholar | 16845554PubMed |
Williams RR, Holliday KC, Bennell MR (1989) Cultivation of the pink mulla mulla, Ptilotus exaltatus Nees. 1. Seed germination and dormancy. Scientia Horticulturae 40, 267–274.
| Cultivation of the pink mulla mulla, Ptilotus exaltatus Nees. 1. Seed germination and dormancy.Crossref | GoogleScholarGoogle Scholar |
Wright SR, Jennette MW, Coble HD, Rufty TW (1999) Root morphology of young Glycine max, Senna obtusifolia, and Amaranthus palmeri. Weed Science 47, 706–711.
| Root morphology of young Glycine max, Senna obtusifolia, and Amaranthus palmeri.Crossref | GoogleScholarGoogle Scholar |
Yang S, Huang T, Kou H, Chiou T (2017) Role of vacuoles in phosphorus storage and remobilization. Journal of Experimental Botany 68, 3045–3055.
| Role of vacuoles in phosphorus storage and remobilization.Crossref | GoogleScholarGoogle Scholar | 28077447PubMed |
Ye D, Li T, Zheng Z, Zhang X, Yu H (2018) P uptake characteristics and root morphological responses in the mining ecotype of Polygonum hydropiper under high organic P media. International Journal of Phytoremediation 20, 608–615.
| P uptake characteristics and root morphological responses in the mining ecotype of Polygonum hydropiper under high organic P media.Crossref | GoogleScholarGoogle Scholar | 29688058PubMed |
Zobel RW, Kinraide TB, Baligar VC (2007) Fine root diameters can change in response to changes in nutrient concentrations. Plant and Soil 297, 243–254.
| Fine root diameters can change in response to changes in nutrient concentrations.Crossref | GoogleScholarGoogle Scholar |