Abstract
Background and aims
The genus Denhamia(Celastraceae) includes fifteen Australian species, many of which have a propensity for manganese (Mn) (hyper)accumulation. Among the key aims of this study were to: i) elucidate Mn accumulation in D. bilocularis, D. celastroides, D. pittosporoides and D. silvestris under controlled conditions; ii) examine the in situ distributions of Mn and other elements in tissues of i) above, and also in two other species growing in their natural habitat, i.e. D. silvestris and D. cunninghamii; iii) test numerous Denhamia herbarium specimens for Mn accumulation using portable X-ray fluorescence spectroscopy (XRF).
Methods
Portable XRF and laboratory micro-XRF were used to examine Mn accumulation and foliar distribution patterns in several Australian Denhamia species. These techniques were variously applied to fresh field material and experimentally-raised plants treated with Mn (250 μg g−1, 500 μg g−1 and 1000 μg g−1) and dry herbarium material.
Results
The findings revealed D. bilocularis as a new Mn hyperaccumulator, with foliar Mn concentrations of up to 15,300 μg g−1 in herbarium samples, and 13,700 μg g−1 in experimentally grown plants. Laboratory μXRF maps consistently showed that foliar Mn accumulation was localized at the extremities of wild D. cunninghamii and D. silvestris leaves; whereas it was found in the vasculature of experimentally grown D. bilocularis and D. pittosporoides leaves.
Conclusions
This study presents evidence that Mn accumulation across the Australian Denhamia species is taxonomically variable, however further work is required.
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References
Abubakari F, Nkrumah PN, Fernando DR, Brown GK, Erskine PD, Echevarria G, van der Ent A (2020) Incidence of hyperaccumulation and tissue-level distribution of manganese, cobalt and zinc in the genus Gossia (Myrtaceae). Metallomics. In Press. https://doi.org/10.1093/mtomcs/mfab008
Alvarez-Tinaut MC, Leal A, Martínez LR (1980)Iron-manganese interaction and its relation to boron levels in tomato plants. Plant Soil 55:377–388
APC - Australian Plant Census (2020) Accessed online: https://biodiversity.org.au/nsl/services/search?product=APC&tree.id=51209179&name=Denhamia&inc._scientific=&inc.scientific=on&inc._cultivar=&max=100&display=apc&search=true
Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126
Becquer T, Bourdon E, Pétard J (1995) Disponibilité du nickel le long d'une toposéquence de sols développés sur roches ultramafiques de Nouvelle-Calédonie. Comptes Rendus de l'Académie des Sciences Série 2a 321:585–592
Bidwell SD, Woodrow IE, Batianoff GN, Sommer-Knudsen J (2002) Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii(Myrtaceae) from Queensland, Australia. Funct Plant Biol 29:899–905
Boyd R, Martens S (1992) The raison d’être for metal hyperaccumulation by plants. In: The vegetation of ultramafic (serpentine) soils Baker, AJM, Proctor, J, and Reeves, RD, Eds, Intercept Ltd, Andover pp. 279–289
Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of nutrients: micronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Academic Press, San Diego, pp 212–223
Brooks RR, Trow JM, Veillon JM, Jaffré T (1981) Studies on manganese-accumulatingAlyxia species from New Caledonia. Taxon:420–423
Chen RF, Shen RF, Gu P, Wang HY, Xu XH (2008) Investigation of aluminum-tolerant species in acid soils of South China. Comm Soil Sci Plant Anal 39(9–10):1493–1506
Clair SBS, Lynch JP (2004) Photosynthetic and antioxidant enzyme responses of sugar maple and red maple seedlings to excess manganese in contrasting light environments. Funct Plant Biol 31:1005–1014
Clair SBS, Carlson JE, Lynch JP (2005) Evidence for oxidative stress in sugar maple stands growing on acidic, nutrient imbalanced forest soils. Oecologia 145:257–268
Clarkson DT (1988) The uptake and translocation of manganese by plant roots. In: Graham RD, Hannam RJ, Uren NJ (eds) Manganese in soil and plants. Kluwer Academic Publishers, Dordrecht, pp 101–111
Corso M, Schvartzman MS, Guzzo F, Souard F, Malkowski E, Hanikenne M, Verbruggen N (2018) Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri. New Phytol 218:283–297
DeGroote KV, McCartha GL, Pollard AJ (2018) Interactions of the manganese hyperaccumulator Phytolacca americana L. with soil pH and phosphate. Ecol Res 33:749–755
Dou CM, Fu XP, Chen XC, Shi JY, Chen YX (2009) Accumulation and detoxification of manganese in hyperaccumulator Phytolacca americana. Plant Biol 11:664–670
Fernando DR, Lynch JP (2015) Manganese phytotoxicity: new light on an old problem. Ann Bot 116:313–319
Fernando DR, Bakkaus EJ, Perrier N, Baker AJM, Woodrow IE, Batianoff GN, Collins RN (2006a) Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytol 171:751–758
Fernando DR, Batianoff GN, Baker AJM, Woodrow IE (2006b) In vivo localization of manganese in the hyperaccumulator Gossia bidwillii (Benth.) N. Snow & Guymer (Myrtaceae) by cryo-SEM/EDAX. Plant Cell Environ 29:1012–1020
Fernando DR, Marshall AT, Gouget B, Carrière M, Collins RN, Woodrow IE, Baker AJM (2008a) Novel pattern of foliar metal distribution in a manganese hyperaccumulator. Funct Plant Biol 35:193–200
Fernando DR, Woodrow IE, Jaffré T, Dumontet V, Marshall AT, Baker AJM (2008b) Foliar manganese accumulation by Maytenus founieri(Celastraceae) in its native new Caledonian habitats: populational variation and localization by X-ray microanalysis. New Phytol 177:178–185
Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJM, Batianoff GN (2009a) Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy. Ann Bot 103:931–939
Fernando D, Baker A, Woodrow I (2009b) Physiological responses in Macadamia integrifolia on exposure to manganese treatment. Aust J Bot 57:406–413
Fernando DR, Marshall AT, Forster PI, Hoebee SE, Siegele R (2013) Multiple metal accumulation within a manganese-specific genus. Am J Bot 100:690–700
Fernando DR, Smith CS, Steinbauer MJ, Farnier K, Watson SJ, Green PT (2018) Does foliage metal accumulation influence plant–insect interactions? A field study of two sympatric tree metallophytes. Funct Plant Biol 45:945–956
Foy CD, Chaney RL, White MC (1978) The physiology of metal toxicity in plants. Ann Rev Plant Physio 29:511–566
Foulds W (2003) Nutrient concentrations of foliage and soil in South‐western Australia. New Phytologist 125: 529-546
Gei V, Isnard S, Erskine PD, Echevarria G, Fogliani B, Jaffré T, van der Ent A (2020) A systematic assessment of the occurrence of trace element hyperaccumulation in the flora of New Caledonia. Bot J Linn Soc 194:1–22
González A, Steffen KL, Lynch JP (1998) Light and excess manganese: implications for oxidative stress in common bean. Plant Physiol 118:493–504
Graham RD, Hannam RJ, Uren NC eds (1988) Manganese in soils and plants: proceedings of the international symposium on ‘manganese in soils and plants’ held at the Waite Agricultural Research Institute, The University of Adelaide, Glen Osmond, South Australia, August 22–26, as an Australian bicentennial event. Springer Science & Business Media
Halford JJ, Jessup LW (2020)Denhamia megacarpa J.J. Halford & Jessup and D. peninsularis J.J. Halford & Jessup (Celastraceae), two new species from Queensland. Austrobaileya 10(4):594–603
He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140
Ingwersen J, Streck T (2005) A regional-scale study on the crop uptake of cadmium from sandy soils. J Environ Qual 34:1026–1035
Jaffré T (1977) Accumulation du manganèse par des especes associées aux terrains ultrabasiques de Nouvelle-Calédonie. Cr Acad Sci Paris, D 284:1573–1575
Jaffré T (1979) Accumulation du manganèse par les Protéacées de Nouvelle Calédonie. Comptes Rendus de l'Académie des Sciences Série D: Sciences Naturelles 289:425–428
Jaffré T (1980) Étude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle Calédonie. Paris: Travaux et Documents de l'ORSTOM 124
Jiang WZ (2006) Mn use efficiency in different wheat cultivars. Environ Exp Bot 57:41–50
Jones MW, Kopittke PM, Casey L, Reinhardt J, Blamey FP, van der Ent A (2019) Assessing radiation dose limits for X-ray fluorescence microscopy analysis of plant specimens. Ann Bot 13 125(4):599–610
Kabata-Pendias A (2010) Trace elements in soils and plants. CRC Press
Kukier U, Chaney RL (2001) Amelioration of nickel phytotoxicity in muck and mineral soils. J Environ Qual 30:1949–1960
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428
Marschner H (2002) Mineral nutrition of higher plants. Academic Press, London
Marschner H (2011) Marschner's mineral nutrition of higher plants. Academic Press, London
McKenna MJ, Simmons MP, Bacon CD, Lombardi JA (2011) Delimitation of the segregate genera of Maytenus sl. (Celastraceae) based on morphological and molecular characters. Syst Bot 36(4):92–932
McLay T, Holmes GD, Forster PI, Hoebee SE, Fernando DR (2019) Phylogeny, biogeography and foliar manganese accumulation of Gossia (Myrtaceae). Aust Syst Bot 31:374–388
Meier SK, Adams N, Wolf M, Balkwill K, Muasya AM, Gehring CA, Bishop JM, Ingle RA (2018) Comparative RNA-seq analysis of nickel hyperaccumulating and non-accumulating populations of Senecio coronatus (Asteraceae). Plant J 95:1023–1038
Millaleo R, Reyes-Díaz M, Ivanov A, Mora M, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10:470–481
Nable R, Bar-Akiva A, Loneragan J (1984) Functional manganese requirement and its use as a critical value for diagnosis of manganese deficiency in subterranean clover (Trifolium subterraneum L. cv. Seaton Park). Ann Bot 54:39–49
Perronnet K, Schwartz C, Morel JL (2003) Distribution of cadmium and zinc in the hyperaccumulator Thlaspi caerulescens grown on multicontaminated soil. Plant Soil 249(1):19–25
Pittman JK (2005) Managing the manganese: molecular mechanisms of manganese transport and homeostasis. New Phytol 167:733–742
PlantNET. The Plant Information Network System of The Royal Botanic Gardens and DomainTrust, http://plantnet.rbgsyd.nsw.gov.au
Pollard AJ, Powell KD, Harper FA, JAC S (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566
Proctor J (2003) Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East. Perspect Plant Ecol Evol Syst 6:105–124
Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249:57–65
Reeves RD, Baker AJ, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218:407–411
Salt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109:1427–1433
Schmidt SB, Jensen PE, Husted S (2016) Manganese deficiency in plants: the impact on photosystem II. Trends Plant Sci 21:622–632
Schvartzman MS, Corso M, Fataftah N, Scheepers M, Nouet C, Bosman B, Carnol M, Motte P, Verbruggen N, Hanikenne M (2018) Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri. New Phytol 218:269–282
St. Clair SB, Lynch JP (2005) Element accumulation patterns of deciduous and evergreen tree seedlings on acid soils: implications for sensitivity to manganese toxicity. Tree Physiol 25:85–92
Tappero R, Peltier E, Gräfe M, Heidel K, Ginder-Vogel M, Livi KJT, Rivers ML, Marcus MA, Chaney RL, Sparks DL (2007) Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol 175(4):641–654
van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334
van der Ent A, Jaffré T, L’Huillier L, Gibson N, Reeves RD (2015) The flora of ultramafic soils in the Australia-Pacific region: state of knowledge and research priorities. Aust J Bot 63:173–190
van der Ent A, Przybyłowicz WJ, de Jonge MD, Harris HH, Ryan CG, Tylko G, Paterson DJ, Barnabas AD, Kopittke PM, Mesjasz-Przybyłowicz J (2018)X-ray elemental mapping techniques for elucidating the ecophysiology of hyperaccumulator plants. New Phytol 218:432–452
van der Ent A, Echevarria G, Pollard AJ, Erskine PD (2019)X-ray fluorescence ionomics of herbarium collections. Sci Rep 9:4746
van der Vliet L, Peterson C, Hale B (2007) Cd accumulation in roots and shoots of durum wheat: the roles of transpiration rate and apoplastic bypass. J Exp Bot 58:2939–2947
Xu X, Shi J, Chen Y, Chen X, Wang H, Perera A (2006) Distribution and mobility of manganese in the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Plant Soil 285:323–331
Xue S, Chen Y, Reeves RD, Baker AJM, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ Pollut 131:393–399
Acknowledgements
Farida Abubakari is the recipient of a UQ Graduate School Scholarship (UQGSS) from The University of Queensland. We thank Lachlan Casey (Centre for Microscopy and Microanalysis at the University of Queensland) for technical support with the μXRF analysis. We acknowledge the support of the AMMRF at the Center for Microscopy and Microanalysis at the University of Queensland.
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Abubakari, F., Nkrumah, P.N., Erskine, P.D. et al. Manganese (hyper)accumulation within Australian Denhamia (Celastraceae): an assessment of the trait and manganese accumulation under controlled conditions. Plant Soil 463, 205–223 (2021). https://doi.org/10.1007/s11104-021-04833-z
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DOI: https://doi.org/10.1007/s11104-021-04833-z