Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Biomass partitioning and ionomics of Macadamia with high manganese and low phosphorus concentrations

Xin Zhao A , Yang Lyu A , Qianqian Dong A , Xiyong He B , Hai Yue B , Liping Yang B , Liang Tao B , Lidan Gong B , Hongxu Zheng A , Sijie Wen A , Hans Lambers https://orcid.org/0000-0002-4118-2272 A C and Jianbo Shen https://orcid.org/0000-0001-8943-948X A *
+ Author Affiliations
- Author Affiliations

A Department of Plant Nutrition, College of Resources and Environmental Sciences, Key Laboratory of Plant-Soil Interactions, Ministry of Education, National Academy of Agriculture Green Development, China Agricultural University, Beijing 100193, P. R. China.

B Yunnan Institute of Tropical Crops, Jinghong, Yunnan 666100, P. R. China.

C School of Biological Sciences and Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Perth, WA 6009, Australia.

* Correspondence to: jbshen@cau.edu.cn

Handling Editor: Tim Cavagnaro

Functional Plant Biology 50(7) 559-570 https://doi.org/10.1071/FP22197
Submitted: 27 August 2022  Accepted: 13 April 2023   Published: 22 May 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Knowledge of the ionome of plant organs helps us understand a plant’s nutritional status. However, the ionome of Macadamia (Proteaceae), which is an important nut-producing tree, remains unknown. We aimed to characterise the allocation of biomass and nutrient-partitioning patterns in three macadamia genotypes. We excavated 15 productive trees (three cultivars at 21 years of age; two cultivars at 16 years of age) in an orchard. Biomass, nutrient concentrations, and contents of roots, stems, branches, and leaves were analysed. Dry weight of roots, stems, branches and leaves accounted for 14–20%, 19–30%, 36–52%, and 12–18% of total plant weight, respectively. No significant difference was found in the total biomass among the cultivars at the same age. Compared with most crop plants, macadamia had low phosphorus (P) concentrations in all organs (<1 g kg−1), and low leaf zinc (Zn) concentration (8 mg kg−1). In contrast, macadamia accumulated large amounts of manganese (Mn), with a 20-fold higher leaf Mn concentration than what is considered sufficient for crop plants. Leaves exhibited the highest nutrient concentrations, except for iron and Zn, which exhibited the highest concentrations in roots. The organ-specific ionomics of Macadamia is characterised by low P and high Mn concentrations, associated with adaptation to P-impoverished habitats.

Keywords: biomass partitioning, ionomics, leaf zinc concentration, macadamia, manganese concentration, nutrient allocation, phosphorus concentration, plant organs.


References

Abubakari F, Fernando DR, Nkrumah PN, Harris HH, Erskine PD, van der Ent A (2022) Cellular-level distribution of manganese in Macadamia integrifolia, M. ternifolia, and M. tetraphylla from Australia. Metallomics 14, mfac045
Cellular-level distribution of manganese in Macadamia integrifolia, M. ternifolia, and M. tetraphylla from Australia.Crossref | GoogleScholarGoogle Scholar |

Aitken RL, Moody PW, Compton BL, Gallagher EC (1992) Plant and soil diagnostic tests for assessing the phosphorus status of seedling Macadamia integrifolia. Australian Journal of Agricultural Research 43, 191–201.
Plant and soil diagnostic tests for assessing the phosphorus status of seedling Macadamia integrifolia.Crossref | GoogleScholarGoogle Scholar |

Bazzaz FA, Grace J (1997) ‘Plant resource allocation.’ (Academic Press: London, UK)

Bender RR, Haegele JW, Ruffo ML, Below FE (2013) Nutrient uptake, partitioning, and remobilization in modern, transgenic insect-protected maize hybrids. Agronomy Journal 105, 161–170.
Nutrient uptake, partitioning, and remobilization in modern, transgenic insect-protected maize hybrids.Crossref | GoogleScholarGoogle Scholar |

Borompichaichartkul C, Luengsode K, Chinprahast N, Devahastin S (2009) Improving quality of macadamia nut (Macadamia integrifolia) through the use of hybrid drying process. Journal of Food Engineering 93, 348–353.
Improving quality of macadamia nut (Macadamia integrifolia) through the use of hybrid drying process.Crossref | GoogleScholarGoogle Scholar |

Bouranis DL, Chorianopoulou SN, Zakynthinos G, Sarlis G, Drossopoulos JB (2001) Flower analysis for prognosis of nutritional dynamics of almond tree. Journal of Plant Nutrition 24, 705–716.
Flower analysis for prognosis of nutritional dynamics of almond tree.Crossref | GoogleScholarGoogle Scholar |

Broadley MR, White PJ (2010) Eats roots and leaves. Can edible horticultural crops address dietary calcium, magnesium and potassium deficiencies? Proceedings of the Nutrition Society 69, 601–612.
Eats roots and leaves. Can edible horticultural crops address dietary calcium, magnesium and potassium deficiencies?Crossref | GoogleScholarGoogle Scholar |

Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of nutrients: micronutrients. In ‘Marschner’s mineral nutrition of higher plants’. (Ed. P Marschner) pp. 191–248. (Academic Press: Waltham, MA, USA)

Cooil BJ (1967) Potassium and magnesium nutrition of macadamia. In ‘Proceedings of the 7th annual meeting Hawaii Macadamia Producers Association’. pp. 19–23. (CABI: Hilo, HI, USA)

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 & Environment 30, 1557–1565.
Banksia species (Proteaceae) from severely phosphorus-impoverished soils exhibit extreme efficiency in the use and re-mobilization of phosphorus.Crossref | GoogleScholarGoogle Scholar |

Dinkelaker B, Römheld V, Marschner H (1989) Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.). Plant, Cell & Environment 12, 285–292.
Citric acid excretion and precipitation of calcium citrate in the rhizosphere of white lupin (Lupinus albus L.).Crossref | GoogleScholarGoogle Scholar |

Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108, 183–200.
Distribution and function of proteoid roots and other root clusters.Crossref | GoogleScholarGoogle Scholar |

Dinkelaker B, Hengeler G, Neumann G, Eltrop L, Marschner H (1997) Root exudates and mobilization of nutrients. In ‘Trees – contributions to modern tree physiology’. (Eds H Rennenberg, W Eschrich, H Ziegler) pp. 441–452. (Backhuys Publishers: Leiden, Netherlands)

Epstein E, Bloom AJ (2005) ‘Mineral nutrition of plants: principles and perspectives.’ 2nd edn. p. 400. (Sinauer Associates: Sunderland, MA, USA)

Fernando DR, Bakkaus EJ, Perrier N, Baker AJM, Woodrow IE, Batianoff GN, Collins RN (2006) Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study. New Phytologist 171, 751–758.
Manganese accumulation in the leaf mesophyll of four tree species: a PIXE/EDAX localization study.Crossref | GoogleScholarGoogle Scholar |

Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJ, Batianoff GN (2009) Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy. Annals of Botany 103, 931–939.
Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy.Crossref | GoogleScholarGoogle Scholar |

Firth DJ, Whalley RDB, Johns GG (2003) Distribution and density of the root system of macadamia on krasnozem soil and some effects of legume groundcovers on fibrous root density. Australian Journal of Experimental Agriculture 43, 503–514.
Distribution and density of the root system of macadamia on krasnozem soil and some effects of legume groundcovers on fibrous root density.Crossref | GoogleScholarGoogle Scholar |

Foulds W (1993) Nutrient concentrations of foliage and soil in south-western Australia. New Phytologist 125, 529–546.
Nutrient concentrations of foliage and soil in south-western Australia.Crossref | GoogleScholarGoogle Scholar |

Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant and Soil 70, 107–124.
The acquisition of phosphorus by Lupinus albus L. III. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced.Crossref | GoogleScholarGoogle Scholar |

Garg ML, Blake RJ, Wills RBH, Clayton EH (2007) Macadamia nut consumption modulates favourably risk factors for coronary artery disease in hypercholesterolemic subjects. Lipids 42, 583–587.
Macadamia nut consumption modulates favourably risk factors for coronary artery disease in hypercholesterolemic subjects.Crossref | GoogleScholarGoogle Scholar |

Gebbing T, Schnyder H, KÜhbauch W (1999) The utilization of pre-anthesis reserves in grain filling of wheat. Assessment by steady-state 13CO2/12CO2 labelling. Plant, Cell & Environment 22, 851–858.
The utilization of pre-anthesis reserves in grain filling of wheat. Assessment by steady-state 13CO2/12CO2 labelling.Crossref | GoogleScholarGoogle Scholar |

Grag ML, Rudra P, Blake R, Wills R (2003) Macadamia nut consumption lowers plasma Total and LDL cholesterol levels in hypercholesterolemic men. The Journal of Nutrition 133, 1060–1063.
Macadamia nut consumption lowers plasma Total and LDL cholesterol levels in hypercholesterolemic men.Crossref | GoogleScholarGoogle Scholar |

Grusak MA, Broadley MR, White PJ (2016) Plant macro- and micronutrient minerals (Version 2.0). eLS
Plant macro- and micronutrient minerals (Version 2.0).Crossref | GoogleScholarGoogle Scholar |

Hardner C (2016) Macadamia domestication in Hawai‘i. Genetic Resources and Crop Evolution 63, 1411–1430.
Macadamia domestication in Hawai‘i.Crossref | GoogleScholarGoogle Scholar |

Hardner CM, Peace C, Lowe AJ, Neal J, Pisanu P, Powell M, Schmidt A, Spain C, Williams K (2009) Genetic resources and domestication of macadamia. In ‘Horticultural Reviews, Vol. 35’. (Ed. J Janick) pp. 1–125. (Wiley: Hoboken, NJ, USA)

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. Journal of Ecology 102, 396–410.
Foliar nutrient concentrations and resorption efficiency in plants of contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence.Crossref | GoogleScholarGoogle Scholar |

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 & Environment 41, 605–619.
Proteaceae from phosphorus-impoverished habitats preferentially allocate phosphorus to photosynthetic cells: an adaptation improving phosphorus-use efficiency.Crossref | GoogleScholarGoogle Scholar |

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 Phytologist 221, 764–777.
Calcium-enhanced phosphorus toxicity in calcifuge and soil-indifferent Proteaceae along the Jurien Bay chronosequence.Crossref | GoogleScholarGoogle Scholar |

Hayes PE, Nge FJ, Cramer MD, Finnegan PM, Fu P, Hopper SD, Oliveira RS, Turner BL, Zemunik G, Zhong H, Lambers H (2021) Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus-impoverished landscapes. Plant and Soil 462, 67–88.
Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus-impoverished landscapes.Crossref | GoogleScholarGoogle Scholar |

Herbert SW, Walton DA, Wallace HM (2019) Pollen-parent affects fruit, nut and kernel development of Macadamia. Scientia Horticulturae 244, 406–412.
Pollen-parent affects fruit, nut and kernel development of Macadamia.Crossref | GoogleScholarGoogle Scholar |

Hikosaka K, Takashima T, Kabeya D, Hirose T, Kamata N (2005) Biomass allocation and leaf chemical defence in defoliated seedlings of quercus serrata with respect to carbon-nitrogen balance. Annals of Botany 95, 1025–1032.
Biomass allocation and leaf chemical defence in defoliated seedlings of quercus serrata with respect to carbon-nitrogen balance.Crossref | GoogleScholarGoogle Scholar |

Holland B, Unwin ID, Buss DH (1992) ‘Fruits and nuts: the composition of foods.’ McCance and Widdowson’s 5th edn. (Royal Society of Chemistry: Cambridge, UK)

Hue NV (2009) Iron and phosphorus fertilizations and the development of proteoid roots in macadamia (Macadamia integrifolia). Plant and Soil 318, 93–100.
Iron and phosphorus fertilizations and the development of proteoid roots in macadamia (Macadamia integrifolia).Crossref | GoogleScholarGoogle Scholar |

Hue NV, Fox RL, Mccall WW (1987) Aluminum, Ca, and Mn concentrations in macadamia seedlings as affected by soil acidity and liming. Communications in Soil Science and Plant Analysis 18, 1253–1267.
Aluminum, Ca, and Mn concentrations in macadamia seedlings as affected by soil acidity and liming.Crossref | GoogleScholarGoogle Scholar |

Huett DO, Vimpany I (2007) Revised diagnostic leaf nutrient standards for macadamia growing in Australia. Australian Journal of Experimental Agriculture 47, 869–876.
Revised diagnostic leaf nutrient standards for macadamia growing in Australia.Crossref | GoogleScholarGoogle Scholar |

Ko W-H (2009) Nature of slow and quick decline of macadamia trees. Botanical Studies 50, 1–10.

Lambers H (2022) Phosphorus acquisition and utilization in plants. Annual Review of Plant Biology 73, 17–42.
Phosphorus acquisition and utilization in plants.Crossref | GoogleScholarGoogle Scholar |

Lambers H, Cawthray GR, Giavalisco P, Kuo J, Laliberté E, Pearse SJ, Scheible W-R, 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 Phytologist 196, 1098–1108.
Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency.Crossref | GoogleScholarGoogle Scholar |

Lambers H, Clode PL, Hawkins H-J, Laliberté E, Oliveira RS, Reddell P, Shane MW, Stitt M, Weston P (2015a) Metabolic adaptations of the non-mycotrophic Proteaceae to soils with low phosphorus availability. In ‘Annual plant reviews, Vol. 48’. (Eds WC Plaxton, H Lambers) pp. 289–335. (Wiley: Hoboken, NJ, USA)

Lambers H, Hayes PE, Laliberté E, Oliveira RS, Turner BL (2015b) Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends in Plant Science 20, 83–90.
Leaf manganese accumulation and phosphorus-acquisition efficiency.Crossref | GoogleScholarGoogle Scholar |

Lu RK (1999) ‘Analytical methods of soil agrochemistry (in Chinese).’ 1st edn. (China Agricultural Science and Technology Press: Beijing, China)

Malcolm H, Trochoulias T (1979) Proteoid roots help macadamia nut trees. Agricultural Gazette of New South Wales 90, 42–43.

Marschner P (2012) ‘Marschner’s mineral nutrition of higher plants.’ 3rd edn. (Academic Press: London, UK)

Mast AR, Willis CL, Jones EH, Downs KM, Weston PH (2008) A smaller Macadamia from a more vagile tribe: inference of phylogenetic relationships, divergence times, and diaspore evolution in Macadamia and relatives (tribe Macadamieae; Proteaceae). American Journal of Botany 95, 843–870.
A smaller Macadamia from a more vagile tribe: inference of phylogenetic relationships, divergence times, and diaspore evolution in Macadamia and relatives (tribe Macadamieae; Proteaceae).Crossref | GoogleScholarGoogle Scholar |

Mayer DG, Chandra KA, Burnett JR (2019) Improved crop forecasts for the Australian macadamia industry from ensemble models. Agricultural Systems 173, 519–523.
Improved crop forecasts for the Australian macadamia industry from ensemble models.Crossref | GoogleScholarGoogle Scholar |

Mediavilla S, Escudero A (2010) Differences in biomass allocation patterns between saplings of two co-occurring Mediterranean oaks as reflecting different strategies in the use of light and water. European Journal of Forest Research 129, 697–706.
Differences in biomass allocation patterns between saplings of two co-occurring Mediterranean oaks as reflecting different strategies in the use of light and water.Crossref | GoogleScholarGoogle Scholar |

Mehlich A (1984) Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Communications in Soil Science and Plant Analysis 15, 1409–1416.
Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant.Crossref | GoogleScholarGoogle Scholar |

Moraghan JT (1992) Iron-manganese relationships in white lupine grown on a calciaquoll. Soil Science Society of America Journal 56, 471–475.
Iron-manganese relationships in white lupine grown on a calciaquoll.Crossref | GoogleScholarGoogle Scholar |

Morris DM, MacDonald GB, McClain KM (1990) Evaluation of morphological attributes as response variables to perennial competition for 4-year-old black spruce and jack pine seedlings. Canadian Journal of Forest Research 20, 1696–1703.
Evaluation of morphological attributes as response variables to perennial competition for 4-year-old black spruce and jack pine seedlings.Crossref | GoogleScholarGoogle Scholar |

Nagao MA, Hirae HH, Stephenson RA (1992) Macadamia: cultivation and physiology. Critical Reviews in Plant Sciences 10, 441–470.
Macadamia: cultivation and physiology.Crossref | GoogleScholarGoogle Scholar |

Neugebauer K, Broadley MR, El-Serehy HA, George TS, McNicol JW, Moraes MF, White PJ (2018) Variation in the angiosperm ionome. Physiologia Plantarum 163, 306–322.
Variation in the angiosperm ionome.Crossref | GoogleScholarGoogle Scholar |

Neumann G, Martinoia E (2002) Cluster roots – an underground adaptation for survival in extreme environments. Trends in Plant Science 7, 162–167.
Cluster roots – an underground adaptation for survival in extreme environments.Crossref | GoogleScholarGoogle Scholar |

O’Connor K, Powell M, Nock C, Shapcott A (2015) Crop to wild gene flow and genetic diversity in a vulnerable Macadamia (Proteaceae) species in New South Wales, Australia. Biological Conservation 191, 504–511.
Crop to wild gene flow and genetic diversity in a vulnerable Macadamia (Proteaceae) species in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |

Ojeda-Barrios D, Abadía J, Lombardini L, Abadía A, Vázquez S (2012) Zinc deficiency in field-grown pecan trees: changes in leaf nutrient concentrations and structure. Journal of the Science of Food and Agriculture 92, 1672–1678.
Zinc deficiency in field-grown pecan trees: changes in leaf nutrient concentrations and structure.Crossref | GoogleScholarGoogle Scholar |

Oksanen J, Blanchet FG, Friendly M, Kindt R (2016) Community ecology package. R package version 2.2-0 2014. Available at http://CRAN.Rproject.org/package=vegan

Pang J, Bansal R, Zhao H, Bohuon E, Lambers H, Ryan MH, Ranathunge K, Siddique KHM (2018) The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytologist 219, 518–529.
The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Sack L (2012) Pitfalls and possibilities in the analysis of biomass allocation patterns in plants. Frontiers in Plant Science 3, 259
Pitfalls and possibilities in the analysis of biomass allocation patterns in plants.Crossref | GoogleScholarGoogle Scholar |

Prodhan MA, Finnegan PM, Lambers H (2019) How does evolution in phosphorus-impoverished landscapes impact plant nitrogen and sulfur assimilation? Trends in Plant Science 24, 69–82.
How does evolution in phosphorus-impoverished landscapes impact plant nitrogen and sulfur assimilation?Crossref | GoogleScholarGoogle Scholar |

Przulj N, Momcilovic V (2001) Genetic variation for dry matter and nitrogen accumulation and translocation in two-rowed spring barley. I. Dry matter translocation. European Journal of Agronomy 15, 241–254.
Genetic variation for dry matter and nitrogen accumulation and translocation in two-rowed spring barley. I. Dry matter translocation.Crossref | GoogleScholarGoogle Scholar |

Reeves RD, Baker AJM (2000) Metal-accumulating plants. In ‘Phytoremediation of toxic metals: using plants to clean up the environment’. (Eds I Raskin, BD Ensley) pp. 193–229. (Wiley: New York, USA)

Salt DE, Baxter I, Lahner B (2008) Ionomics and the study of the plant ionome. Annual Review of Plant Biology 59, 709–733.
Ionomics and the study of the plant ionome.Crossref | GoogleScholarGoogle Scholar |

Schlörmann W, Birringer M, Böhm V, Löber K, Jahreis G, Lorkowski S, Müller AK, Schöne F, Glei M (2015) Influence of roasting conditions on health-related compounds in different nuts. Food Chemistry 180, 77–85.
Influence of roasting conditions on health-related compounds in different nuts.Crossref | GoogleScholarGoogle Scholar |

Shane MW, Lambers H (2005a) Cluster roots: a curiosity in context. Plant and Soil 274, 101–125.
Cluster roots: a curiosity in context.Crossref | GoogleScholarGoogle Scholar |

Shane MW, Lambers H (2005b) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiologia Plantarum 124, 441–450.
Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply.Crossref | GoogleScholarGoogle Scholar |

Shibuya T, Watanabe T, Ikeda H, Kanayama Y (2015) Ionomic analysis of horticultural plants reveals tissue-specific element accumulation. The Horticulture Journal 84, 305–313.
Ionomic analysis of horticultural plants reveals tissue-specific element accumulation.Crossref | GoogleScholarGoogle Scholar |

Stephenson RA, Cull BW (1986) Standard leaf nutrient levels for bearing macadamia trees in south east Queensland. Scientia Horticulturae 30, 73–82.
Standard leaf nutrient levels for bearing macadamia trees in south east Queensland.Crossref | GoogleScholarGoogle Scholar |

Stephenson RA, Trochoulias T (1994) Macadamia. In ‘Handbook of environmental physiology of fruit crops, Vol. 2: subtropical and tropical crops’. (Eds B Schaffer, PC Andersen) pp. 147–163. (CRC Press: Boca Raton, FL, USA)

Stephenson RA, Gallagher EC, Pepper PM (2002) Macadamia yield and quality responses to phosphorus. Australian Journal of Agricultural Research 53, 1165–1172.
Macadamia yield and quality responses to phosphorus.Crossref | GoogleScholarGoogle Scholar |

Sulpice R, Ishihara H, Schlereth A, Cawthray GR, Encke B, Giavalisco P, Ivakov A, Arrivault S, Jost R, Krohn N, Kuo J, Laliberté E, Pearse SJ, Raven JA, Scheible WR, Teste F, Veneklaas EJ, Stitt M, Lambers H (2014) Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant, Cell & Environment 37, 1276–1298.
Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species.Crossref | GoogleScholarGoogle Scholar |

Tackenberg O (2007) A new method for non-destructive measurement of biomass, growth rates, vertical biomass distribution and dry matter content based on digital image analysis. Annals of Botany 99, 777–783.
A new method for non-destructive measurement of biomass, growth rates, vertical biomass distribution and dry matter content based on digital image analysis.Crossref | GoogleScholarGoogle Scholar |

Trueman SJ (2013) The reproductive biology of macadamia. Scientia Horticulturae 150, 354–359.
The reproductive biology of macadamia.Crossref | GoogleScholarGoogle Scholar |

Vemmos SN (1999) Mineral composition of leaves and flower buds in fruiting and non-fruiting pistachio trees. Journal of Plant Nutrition 22, 1291–1301.
Mineral composition of leaves and flower buds in fruiting and non-fruiting pistachio trees.Crossref | GoogleScholarGoogle Scholar |

Warner RM, Fox RL (1972)Concentration and distribution of S, Mg and five micronutrients in macadamia in relation to yields. In ‘Proceedings of the 12th annual meeting Hawaii Macadamia Producers Association’. pp. 26–37.

White PJ, Brown PH (2010) Plant nutrition for sustainable development and global health. Annals of Botany 105, 1073–1080.
Plant nutrition for sustainable development and global health.Crossref | GoogleScholarGoogle Scholar |

Williams L, Salt DE (2009) The plant ionome coming into focus. Current Opinion in Plant Biology 12, 247–249.
The plant ionome coming into focus.Crossref | GoogleScholarGoogle Scholar |

Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Garnier E, Hikosaka K, Lamont BB, Lee W, Oleksyn J, Osada N, Poorter H, Villar R, Warton DI, Westoby M (2005) Assessing the generality of global leaf trait relationships. New Phytologist 166, 485–496.
Assessing the generality of global leaf trait relationships.Crossref | GoogleScholarGoogle Scholar |

Zhang H, Wang K, Xu X, Song T, Xu Y, Zeng F (2015) Biogeographical patterns of biomass allocation in leaves, stems and roots in China’s forests. Scientific Reports 5, 15997
Biogeographical patterns of biomass allocation in leaves, stems and roots in China’s forests.Crossref | GoogleScholarGoogle Scholar |

Zhao X, Dong Q, Ni S, He X, Yue H, Tao L, Nie Y, Tang C, Zhang F, Shen J (2019) Rhizosphere processes and nutrient management for improving nutrient-use efficiency in macadamia production. HortScience 54, 603–608.
Rhizosphere processes and nutrient management for improving nutrient-use efficiency in macadamia production.Crossref | GoogleScholarGoogle Scholar |

Zhao X, Lyu Y, Jin K, Lambers H, Shen J (2021) Leaf phosphorus concentration regulates the development of cluster roots and exudation of carboxylates in Macadamia integrifolia. Frontiers in Plant Science 11, 610591
Leaf phosphorus concentration regulates the development of cluster roots and exudation of carboxylates in Macadamia integrifolia.Crossref | GoogleScholarGoogle Scholar |