Abstract
Macadamia nuts are known globally for their high quality and economic value. Global macadamia commercial nut production amounts to 60,000 metric tonnes and is increasing steadily. South Africa is the leading producer with 29% of worldwide kernel production. Commercial macadamia germplasm was originally selected from a small genepool (mainly Macadamia integrifolia species) from a limited geographic distribution in Australia. These accessions were subsequently bred, cloned and exported across the world to start local macadamia industries. The South African macadamia industry was established with pre-commercial and commercial macadamia from different parts of the world, and local selections were also performed. Many of these accessions have unique genetic compositions that have not been characterized yet. We used 13 nuclear microsatellite markers to study the genetic diversity and structure of macadamia germplasm cultivated in South Africa. We compared four groups of accessions including 31 originating from the Hawaiian Agricultural Experimental Station (HAES), 19 from Australia (AUS), two from California and one from Israel (OTH), 31 from South Africa’s locally selected accessions (SA) and 26 from two local Farmers (FARM). We used STRUCTURE, PCoA and neighbour-joining phylogenetic analyses to show that the South African selected accessions include diverse hybrid genotypes with strong Macadamia tetraphylla composition, unlike the Hawaiian commercially released and Australian representative collections that mostly have M. integrifolia or hybrid composition. Our results suggest that the South African selections represent a unique and diverse set of germplasm for future macadamia improvement efforts that will benefit from genomic breeding technologies.
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All of the data are included in the electronic supplementary material (Table S3).
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22 July 2022
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References
Alam M, Neal J, O’Connor K, Kilian A, Topp B (2018) Ultra-high-throughput DArTseq-based silicoDArT and SNP markers for genomic studies in macadamia. PLOS ONE 13(8):e0203465
Allan P (1993) Quality of macadamia cultivars and selections in subtropical areas. South African Macadamia Growers Association Yearbook 1:26–31
Allan P (1997) Future macadamia cultivar research. Macadamia Yearbook 1997:52–55
Allan P (2016) Development of the macadamia nut industry in South Africa. Subtop Quarterly Journal 13(January-March):24–30
Allan P, Apostolides K, Blore N, Williams M (1997) Cultivar evaluation and rooting at Pietermaritzburg. Macadamia Yearbook 1997:49–55
Allan P, Hauff N (1995) Evaluation of macadamia cultivars and selections at Pietermaritzburg. South African Macadamia Growers Association Yearbook 1995:24–28
Baldoni AB et al (2020) Genetic diversity of Brazil nut tree (Bertholletia excelsa Bonpl.) in southern Brazilian Amazon. For Ecol Manag 458:117795
Beck HE, Zimmermann NE, McVicar TR, Vergopolan N, Berg A, Wood EF (2018) Present and future Köppen-Geiger climate classification maps at 1-km resolution. Scientific Data 5:180214
Bernard A, Barreneche T, Lheureux F, Dirlewanger E (2018) Analysis of genetic diversity and structure in a worldwide walnut (Juglans regia L.) germplasm using SSR markers. PLOS ONE 13(11):e0208021
Cabral J, Baldoni A, Tonini H, Azevedo V, Giustina L, Tiago A, Rossi A (2017) Diversity and genetic structure of the native Brazil nut tree (Bertholletia excelsa Bonpl.) population. Genet Mol Res 16(3):gmr16039702
Collard BCY, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B Biol Sci 363(1491):557–572
Coverdale C, Hardner C, Wegener MK (1999) Evaluation of economic weights for selection and breeding in macadamia. Australian Agricultural and Resource Economics Society Conference (43th), January 19–22, Christchurch, New Zealand
dos Santos JO, Mayo SJ, Bittencourt CB, de Andrade IM (2019) Genetic diversity in wild populations of the restinga ecotype of the cashew (Anacardium occidentale) in coastal Piauí, Brazil. Plant Syst Evol 305(10):913–924
Earl DA and von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
Everaert H et al (2017) Molecular characterization of Vietnamese cocoa genotypes (Theobroma cacao L.) using microsatellite markers. Tree Genet Genomes 13(5):1–11
Francis R (2015) Structure ‘Sort by Q’ explained. https://www.royfrancis.com/structure-sort-by-q-explained/. Accessed 20 Oct 2020
Frichot E, François O (2015) LEA: An R package for landscape and ecological association studies. Methods Ecol Evol 6(8):925–929
Govindaraj M, Vetriventhan M, Srinivasan M (2015) Importance of genetic diversity assessment in crop plants and its recent advances: an overview of its analytical perspectives. Genetics Research International 2015
Giustina LD et al (2017) Genetic diversity between and within half-sib families of Brazil nut tree (Bertholletia excelsa Bonpl.) originating from native forest of the Brazilian Amazon. Genetics and Molecular Research 16(4):gmr16039839
Guichoux E et al (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11(4):591–611
Hardner C (2016) Macadamia domestication in Hawai‘i. Genetic Resources for Crop Evolution 63(8):1411–1430
Hardner CM, Peace C, Lowe AJ, Neal J, Pisanu P (2009) Genetic resources and domestication of macadamia, vol 35. Horticultural Reviews. John Wiley & Sons Inc, USA
Heard TA (1993) Pollinator requirements and flowering patterns of Macadamia integrifolia. Aust J Bot 41(5):491–497
Helmstetter AJ, Oztolan-Erol N, Lucas SJ, Buggs RJA (2020) Genetic diversity and domestication of hazelnut (Corylus avellana L.) in Turkey. Plants, People, Planet 2(4):326–339
Hildebrand CE, Torney DC, Wagner RP (1992) Informativeness of polymorphic DNA markers. Los Alamos Science 20(20):100–102
Hobson L (2013) A few thoughts on macadamia varieties. SUBTROP Quarterly Journal 1(Jan-Mar):24–25
Howlett BG, Nelson WR, Pattemore DE, Gee M (2015) Pollination of macadamia: review and opportunities for improving yields. Sci Hortic 197:411–419
INC (2019–2020) Nut and dried fruits statistical yearbook 2019/2020 vol 2019–2020. International Nut and Dried Fruit Council Foundation, Spain
Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177(3):309–334
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16(5):1099–1106
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15(5):1179–1191
Langdon KS, King GJ, Nock CJ (2019) DNA paternity testing indicates unexpectedly high levels of self-fertilisation in macadamia. Tree Genet Genomes 15:29
Langella O (1999) Populations 1.2.30: population genetic software (individuals or populations distances, plylogenetic tree). http://www.bioinformatics.org/populations/
Lee P (1995) Macadamia cultivars for Southern Africa. Macadamia Yearbook 1995:42–46
Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47(W1):W256–W259
Mai T, Alam M, Hardner C, Henry R, Topp B (2020) Genetic structure of wild germplasm of macadamia: species assignment, diversity and phylogeographic relationships. Plants 9(6):714
Moose SP, Mumm RH (2008) Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol 147(3):969–977
Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19(2):153–170
Nock CJ, Elphinstone MS, Ablett G, Kawamata A, Hancock W, Hardner CM, King GJ (2014) Whole genome shotgun sequences for microsatellite discovery and application in cultivated and wild Macadamia (Proteaceae). Appl Plant Sci 2(4):apps.1300089
Nock CJ et al (2019) Wild origins of macadamia domestication identified through intraspecific chloroplast genome sequencing. Front Plant Sci 10:334
Niu Y-F et al. (2020) Genome assembly and annotation of Macadamia tetraphylla. bioRxiv:2020.2003.2011.987057
Nock CJ et al. (2020) Chromosome-scale assembly and annotation of the macadamia genome (Macadamia integrifolia HAES 741). G3 10(10):3497–3504
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. Biol Cons 191:504–511
O’Connor K et al (2019) Population structure, genetic diversity and linkage disequilibrium in a macadamia breeding population using SNP and silicoDArT markers. Tree Genet Genomes 15:24
Peace C, Ming R, Schmidt A, Manners J, Vithanage V (2008) Genomics of macadamia, a recently domesticated tree nut crop. In: Moore PH, Ming R (eds) Genomics of Tropical Crop Plants, vol 1. Plant Genetics and Genomics: Crops and Models. Springer, New York, pp 313–332
Peace CP, Allan P, Vithanage V, Turnbull CN, Carroll BJ (2005) Genetic relationships amongst macadamia varieties grown in South Africa as assessed by RAF markers. South African Journal of Plant and Soil 22(2):71–75
Peace CP, Vithanage V, Neal J, Turnbull CGN, Carroll BJ (2004) A comparison of molecular markers for genetic analysis of macadamia. J Hortic Sci Biotechnol 79(6):965–970
Peace C, Vithanage V, Turnbull C, Carroll BJ (2002a) Characterising macadamia germplasm with codominant radiolabelled DNA amplification fingerprinting (RAF) markers In: International Symposium on Tropical and Subtropical Fruits, 2002. International Society for Horticultural Science (ISHS), Leuven, Belgium, 371–380. https://doi.org/10.17660/ActaHortic.2002a.575.42
Peace C, Hardner C, Brown AHD, O’Connor K, Vithanage V, Turnbull C, Carroll BJ (2002b) The diversity and origins of macadamia cultivars. WANATCA Yearbook 26:19–25
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. Bioinformatics 28(19):2537–2539
Penter M (2016) Progress of new cultivar trials for the South African macadamia industry. SUBTROP Quarterly Journal 15(July - September 2016):24–27
Penter M, Schoeman S, Nkwana E (2007) Cross-pollination for improved nut set in ‘Beaumont’ macadamias. South African Macadamia Growers Association Yearbook 15:13–16
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
SAMAC (2020) Statistics of the Southern African Macadamia Industry. SAMAC, Macadamias South Africa. https://www.samac.org.za/industry-statistics/. Accessed 11/05/2020
Schmidt AL, Scott L, Lowe AJ (2006) Isolation and characterization of microsatellite loci from Macadamia. Mol Ecol Notes 6(4):1060–1063
Schneider SJ, Hwang AY, Land SD, Chen L-L, Thomas AL, Hwang C-F (2019) Genetic diversity of ten black walnut (Juglans nigra L.) cultivars and construction of a mapping population. Tree Genet Genomes 15:62
Sedgley M, Bell FDH, Bell D, Winks CW, Pattison SJ, Hancock TW (1990) Self-and cross-compatibility of macadamia cultivars. Journal of Horticultural Science 65(2):205–213
Sievert C (2020) Interactive web-based data visualization with R, plotly, and shiny. CRC Press, Florida
Simpson WA, Allan P (1998) Revised key for identifying macadamia cultivars. South African Macadamia Growers’ Association Yearbook 6:47–56
Spain CS, Lowe AJ (2011) Genetic consequences of subtropical rainforest fragmentation on Macadamia tetraphylla (Proteaceae). Silvae Genetica 60(1–6):241–249
Steiger DL, Moore PH, Zee F, Liu Z, Ming R (2003) Genetic relationships of macadamia cultivars and species revealed by AFLP markers. Euphytica 132:269–277
Trueman SJ (2013) The reproductive biology of macadamia. Sci Hortic 150:354–359
Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23(1):48–55
Vieira MLC, Santini L, Diniz AL, Munhoz CdF (2016) Microsatellite markers: what they mean and why they are so useful. Genet Mol Biol 39(3):312–328
Vithanage V, Winks C (1992) Isozymes as genetic markers for Macadamia. Sci Hortic 49(1–2):103–115
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10(1):249–256
Wallace HM, Vithanage V, Exley E (1996) The effect of supplementary pollination on nut set of Macadamia (Proteaceae). Ann Bot 78:765–773
Weinert IAG (1993) Macadamia nut processing. The Southern African Macadamia Growers Association Yearbook 1993:54–75
Wickham H (2011) The split-apply-combine strategy for data analysis. J Stat Softw 40(1):1–29
Acknowledgements
The authors thank Mark Penter (Agricultural Research Council–Institute for Tropical and Subtropical Crops (ARC-ITSC) of South Africa) for assistance with sample collection from Mpumalanga, constructive comments on the manuscript and valuable information and discussions. The authors also thank Matthew Erasmus for the sample collection from University of KwaZulu-Natal–Ukulinga Research Farm. We would like to thank the local Farmer for allowing us to use the breeding population and the second farmer for his sample. Further thanks to Dr Catherine Nock (Southern Cross University) for assistance with the microsatellite markers. We would like to thank Dr Nanette Christie (University of Pretoria) and Annie Chan (Agricultural Research Council–Biotechnology Platform) for assistance with RStudio and the Forest Molecular Genetics Team (University of Pretoria) for their guidance with the GeneMarker. This work was funded by the National Research Foundation (NRF) of South Africa (UID 112133) and Macadamias South Africa (SAMAC). MR acknowledges PhD scholarship support from the Agricultural Research Council–Professional Development Programme (ARC-PDP) of South Africa.
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This work was funded by the National Research Foundation (NRF) of South Africa (grant to CH, UID 112133). Further funding was received from Macadamias South Africa (SAMAC, strategic grant to GF).
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The experimental design was contributed by CH, AAM and MR. MR did data collection and data analysis and wrote the first draft of the paper as part of her PhD thesis. The study was supervised by AAM, CH, GF and RP. The final manuscript was edited and approved by all the authors.
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Ranketse, M., Hefer, C.A., Pierneef, R. et al. Genetic diversity and population structure analysis reveals the unique genetic composition of South African selected macadamia accessions. Tree Genetics & Genomes 18, 15 (2022). https://doi.org/10.1007/s11295-022-01543-0
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DOI: https://doi.org/10.1007/s11295-022-01543-0