Multiple haploids, triploids, and tetraploids found in modern-day “living fossil” Ginkgo biloba

Petr Šmarda , Lucie Horová , Ondřej Knápek , Heidi Dieck , Martin Dieck , Katarína Ražná , Pavel Hrubík , Laszlo Orlóci , Laszlo Papp , Kristýna Veselá , Pavel Veselý , Petr Bureš

Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) : 55

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Horticulture Research ›› 2018, Vol. 5 ›› Issue (1) :55 DOI: 10.1038/s41438-018-0055-9
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Multiple haploids, triploids, and tetraploids found in modern-day “living fossil” Ginkgo biloba
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Abstract

Ginkgo biloba, the last extant representative of a lineage of Mesozoic gymnosperms, is one of the few seed plants with an exceptionally long (~300 Myr) evolutionary history free of genome-wide duplications (polyploidy). Despite this genome conservatism, we have recently found a viable spontaneous tetraploid Ginkgo sapling during routine screening of several plants, demonstrating that natural polyploidy is possible in Ginkgo. Here we provide a much wider flow cytometry survey of ploidy in some European Ginkgo collections, and own seedlings (>2200 individuals and ~200 cultivars). We found a surprisingly high level of ploidy variation in modern-day Ginkgo and documented altogether 13 haploid, 3 triploid, and 10 tetraploid Ginkgo plants or cultivars, most of them being morphologically distinct from common diploids. Haploids frequently produced polyploid (dihaploid) buds or branches. Tetraploids showed some genome size variation. The surveyed plants provide a unique resource for future Ginkgo research and breeding, and they might be used to accelerate the modern diversification of this nearly extinct plant lineage.

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Petr Šmarda, Lucie Horová, Ondřej Knápek, Heidi Dieck, Martin Dieck, Katarína Ražná, Pavel Hrubík, Laszlo Orlóci, Laszlo Papp, Kristýna Veselá, Pavel Veselý, Petr Bureš. Multiple haploids, triploids, and tetraploids found in modern-day “living fossil” Ginkgo biloba. Horticulture Research, 2018, 5 (1) : 55 DOI:10.1038/s41438-018-0055-9

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References

[1]

Zhou, Z. An overview of fossil Ginkgoales. Palaeoworld 18, 1-22 (2009).

[2]

Taylor, T. S., Taylor, E. L. & Krings, M. Paleobotany (Academic Press, Singapore, 2009).

[3]

Tralau, H. The phytogeographic evolution of the genus Ginkgo L.. Bot. Notiser 120, 409-422 (1967).

[4]

Bego, B. M. B. Nature's miracle. Ginkgo biloba L. 1771. 1, 2 (2011).

[5]

Crane, P. R. Ginkgo: The Tree that Time Forgot (Yale University Press, New Haven, CT, USA and London, UK, 2013).

[6]

Gong, W., Chen, C., Dobes, C., Fu, C. X. & Koch, M. A. Phylogeography of a living fossil: Pleistocene glaciations forced Ginkgo biloba L. (Ginkgoaceae) into two refuge areas in China with limited subsequent postglacial expansion. Mol. Phyl. Evol. 48, 1095-1105 (2008).

[7]

Santamour, F. S., He, S. & McArdle, A. J. Checklist of cultivated Ginkgo. J. Arboric. 9, 88-92 (1983).

[8]

Dieck, H. Ginkgo: Das Sortenbuch (Herrenkamper Gärten, Siedenburg, Germany, 2010).

[9]

Levin, D. A. The Role of Chromosomal Change in Plant Evolution (Oxford University Press, Oxford, UK, 2002).

[10]

Otto, S. P. The evolutionary consequences of polyploidy. Cell 131, 452-462 (2007).

[11]

Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411-424 (2017).

[12]

Fawcett, J. A., Maere, S. & Van de Peer, Y. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc. Natl. Acad. Sci. USA 106, 5737-5742 (2009).

[13]

Soltis, D. E. et al. Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336-348 (2009).

[14]

Vanneste, K., Baele, G., Maere, S. & Van de Peer, Y. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Res. 24, 1334-1347 (2014).

[15]

Soltis, P. S. & Soltis, D. E. Ancient WGD events as drivers of key innovations in angiosperms. Curr. Opin. Plant Biol. 30, 159-165 (2016).

[16]

Sax, K. & Sax, H. J. Chromosome number and morphology in conifers. J. Arnold Arbor. 14, 356-375 (1933).

[17]

Khoshoo, T. N. Polyploidy in gymnosperms. Evolution 13, 24-39 (1959).

[18]

Ahuja, M. R. Polyploidy in gymnosperms: revisited. Silvae Genet. 54, 59-69 (2005).

[19]

Leitch, A. R. & Leitch, I. J. Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol. 194, 629-646 (2012).

[20]

Husband, B. C., Baldwin, S. J. & Suda, J. in Plant Genome Diversity, Vol. 2. (eds Leitch, I. J., Greilhuber, J., Dolezel, J. & Wendel, J.) pp 255-276 (Springer, Vienna, Austria, 2013).

[21]

Li, Z. et al. Early genome duplications in conifers and other seed plants. Sci. Adv. 1, e1501084 (2015).

[22]

Roodt, D. et al. Evidence for an ancient whole genome duplication in the cycad lineage. PLoS ONE 12, e0184454 (2017).

[23]

Tulecke, W. R. A tissue derived from the pollen of Ginkgo biloba. Science 117, 599-600 (1953).

[24]

Trémouillaux-Guiller, J., Laurain, D. & Chénieux, J. C. in In Vitro Haploid Production in Higher Plants, Vol. 3. Important Selected Plants (eds Mohan, J., Sopory, S. K. & Veilleux, R. E.) 277-295 (Springer, Dordrecht, Neederlands, 1996).

[25]

Sun, Y. et al. Effect of colchicine treatment on the microtubule cytoskeleton and total protein during microsporogenesis in Ginkgo biloba L.. Pak. J. Bot. 47, 159-170 (2015).

[26]

Šmarda, P. et al. Polyploidy in a “living fossil” Ginkgo biloba. New Phytol. 212, 11-14 (2016).

[27]

Ražná, K. & Hrubík, P. Ginkgo dvojlaločné (Ginkgo biloba L.)-genomická štúdia a kultúrne rozšírenie na Slovensku [Maidenhair tree (Ginkgo biloba L.)-Genomic Study and Cultural Distribution in Slovakia] (Slovenská poľnohospodárská univerzita v Nitre, Nitra, Slovakia, 2016).

[28]

Doležel, J., Sgorbati, S. & Lucretti, S. Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content estimation in plants. Physiol. Plant 85, 625-631 (1992).

[29]

Veselý, P., Bureš, P., Šmarda, P. & Pavlíček, T. Genome size and DNA base composition of geophytes: the mirror of phenology and ecology?. Ann. Bot. 109, 65-75 (2012).

[30]

Otto, F. DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. Methods Cell Biol. 33, 105-110 (1990).

[31]

Masterson, J. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264, 421-424 (1994).

[32]

Hodgson, J. G. et al. Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog?. Ann. Bot. 105, 573-584 (2010).

[33]

Zhao, Y., Paule, J., Fu, C. & Koch, M. A. Out of China: distribution history of Ginkgo biloba L.. Taxon 59, 495-504 (2010).

[34]

Cao, F. S. An Illustrated Monograph of Ginkgo biloba L. Cultivars in China (Science Press, Bejing, China, 2011).

[35]

Isakov, Y. N., Butorina, A. K. & Muraya, L. S. Discovery of spontaneous haploids in Pinus silvestris and the prospects of their using in forest genetics and selection. Genetika 17, 701-707 (1981).

[36]

Andersen, S. B. in Haploids in Crop Improvement (eds Palmer, C. E., Keller, W. A. & Kasha, K. J.) pp 243-257 (Springer, Berlin, Heidelberg, Germany, 2005).

[37]

Dunwell, J. M. Haploids in flowering plants: origins and exploitation. Plant Biotechnol. J. 8, 377-424 (2010).

[38]

Chen, R. Y., Song, W. Q. & Li, X. L. in Proceedings of Sino-Japan Symposium on Plant Chromosome Research (ed Hong, D.) pp 381-386 (Organizing Committee of the Symposium, Bejing, China, 1989).

[39]

Lan, T. et al. Microdissection and painting of the W chromosome in Ginkgo biloba showed different labelling patterns. Bot. Stud. 49, 33-37 (2008).

[40]

Coder, K. D. Selected Ginkgo Forms and Cultivars (University of Georgia, Georgia, USA, 2003).

[41]

Murovec, J. & Bohanec, B. in Plant Breeding (ed. Abdurakhmonov, I.) pp 87-106 (inTech, Rijeka, Croatia, 2012).

[42]

Kasha, K. J. in Haploids in Crop Improvement II (eds Palmer, C. E., Keller, W. A. & Kasha, K. J. ) pp 123-152 (Springer, Heidelberg, Germany, 2005).

[43]

Kimber, G. & Riley, R. Haploid angiosperms. Bot. Rev. 29, 480-531 (1963).

[44]

Cook, M. T. Polyembryony in Ginkgo. Bot. Gaz. 36, 142 (1903).

[45]

Illies, Z. M. Auftreten haploider Keimlinge bei Picea abies. Naturwissenschaften 51, 442 (1964).

[46]

Dwivedi, S. L. et al. Haploids: constraints and opportunities in plant breeding. Biotechnol. Adv. 33, 812-829 (2015).

[47]

Neale, D. B. et al. Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol. 15, 1-13 (2014).

[48]

Harkess, A. et al. The asparagus genome shed light on the origin and evolution of a young Y chromosome. Nat. Commun. 18, 1279 (2017).

[49]

Guan, R. et al. Draft genome of the living fossil Ginkgo biloba. Gigascience 5, 49 (2016).

[50]

Abraham, A. & Mathew, P. M. Cytology of Encephalartos hildebrandtii A. Br. et Bouche. Ann. Bot. 30, 239-241 (1966).

[51]

Ramsey, J. & Schemske, D. W. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Ann. Rev. Ecol. Syst. 29, 467-501 (1998).

[52]

Johnsson, H. Observations on induced polyploidy in some conifers. Silvae Genet. 24, 62-68 (1975).

[53]

Christiansen, H. A tetraploid Larix decidua Miller. Det. K. Dan. Vidensk. Selsk. Biol. Medd. 18, 1-8 (1950).

[54]

Libby, W. J., Stettler, R. F. & Seitz, F. W. Forest genetics and forest tree breeding. Ann. Rev. Genet. 3, 469-494 (1969).

[55]

Nagata, T., Hasebe, M., Toriba, T., Taneda, H., & Crane, P. R. Sex conversion in Ginkgo biloba (Ginkgoaceae). J. Jpn. Bot. 91(Suppl.), 120-127 (2016).

[56]

Ming, R., Bendahmane, S. & Renner, S. S. Sex chromosomes in land plants. Ann. Rev. Plant Biol. 62, 485-514 (2011).

[57]

Charlesworth, D. Plant sex chromosome evolution. J. Exp. Bot. 64, 405-420 (2013).

[58]

Akagi, T., Henry, I. M., Tao, R. & Comai, L. A Y-chromosome-encoded small RNA acts as sex determinant in persimmons. Science 346, 646-650 (2014).

[59]

Osborn, T. C. et al. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19, 141-147 (2003).

[60]

Jackson, S. & Chen, Z. J. Genomic and expression plasticity of polyploidy. Curr. Opin. Plant. Biol. 13, 153-159 (2010).

[61]

Westergaard, M. The mechanism of sex determination in dioecious flowering plants. Adv. Genet. 9, 217-281 (1958).

[62]

Richards, A. J. Plant Breeding Systems (Chapman & Hall, London, UK, 1997).

[63]

Pannell, J. R., Obbard, D. J. & Buggs, R. J. A. Polyploidy and the sexual system: what can we learn from Mercurialis annua. Biol. J. Linn. Soc. 82, 547-560 (2004).

[64]

Russell, J. R. W. & Pannell, J. R. Sex determination in dioecious Mercurialis annua and its close diploid and polyploid relatives. Heredity 114, 262-271 (2015).

[65]

Cavalier-Smith, T. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann. Bot. 95, 147-175 (2005).

[66]

Stebbins, G. L. Variation and Evolution of Plants (Columbia University Press, New York, USA, 1950).

[67]

Beaulieu, J. M., Leitch, I. J., Patel, S., Pendharkar, A. & Knight, C. A. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytol. 179, 975-986 (2008).

[68]

Stebbins, G. L. Chromosomal Evolution in Higher Plants (Edward Arnold, London, UK, 1971).

[69]

Beaulieu, J. M. et al. Correlated evolution of genome size and seed mass. New Phytol. 173, 422-437 (2007).

[70]

Knight, C. A. & Beaulieu, J. M. Genome size scaling through phenotype space. Ann. Bot. 101, 759-766 (2008).

[71]

Lomax, B. H., Woodward, F. I., Leitch, I. J., Knight, C. A. & Lake, J. A. Genome size as a predictor of guard cell length in Arabidopsis thaliana is independent of environmental conditions. New Phytol. 181, 311-314 (2009).

[72]

McElwain, J. C. & Steinthorsdottir, M. Paleoecology, ploidy, paleoatmospheric composition, and developmental biology: a review of multiple uses of fossil stomata. Plant Physiol. 174, 650-664 (2017).

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