ORIGINAL ARTICLE
 
HIGHLIGHTS
  • Plants perceived to have undergone whole genome duplication at or near the Cretaceous/Paleogene boundary exhibit greater numbers of late embryogenesis abundant (LEA) genes than plants that did not.
  • LEA genes confer desiccation tolerance and seed longevity.
  • These data support paleobotanical datasets that suggest plants capable of forming relatively long-lived, frost-tolerant seed banks preferentially crossed the KPB.
KEYWORDS
ABSTRACT
Paleobotanists debate whether the Cretaceous/Paleogene boundary (KPB) event was selective. As the hypothesis that the KPB event selected for plants with fast-return leaf economic traits (e.g. deciduousness) has lost empirical support in recent investigations, researchers have turned to alternative hypotheses to explain an abrupt decline in primary productivity across the KPB. Two contemporary hypotheses designed to explain selectivity among plants across the KPB are that (1) polyploids exhibited greater survivorship than their diploid progenitors or counterparts (i.e. the KPB-whole genome duplication or WGD hypothesis) and that (2) plants with desiccation-tolerant (DT), i.e. orthodox, seeds exhibited greater survivorship than plants with desiccationsensitive (DS), also known as recalcitrant, seeds. Late embryogenesis abundant (LEA) protein gene families are perceived to confer DT and seed longevity among vascular plants. Non-parametric Wilcoxon signed-rank test for matched pairs and a Mann-Whitney U test reveal that plant lineages perceived to have undergone WGD across the KPB exhibit significantly greater numbers of LEA genes than those that did not. On the basis of these data, this investigation elicits a merger between the KPB-WGD and KPB-seed traits concepts. However, emphasis is shifted from the concept of WGD as an immediate adaptation to climatic stress at the KPB (the KPB-WGD hypothesis) to the concept that WGD was an exaptation, which, by definition, fortuitously enhanced the survival of vascular plants across the KPB but that probably evolved initially in other climatic contexts.
REFERENCES (101)
1.
Artur, M.A.S., Zhao, T., Ligterink, W., Schranz, E., Hilhorst, H.W.M., 2019a. Dissecting the genomic diversification of late embryogenesis abundant (LEA) protein gene families in plants. Genome Biology and Evolution 11, 459–471. https://doi.org/10.1093/gbe/ev....
 
2.
Artur, M.A.S., Rienstra, J., Dennis, T.J., Farrant, J.M., Ligterink, W., Hilhorst, H., 2019b. Structural plasticity of intrinsically disordered LEA proteins from Xerophyta schlechteri provides protection in vitro and in vivo. Fron-tiers in Plant Science 10, 1–15. https://doi.org/10.3389/fpls.2....
 
3.
Aziz, M.A., Sabeem, M., Mullath, S.K., Brini, F., Masmoudi, K., 2021. Plant group II LEA proteins: intrinsically disordered structure for multiple functions in response to environmental stresses. Biomolecules 11, 1–27. https://doi.org/10.3390/biom11....
 
4.
Barker, W.G., Johnston, G.R., 1980. The longevity of seeds of the common potato, Solanum tuberosum. American Potato Journal 57, 601–607. https://doi.org/10.1007/BF0285....
 
5.
Barreda, V.D., Cúneo, N.R., Wilf, P., Currano, E.D., Scasso, R.A., Brinkhuis, H., 2012. Cretaceous/Paleogene floral turnover in Patagonia: drop in diversity, low extinction, and a Classopollis spike. PLoS ONE 7, 1–8. https://doi.org/10.1371/journa....
 
6.
Barrett, C.F., McKain, M.R., Sinn, B.T., Ge, X.-J., Zhang, Y., Antonelli, A., Bacon, C.D., 2019. Ancient polyploidy and genome evolution in palms. Genome Biology and Evolution 11, 1501–1511. https://doi.org/10.1093/gbe/ev....
 
7.
Baskin C.C., Baskin J.M., 2014. Seeds: Ecology, Biogeography, and Evolution: Second Edition. Academic Press, San Diego.
 
8.
Belzunce, M., Navarro, R.M., Rapoport, H.F., 2008. Posidonia oceanica seeds from drift origin: viability, germination and early plantlet development. Botanica Marina 51, 1–9. https://doi.org/10.1515/BOT.20....
 
9.
Berry, K., 2020. Seed traits linked to differential survival of plants during the Cretaceous/Paleogene impact winter. Acta Palaeobotanica 60, 307–322. https://doi.org/10.35535/acpa-....
 
10.
Berry, K., 2022a. Which is more appropriate for deciphering recursive patterns in plant recovery across the Trias-sic/Jurassic and Cretaceous/Paleogene boundaries, nomothetic or idiographic approaches? New Mexico Museum of Natural History and Science Bulletin 90: Fossil Record 8, 1–8.
 
11.
Berry K., 2022b. Was the K/Pg boundary Classopollis spike a singular event? Review of global palynological records suggests otherwise, with broad implications. Rocky Mountain Geology 57, 17–29.
 
12.
Berry, K., 2022c. Paleobiogeography of the stenochlaenoid ferns: Using fossils and molecules to investigate macroevolutionary patterns and processes. International Journal of Plant Sciences 183, 268–278. https://doi.org/10.1086/718576.
 
13.
Berry, K., 2022d. Conifer turnover across the K/Pg boundary in Colorado, U.S.A., parallels South American pat-terns: New and emerging perspectives. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen 303, 11–28. https://doi.org/10.1127/njgpa/....
 
14.
Berry, K., 2022e. A Classopollis “spike” in the Rugubivesiculites Zone of the Kayan Sandstone, western Sarawak, Borneo, suggests a Danian age for these deposits. Review of Palaeobotany and Palynology 304, 104728. https://doi.org/10.1016/j.revp....
 
15.
Blanc, G., Wolfe, K.H., 2004. Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. The Plant Cell 16, 1679–1691. https://doi.org/10.1105/tpc.02....
 
16.
Blonder, B., Royer, D.L., Johnson, K.R., Miller, I., Enquist, B.J., 2014. Plant ecological strategies shift across the Cretaceous-Paleogene boundary. PLoS Biology 12, 1–7. https://doi.org/10.1371/journa....
 
17.
Butrim, M.J., Royer, D.L., Miller, I.M., Dechesne, M., Neu-Yagle, N., Lyson, T.R., Johnson, K.R., Barclay, R.S., 2022. No consistent shift in leaf dry mass per area across the Cretaceous-Paleogene boundary. Frontiers in Plant Science 13, 1–11. https://doi.org/10.3389/fpls.2....
 
18.
Carvalho, M.R., Jaramillo, C., de la Parra, F., Caballero-Rodríguez, F.H., Wing, S., Turner, B.L., D’Apolito, C., Romero-Báez, M., Narváez, P., Martínez, C., Gutierrez, M., Labandeira, C., Bayona, G., Rueda, M., Paez-Reyes, M., Cárdenas, D., Duque, A., Crowley, J.L., Santos, C., Silvestro, D., 2021. Extinction at the end-Cretaceous and the origin of modern neotropical rainforests. Science 372, 63–68. https://doi.org/10.1126/scienc....
 
19.
Centeno-González, N.K., Martínez-Cabrera, H.I., Porras-Múzquiz, H., Estrada-Ruiz, E., 2021. Late Campanian fossil of a legume fruit supports Mexico as a center of Fabaceae radiation. Communications Biology 4, 1–8. https://doi.org/10.1038/s42003....
 
20.
Chain, F.J.J., Dushoff, J., Evans, B.J., 2011. The odds of duplicate gene persistence after polyploidization. BMC Genomics 12, 1–7. https://doi.org/10.1186/1471-2....
 
21.
Chen, Y., Li, C., Zhang, B., Yi, J., Yang, Y., Kong, C., Lei, C., Gong, M., 2019. The role of the Late Embryogene-sis-Abundant (LEA) protein family in development and the abiotic stress response: a comprehensive expression analysis of potato (Solanum tuberosum). Genes 10, 1–16. https://doi.org/10.3390/genes1....
 
22.
Chiarenza, A.A., Farnsworth, A., Mannion, P.D., Lunt, D.J., Valdes, P.J., Morgan, J.V., Allison, P.A., 2020. Asteroid impact, not volcanism, caused the end-Cretaceous dinosaur extinction. Proceedings of the National Academy of Sciences USA 117, 17084–17093. https://doi.org/10.1073/pnas.2....
 
23.
Clark, J.W., Donoghue, P.C.J., 2017. Constraining the timing of whole genome duplication in plant evolutionary history. Proceedings of the Royal Society of London, Series B 284, 1–8. https://doi.org/10.1098/rspb.2....
 
24.
Clark, J.W., Donoghue, P.C.J., 2018. Whole-genome duplication and plant macroevolution. Trends in Plant Science 23, 933–945. https://doi.org/10.1016/j.tpla....
 
25.
Clark, J.W., Puttick, M.N., Donoghue, P.C.J., 2019. Origin of horsetails and the role of whole-genome duplication in plant macroevolution. Proceedings of the Royal Society of London, Series B 286, 1–10. https://doi.org/10.1098/rspb.2....
 
26.
Costa, M.-C. D., Artur, M.A.S., Maia, J., Jonkheer, E., Derks, M.F.L., Nijveen, H., Williams, B., Mundree, S.G., Jiménez-Gómez, J.M., Hesselink, T., Schijlen, E.G.W.M., Ligterink, W., Oliver, M.J., Farrant, J.M., Hilhorst, H.W.M., 2017. A footprint of desiccation tolerance in the genome of Xerophyta viscosa. Nature Plants 3, 1–11. https://doi.org/10.1038/nplant....
 
27.
Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer Associates, Oxford, 480 p.
 
28.
Da Silva, D.M., Da Silva Sylvestre, L., Ferreira Mendonça, C.B., Gonçalves-Esteves, V., 2019. Spore diversity among species of Blechnaceae in the Atlantic forest. Acta Palaeobotanica Brasilica 33, 1–13. https://doi.org/10.1590/0102-3....
 
29.
De Casas, R.B., Willis, C.G., Pearse, W.D., Baskin, C.C., Baskin, J.M., Cavender-Bares, J., 2017. Global biogeog-raphy of seed dormancy is determined by seasonality and seed size: a case study in the legumes. New Phytologist 214, 1527–1536. https://doi.org/10.1111/nph.14....
 
30.
Delahaie, J., Hundertmark, M., Bove, J., Leprince, O., Rogniaux, H., Buitink, J., 2013. LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance. Journal of Experimental Botany 64, 4559–4573. https://doi.org/10.1093/jxb/er....
 
31.
Fawcett, J.A., Maere, S., Van de Peer, Y., 2009. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proceedings of the National Academy of Sciences USA 106, 5737–5742. https://doi.org/10.1073/pnas.0....
 
32.
Freeling, M., 2017. Picking up the ball at the K/Pg boundary: The distribution of ancient polyploidies in the plant phylogenetic tree as a spandrel of asexuality with occasional sex. The Plant Cell 29, 202–206. https://doi.org/10.1105/tpc.16....
 
33.
Gould, S.J., 2002. The Structure of Evolutionary Theory. The Belknap Press of Harvard University, Cambridge, pp. 1296–1332.
 
34.
Gould, S.J., Lewontin, R.C., 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London, Series B 205, 581–598. https://doi.org/10.1098/rspb.1....
 
35.
Gould, S.J., Vrba, E.S., 1982. Exaptation – a missing term in the science of form. Paleobiology 8, 4–15. https://doi.org/10.1017/S00948....
 
36.
Gout, J.-F., Lynch, M., 2015. Maintenance and loss of duplicated genes by dosage subfunctionalization. Molecular Biology and Evolution 32, 2141–2148. https://doi.org/10.1093/molbev....
 
37.
Greenwood, D., Christophel, D., 2005. The origins and Tertiary history of Australian “tropical” rainforests. In: Bermingham, E., Dick, C.W., Moritz, C. (eds), Tropical Rainforests: Past, Present, and Future. University of Chicago Press, Chicago, 322–335.
 
38.
Hart, M.B., FitzPatrick, M.E.J., Smart, C.W., 2016. The Cretaceous/Paleogene boundary: Foraminifera, sea grasses, sea level change and sequence stratigraphy. Palaeogeography, Palaeoclimatology, Palaeoecology 441, 420–429. https://doi.org/10.1016/j.pala....
 
39.
Herendeen, P.S., Cardoso, D.B.O.S., Herrera, F., Wing, S.L., 2022. Fossil papilionoids of the Bowdichia clade (Le-guminosae) from the Paleogene of North America. American Journal of Botany 109, 130–150. https://doi.org/10.1002/ajb2.1....
 
40.
Huang, C.-H., Qi, X., Chen, D., Qui, J., Ma, H., 2020. Recurrent genome duplication events likely contributed to the ancient and recent rise of ferns. Journal of Integrative Plant Biology 62, 433–455. https://doi.org/10.1111/jipb.1....
 
41.
Jaganathan, G.K., 2021. Ecological insights into the coexistence of dormancy and desiccation-sensitivity in Are-caceae species. Annals of Forest Science 78: 1–14. https://doi.org/10.1007/s13595....
 
42.
Jaganathan, G.K., Dalrymple, S., Liu, B., 2015. Towards an understanding of factors controlling seed bank compo-sition and longevity in the alpine environment. The Botanical Review 81, 70–103. https://doi.org/10.1007/s12229....
 
43.
Jacobs, B.F., 2004. Palaeobotanical studies from tropical Africa: relevance to the evolution of forest, woodland and savannah biomes. Philosophical Transactions: Biological Sciences 359, 1573–1583. https://doi.org/10.1098/rstb.2....
 
44.
Jacobs, B.F., Currano, E.D., 2021. The impactful origin of neotropical rainforests: A mass extinction event led to vast diversity and structural complexity of neotropical rainforests. Science 372, 28–29. https://doi.org/10.1126/scienc....
 
45.
Johnson, K.R., 2002. The megaflora of the Hell Creek and lower part of the Fort Union formations in the western Dakotas: vegetational response to climate change, the Cretaceous-Tertiary boundary event, and rapid marine transgression. Geological Society of America Special Papers 361, 329–391. https://doi.org/10.1130/0-8137....
 
46.
Junium, C.K., Zerkle, A.L., Witts, J.D., Ivany, L.C., Yancey, T.E., Liu, C., Claire, M.W., 2022. Massive perturbations to atmospheric sulfur in the aftermath of the Chicxulub impact. Proceedings of the National Academy of Sciences USA 119, 1–7. https://doi.org/10.1073/pnas.2....
 
47.
Koenen, E.J.M., Ojeda, D.I., Bakker, F.T., Wieringa, J.J., Kidner, C., Hardy, O.J., Pennington, R.T., Herendeen, P.S., Bruneau, A., Hughes, C.E., 2021. The origin of legumes is a complex paleopolyploid phylogenomic tangle closely associated with the Cretaceous-Paleogene (K/Pg) mass extinction event. Systematic Biology 70, 508–526. https://doi.org/10.1093/sysbio....
 
48.
Leck, M.A., Parker, V.T., Simpson, R.L., 1989. Ecology of soil seed banks. Academic Press, Inc., San Diego, 462 p.
 
49.
Lee, H.T., Golicz, A.A., Bayer, P.E., Jiao, Y., Tang, H., Paterson, A.H., Sablok, G., Krishnaraj, R.R., Chan, C.-K.K., Batley, J., Kendrick, G.A., Larkhum, A.W.D., Ralph, P.J., Edwards, D., 2016. The genome of a Southern Hemi-sphere seagrass species (Zostera muelleri). Plant Physiology 172, 272–283. https://doi.org/10.1104/pp.16.....
 
50.
Li, Z., Defoort, J., Tasdighian, S., Maere, S., Van de Peer, Y., De Smet, R., 2016. Gene duplicability is highly con-sistent across all angiosperms. The Plant Cell 28, 326–344. https://doi.org/10.1105/tpc.15....
 
51.
Lohaus, R., Van de Peer, Y., 2016. Of dups and dinos: evolution at the K/Pg boundary. Current Opinion in Plant Biology 30, 62–69. https://doi.org/10.1016/j.pbi.....
 
52.
Lomax, B.H., Hilton, J., Bateman, R.M., Upchurch, G.R., Jr., Lake, J.A., Leitch, I.J., Cromwell, A., Knight, C.A., 2014. Reconstructing relative genome size of vascular plants through geological time. New Phytologist 201, 636–644. https://doi.org/10.1111/nph.12....
 
53.
Long, R.L., Gorecki, M.J., Renton, M., Scott, J.K., Colville, L., Goggin, D.E., Commander, L.E., Westcott, D.A., Cherry, H., Finch-Savage, W.E., 2015. The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biological Reviews 90, 31–59. https://doi.org/10.1111/brv.12....
 
54.
Lyall, R., Schlebusch, S.A., Proctor, J., Prag, M., Hussey, S.G., Ingle, R.A., Illing, N., 2020. Vegetative desiccation tolerance in the resurrection plant Xerophyta humilis has not evolved through reactivation of the seed canonical LAFL regulatory network. The Plant Journal 101, 1349–1367. https://doi.org/10.1111/tpj.14....
 
55.
Lynch, M., Conery, J.S., 2000. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155. https://doi.org/10.1126/scienc....
 
56.
Lyson, T.R., Miller, I.M., Bercovici, A.D., Weissenburger, K., Fuentes, A.J., Clyde, W.C., Hagadorn, J.W., Butrim, M.J., Johnson, K.R., Fleming, R.F., Barclay, R.S., MacCracken, S.A., Lloyd, B., Wilson, G.P., Krause, D.W., Chester, S.G.B., 2019. Exceptional continental record of biotic recovery after the Cretaceous-Paleogene mass extinction. Science 366, 977–983. https://doi.org/10.1126/scienc....
 
57.
Maere, S., De Bodt, S., Raes, J., Casneuf, T., Montagu, M.V., Kuiper, M., Van de Peer, Y., 2005. Modeling gene and genome duplications in eukaryotes. Proceedings of the National Academy of Sciences, USA 102, 5454–5459. https://doi.org/10.1073/pnas.0....
 
58.
Mann, H.B., Whitney, D.R., 1947. On a test of whether one or two random variables is stochastically larger than the other. Annals of Mathematical Statistics 18, 50–60.
 
59.
Marques, A., 2018. Desiccation sensitive seeds: Understanding their evolution, genetics and physiology. Ph.D. Thesis, Wageningen University, Wageningen, the Netherlands, 189 p.
 
60.
Martínez-Cabrera, H.I., Estrada-Ruiz, E., 2014. Wood anatomy reveals high theoretical hydraulic conductivity and low resistance to vessel implosion in a Cretaceous fossil forest from northern Mexico. PLoS ONE 9, 1–11. https://doi.org/10.1371/journa....
 
61.
Matilla, A.J., 2022. The orthodox dry seeds are alive: a clear example of desiccation tolerance. Plants 11, 1–20. https://doi.org/10.3390/plants....
 
62.
Moreno-Dominguez, R., Cascales-Miñana, B., Ferrer, J., Diez, J.B., 2016. First record of the mangrove palm Nypa from the northeastern Ebro Basin, Spain: with taphonomic criteria to evaluate the drifting duration. Geologica Acta 14, 101–111.
 
63.
Morgan, J.V., Bralower, T.J., Brugger, J., Wünneman, K., 2022. The Chicxulub impact and its environmental con-sequences. Nature Reviews Earth and Environment 3, 338–354. https://doi.org/10.1038/s43017....
 
64.
Morley, R.J., 1998. Palynological evidence for Tertiary plant dispersals in the SE Asian region in relation to plate tectonics and climate. In: Hall, R., Holloway, J.D. (eds), Biogeography and Geological Evolution of SE Asia. Backbuys Publishers, Leiden, The Netherlands, pp. 211–234.
 
65.
Muller, J., 1968. Palynology of the Pedawan and Plateau Sandstone Formations (Cretaceous – Eocene) in Sarawak, Malaysia. Micropaleontology 14, 1–37.
 
66.
Nichols, D.J., Johnson, K.R., 2008. Plants and the K-T boundary. Cambridge University Press, Cambridge.
 
67.
Olsen, J.L., Rouzé, P., Verhelst, B., Lin, Y.-C., Bayer, T., Collen, J., Dattolo, E., De Paoli, E., Dittami, S., Maumus, F., Michel, G., Kersting, A., Lauritano, C., Lohaus, R., Töpel, M., Tonon, T., Vanneste, K., Amirebrahimi, M., Brakel, J., Boström, C., Chovatia, M., Grimwood, J., Jenkins, J.W., Jueterbock, A., Mraz, A., Stam, W.T., Tice, H., Bornberg-Bauer, E., Green, P.J., Pearson, G.A., Procaccini, G., Duarte, C.M., Schmutz, J., Reusch, T.B.H., Van de Peer, Y., 2016. The genome of the seagrass Zosteria marina reveals angiosperm adaptation to the sea. Nature 530, 331–335. https://doi.org/10.1038/nature....
 
68.
Orth, R.J., Harwell, M.C., Inglis, G.J., 2006. Ecology of seagrass seeds and dispersal strategies. In: Larkum, A.W.D., Orth, R.J., Duarte, C.M. (eds), Seagrasses: Biology, Ecology and Conservation. Springer, Dordrecht, The Nether-lands, pp. 111–133.
 
69.
Pan, A.D., Jacobs, B.F., Dransfield, J., Baker, W.J., 2006. The fossil record of palms (Arecaceae) in Africa and new records from the Late Oligocene (28–27 Mya) of north-western Ethiopia. Botanical Journal of the Linnean So-ciety 151, 69–81. https://doi.org/10.1111/j.1095....
 
70.
Quattrocchio, M.E., 2006. Palynology and paleocommunities of the Paleogene of Argentina. Revista Brasileira de Paleontology 9, 101–108.
 
71.
Quattrocchio, M.E., Martínez, M.A., Hinojosa, L.F., Jaramillo, C., 2013. Quantitative analysis of Cenozoic paly-nofloras from Patagonia, southern South America. Palynology 37, 246–258. https://doi.org/10.1080/019161....
 
72.
Roberts, E. H., 1973. Predicting the Storage Life of Seeds. Seed Science and Technology 1, 499–514.
 
73.
Royer, D.L., Osborne, C.P., Beerling, D.J., 2003. Carbon loss by deciduous trees in a CO2-rich ancient polar envi-ronment. Nature 424, 60–62. https://doi.org/10.1038/nature....
 
74.
Sano, N., Rajjou, L., North, H.M., Debeaujon, I., Marion-Poll, A., Seo, M., 2016. Staying alive: molecular aspects of seed longevity. Plant and Cell Physiology 57, 660–674. https://doi.org/10.1093/pcp/pc....
 
75.
Sessa, E.B., 2019. Polyploidy as a mechanism for surviving global change. New Phytologist 221, 5–6. https://doi.org/10.1111/nph.15....
 
76.
Sharma, G.S., 2022. Structural and functional role of plant dehydrins in enhancing stress tolerance. In: Roy, S., Mathur, P., Chakraborty, A.P., Saha, S.P. (eds), Plant Stress: Challenges and Management in the New Decade. Cham, Switzerland, Springer Nature, pp. 111–122.
 
77.
Shen-Miller, J., Lindner, P., Xie, Y., Villa, S., Wooding, K., Clarke, S.G., Loo, R.R.O., Loo, J.A., 2013. Thermal-stable proteins of fruit of long-living Sacred Lotus Nelumbo nucifera Gaertn. var. China Antique. Tropical Plant Biology 6, 1–29. https://doi.org/10.1007/s12042....
 
78.
Shi, T., Rahmani, R.S., Gugger, P.F., Wang, M., Li, H., Zhang, Y., Li, Z., Wang, Q., Van de Peer, Y., Marchal, K., Chen, J., 2020. Distinct expression and methylation patterns for genes with different fates following a single whole-genome duplication in flowering plants. Molecular Biology and Evolution 37, 2394–2413. https://doi.org/10.1093/molbev....
 
79.
Smolikova, G., Leonova, T., Vashurina, N., Frolov, A., Medvedev, S., 2021. Desiccation tolerance as the basis of long-term seed viability. International Journal of Molecular Sciences 22, 1–24. https://doi.org/10.3390/ijms22....
 
80.
Soltis, D.E., Burleigh, J.G., 2009. Surviving the K-T mass extinction: New perspectives on polyploidization in an-giosperms. Proceedings of the National Academy of Sciences, USA 106, 5455–5456. https://doi.org/10.1073/pnas.0....
 
81.
Soltis, D.E., Albert, V.A., Leebens-Mack, J., Bell, C.D., Paterson, A.H., Zheng, C., Sankoff, D., DePamphilis, C.W., Wall, P.K., Soltis, P.S., 2009. Polyploidy and angiosperm diversification. American Journal of Botany 96, 336–348. https://doi.org/10.3732/ajb.08....
 
82.
Soltis, D.E., Segovia-Salcedo, M.C., Jordan-Thaden, I., Majure, L., Miles, N.M., Mavrodiev, E.V., Mei, W., Cortez, M.B., Soltis, P.S., Gitzendammer, M.A., 2014. Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytologist, 1105–1117.
 
83.
Stebbins, G.L., 1950. Variation and Evolution in Plants. Columbia University Press, New York.
 
84.
Tabor, C.R., Bardeen, C.G., Otto-Bliesner, B.L., Garcia, R.R., Toon, O.B., 2020. Causes and climatic consequences of the impact winter at the Cretaceous-Paleogene boundary. Geophysical Research Letters 47, 1–10. https://doi.org/10.1029/2019GL....
 
85.
Tasdighian, S., Van Bel, M., Li, Z., Van de Peer, Y., Carreto-Paulet, L., Maere, S., 2017. Reciprocally retained genes in the angiosperm lineage show the hallmarks of dosage balance sensitivity. The Plant Cell 29, 2766–2785. https://doi.org/10.1105/tpc.17....
 
86.
Vajda, V., Bercovici, A., 2014. The global vegetation pattern across the Cretaceous-Paleogene mass extinction in-terval: A template for other extinction events. Global and Planetary Change 122, 29–49. https://doi.org/10.1016/j.glop....
 
87.
Van der Ham, R.W.J.M., Van Konijnenburg-van Cittert, J.H.A., Indeherberge, L., 2007. Seagrass foliage from the Maastrichtian type area (Maastrichtian, Danian, NE Belgium, SE Netherlands). Review of Palaeobotany and Palynology 144, 301–321. https://doi.org/10.1016/j.revp....
 
88.
Van de Peer, Y., Ashman, T.L., Soltis, P.S., Soltis, D.E., 2021. Polyploidy: an evolutionary and ecological force in stressful times. The Plant Cell 33, 1–16. https://doi.org/10.1093/plcell....
 
89.
Van de Peer, Y., Mizrachi, E., Marchal, K., 2017. The evolutionary significance of polyploidy. Nature Review Ge-netics 18, 411–424. https://doi.org/10.1038/nrg.20....
 
90.
Vanneste, K., Maere, S., Van de Peer, Y., 2014. Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philosophical Transactions of the Royal Society of London, Series B 369, 1–13. https://doi.org/10.1098/rstb.2....
 
91.
Vanneste, K., Sterck, L., Myburg, A.A., Van de Peer, Y., Mizrachi, E., 2015. Horsetails are ancient polyploids: evi-dence from Equisetum giganteum. Plant Cell 27, 1567–1578. https://doi.org/10.1105/tpc.15....
 
92.
Verdier, J., Lalanne, D., Pelletier, S., Torres-Jerez, I., Righetti, K., Bandyopadhyay, K., Leprince, O., Chatelain, E., Ly Vu, B., Gouzy, J., Gamas, P., Udvardi, M.K., Buitink, J., 2013. A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago trun-catula seeds. Plant Physiology 163, 757–774. https://doi.org/10.1104/pp.113....
 
93.
Wang, D., Sun, X.Y., Zhao, Y.N., 1990. Late Cretaceous to Tertiary palynofloras in Xinjiang and Qinghai, China. Review of Palaeobotany and Palynology 65, 95–104. https://doi.org/10.1016/0034-6....
 
94.
Wilcoxon, F., 1945. Individual comparisons by ranking methods. Biometrics Bulletin 1, 80–83.
 
95.
Wolfe, J.A., Upchurch, G.R., Jr., 1987. Leaf assemblages across the Cretaceous-Tertiary boundary in the Raton Basin, New Mexico and Colorado. Proceedings of the National Academy of Sciences, USA 84, 5096–5100.
 
96.
Wood, T.E., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B., Rieseberg, L.H., 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences, USA 106, 13875–13879. https://doi.org/10.1073/pnas.0....
 
97.
Wu, H., Ma, T., Kang, M., Ai, F., Dong, G., Liu, J., 2019. A high-quality Actinidia chinensis (kiwifruit) genome. Horticulture Research 6, 1–9. https://doi.org/10.1038/s41438....
 
98.
Wu, S., Han, B., Jiao, Y., 2020. Genetic contribution of paleopolyploidy to adaptive evolution in angiosperms. Mo-lecular Plant 13, 59–71. https://doi.org/10.1016/j.molp....
 
99.
Xu, S., Xu, S., Zhou, Y., Gu, R., Zhang, X., Yue, S., 2020. Long-term seed storage for desiccation sensitive seeds in the marine foundation species Zostera marina L. (eelgrass). Global Ecology and Conservation 24, 1–11. https://doi.org/10.1016/j.gecc....
 
100.
Zanne, A.E., Tank, D.C., Cornwell, W.K., Eastman, J.M., Smith, S.A., FitzJohn, R.G., McGlinn, D.J., O'Meara, B.C., Moles, A.T., Reich, P.B., Royer, D.L., Soltis, D.E., Stevens, P.F., Westoby, M., Wright, I.J., Aarssen, L., Bertin, R.I., Calaminus, A., Govaerts, R., Hemmings, F., Leishman, M.R., Oleksyn, J., Soltis, P.S., Swenson, N.G., Warman, L., Beaulieu, J.M., 2014. Three keys to the radiation of angiosperms into freezing environments. Na-ture 506, 89–92. https://doi.org/10.1038/nature....
 
101.
Zhao, Y., Zhang, R., Jiang, K.-W., Qi, J., Hu, Y., Guo, J., Zhu, R., Zhang, T., Egan, A.N., Yi, T.-S., Huang, C.-H., Ma, H., 2021. Nuclear phylotranscriptomics and phylogenomics support numerous polyploidization events and hy-potheses for the evolution of rhizobial nitrogen-fixing symbiosis in Fabaceae. Molecular Plant 14, 748–773. https://doi.org/10.1016/j.molp....
 
eISSN:2082-0259
ISSN:0001-6594
Journals System - logo
Scroll to top