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Analysis of the Small Chromosomal Prionium Serratum (Cyperid)

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Analysis of the Small Chromosomal Prionium Serratum (Cyperid) bioRxiv preprint doi: https://doi.org/10.1101/2020.07.08.193714; this version posted July 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Analysis of the small chromosomal Prionium serratum (Cyperid) demonstrates 2 the importance of a reliable method to differentiate between mono- and 3 holocentricity 4 5 Baez, M.1,2,5; Kuo, Y.T.1,5; Dias, Y.1,2; Souza, T.1,3; Boudichevskaia, A.1,4; Fuchs, 6 J.1; Schubert, V.1; Vanzela, A.L.L.3, Pedrosa-Harand, A.2, Houben, A.1,6 7 8 1 Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, 9 06466 Stadt Seeland, Germany 10 2 Laboratory of Plant Cytogenetics and Evolution, Department of Botany, Federal 11 University of Pernambuco, Pernambuco, Brazil 12 3 Laboratory of Cytogenetics and Plant Diversity, Department of General Biology, 13 Center for Biological Sciences, State University of Londrina, Londrina 86057-970, 14 Paraná, Brazil 15 4 KWS SAAT SE & Co. KGaA, 37574, Einbeck, Germany 16 17 5 Shared first authorship 18 6 Corresponding author 19 ORCID: Houben: 0000-0003-3419-239X 20 21 Highlight 22 Prionium serratum is monocentric. Hence, holocentricity did not arise at the origin of 23 the Cyperid clade. 24 25 Running title 26 Prionium serratum is monocentric 27 28 Word count: 7378 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.08.193714; this version posted July 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 29 Abstract 30 For a long time, the Cyperid clade (Thurniceae-Juncaceae-Cyperaceae) was 31 considered as a group of species possessing holocentromeres exclusively. The basal 32 phylogenetic position of Prionium serratum L. f. Drège (Thurniceae) within Cyperids 33 makes this species an important specimen to understand the centromere evolution 34 within this clade. Unlike expected, the chromosomal distribution of the centromere- 35 specific histone H3 (CENH3), alpha-tubulin and different centromere associated post- 36 translational histone modifications (H3S10ph, H3S28ph and H2AT120ph) 37 demonstrate a monocentromeric organisation of P. serratum chromosomes. Analysis 38 of the high-copy repeat composition resulted in the identification of a centromere- 39 localised satellite repeat. Hence, monocentricity was the ancestral condition for the 40 Juncaceae-Cyperaceae-Thurniaceae Cyperid clade and holocentricity in this clade 41 has independently arisen at least twice after differentiation of the three families, once 42 in Juncaceae and the other one in Cyperaceae. Methods suitable for the 43 identification of holocentromeres are discussed. 44 45 Keywords 46 CENH3/CENPA, centromere type, holocentric chromosome, evolution, Cyperids, 47 Thurniceae 48 49 Introduction 50 Centromeres are essential for the segregation of chromosomes to the daughter cells 51 during mitosis and meiosis. Most organisms contain one single size-restricted 52 centromere per chromosome (monocentromere) visible as a primary constriction 53 during metaphase. However, in independent eukaryotic taxa, species with 54 chromosomes without distinct primary constrictions visible at metaphase exist, which 55 are referred to as holocentric. Instead, the spindle fibres attach along almost the 56 entire poleward surface of the chromatids (reviewed in Schubert et al. (2020)). 57 Holocentricity evolved at least 19 times independently in various green algae, 58 protozoans, invertebrates, and different higher plant families (Dernburg, 2001; 59 Escudero et al., 2016; Melters et al., 2012). In total, ~1.5 - 2.0% of flowering plants 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.08.193714; this version posted July 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 60 are likely to have holocentric chromosomes (Bures et al., 2012). It is possible that 61 holocentricity is even more common than reported so far, as the identification of the 62 centromere type, especially in small-sized chromosomes, is challenging. 63 64 One common explanation for the evolution of holocentric chromosomes is their 65 putative advantage related to DNA double-strand breaks (Zedek and Bures, 2018). 66 The studies on artificial chromosomal rearrangements in various holocentric species 67 showed that chromosome fragments retaining centromere activity are transmitted 68 during mitosis and meiosis (Jankowska et al., 2015). Comparisons of diversification 69 rates between monocentric and holocentric sister clades in animals and plants did 70 not detect an increase in diversification in holocentric species (Marquez-Corro et al., 71 2018). Nevertheless, these analyses depend on the correct identification of the 72 centromere type in a large number of lineages. 73 Because holocentric taxa are often embedded within broader phylogenetic lineages 74 possessing monocentric chromosomes, it is thought that holocentric chromosome 75 organisation originated from the monocentrics and that this transition occurred 76 independently in multiple phylogenetic lineages (Melters et al., 2012). However, the 77 factors that induced this transition and its mechanisms are currently unknown. 78 Investigations of the changes associated with the transition from monocentric to 79 holocentric chromosome organisation are, in theory, most informative when 80 phylogenetically closely related species that differ in the centromere type are 81 compared. 82 83 In angiosperms, holocentric chromosomes have been confirmed in some dicot 84 species, e.g. in the genus Cuscuta L. subgenus Cuscuta (Convolvulaceae) (Oliveira 85 et al., 2020) and in a few species within the genus Drosera L. (Droseraceae) (Sheikh 86 et al., 1995). Also, in monocots, for example, in the genus Luzula DC (Juncaceae) 87 (Heckmann et al., 2013) and Rhynchospora Vahl. (Cyperaceae) (Marques et al., 88 2015; Ribeiro et al., 2017) holocentricity occurs. These last two families belong to the 89 Cyperid clade (Thurniceae-Juncaceae-Cyperaceae), which was originally considered 90 to share holocentric chromosomes as a synapomorphic feature (Greilhuber, 1995; 91 Judd et al., 2016; Melters et al., 2012). However, exceptions have been reported in 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.08.193714; this version posted July 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 92 the genus Juncus L., in which four species exhibited primary constrictions (Marcelo 93 Guerra et al., 2019). It suggests that this synapomorphy of the Cyperid clade is 94 uncertain. 95 96 Aiming to improve the understanding on the origin and evolution of the holocentricity 97 within the Cyperid clade we studied the centromere organisation of Prionium 98 serratum L. f. Drège (Thurniceae), a species phylogenetically situated at the base of 99 the Cyperid clade (Silva et al., 2020) (Supp. Figure 1). The South African 100 monocotyledonous plant genus Prionium E. Mey is an old, species-poor lineage 101 which split from its sister genus about 26.1 million years ago (Kumar et al., 2017). P. 102 serratum is suspected to be holocentric, as it is closely related to the families 103 Juncaceae and Cyperaceae. Supported was this assumption by the fact that this 104 species has a low genomic GC content, as it is typically described for holocentric 105 species (Smarda et al., 2014). Furthermore, Zedek et al. (2016) observed no 106 significant increase in the proportion of G2 nuclei after gamma irradiation of P. 107 serratum, differing from monocentric species. 108 109 To ascertain the centromere type of P. serratum, we determined the chromosomal 110 distribution of the centromere-specific histone H3 (CENH3) protein, alpha-tubulin, 111 histone H3 phosphorylated at position serine 10, serine 28 (H3S10ph, H3S28ph) and 112 histone H2A phosphorylated at position threonine 120 (H2AT120ph). The cell cycle- 113 dependent post-translational histone modifications are associated with active 114 centromeres (Demidov et al., 2014; Dong and Han, 2012; Gernand et al., 2003). 115 Unlike expected, a monocentromeric organisation of the chromosomes was found. 116 The analysis of the high-copy repeat composition resulted in the identification of two 117 centromere-localised satellite repeats. In addition, a DNA replication behaviour was 118 found typical for small genome monocentric species. The data are discussed in the 119 context of centromere evolution in Cyperids and concerning the suitability of available 120 methods to identify holocentromeres. 121 122 Materials and methods 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.07.08.193714; this version posted July 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 123 Plant material 124 Individuals of Prionium serratum L. f. Drège, collected in western Cape (Cape Town, 125 South Africa; TE2016_413) and provided by the Herrenhäuser Gardens (Hannover, 126 Germany, IPK herbarium 70142) and the Botanical Garden Halle (Halle, Germany) 127 were grown in a greenhouse of the Leibniz Institute of Plant Genetics and Crop Plant 128 Research (IPK Gatersleben, Germany). 129 130 Flow cytometric genome size measurement 131
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