Holocentric Karyotype Evolution in Rhynchospora Is Marked by Intense
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ORIGINAL RESEARCH published: 10 September 2020 doi: 10.3389/fpls.2020.536507 Holocentric Karyotype Evolution in Rhynchospora Is Marked by Intense Numerical, Structural, and Genome Size Changes Edited by: 1 2† 1† 1 Hanna Weiss-Schneeweiss, Paula Burchardt , Christopher E. Buddenhagen , Marcos L. Gaeta , Murilo D. Souza , 3 1 University of Vienna, Austria Andre´ Marques * and Andre´ L. L. Vanzela * Reviewed by: 1 Laborato´ rio de Citogene´ tica e Diversidade Vegetal, Departamento de Biologia Geral, CCB, Universidade Estadual de Ekaterina D. Badaeva, Londrina, Londrina, Brazil, 2 Forage Science, AgResearch Limited, Hamilton, New Zealand, 3 Department of Chromosome Russian Academy of Sciences, Russia Biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany Eva Maria Temsch, University of Vienna, Austria Tae-Soo Jang, Cyperaceae is a family of Monocotyledons comprised of species with holocentric Chungnam National University, South Korea chromosomes that are associated with intense dysploidy and polyploidy events. Within *Correspondence: this family the genus Rhynchospora has recently become the focus of several studies that Andre´ L. L. Vanzela characterize the organization of the holocentric karyotype and genome structures. To [email protected] broaden our understanding of genome evolution in this genus, representatives of Andre´ Marques [email protected] Rhynchospora were studied to contrast chromosome features, C-CMA/DAPI band †ORCID: distribution and genome sizes. Here, we carried out a comparative analysis for 35 taxa Christopher E. Buddenhagen of Rhynchospora, and generated new genome size estimates for 20 taxa. The DNA 2C- orcid.org/0000-0002-3016-1054 Marcos L. Gaeta values varied up to 22-fold, from 2C = 0.51 pg to 11.32 pg, and chromosome numbers orcid.org/0000-0003-1260-9641 ranged from 2n = 4 to 61. At least 37% of our sampling exhibited 2n different from the basic number x = 5, and chromosome rearrangements were also observed. A large Specialty section: variation in C-CMA/DAPI band accumulation and distribution was observed as well. We This article was submitted to Plant Systematics and Evolution, show that genome variation in Rhynchospora is much larger than previously reported. a section of the journal Phylogenetic analysis showed that most taxa were grouped in clades corresponding to Frontiers in Plant Science previously described taxonomic sections. Basic chromosome numbers are the same Received: 20 February 2020 Accepted: 21 August 2020 within every section, however, changes appeared in all the clades. Ancestral chromosome Published: 10 September 2020 number reconstruction revealed n = 5 as the most likely ancestral complements, but n = Citation: 10 appears as a new possibility. Chromosome evolution models point to polyploidy as the Burchardt P, Buddenhagen CE, major driver of chromosome evolution in Rhynchospora, followed by dysploidy. A negative Gaeta ML, Souza MD, Marques A and Vanzela ALL (2020) Holocentric correlation between chromosome size and diploid number open the discussion for Karyotype Evolution in holokinetic drive-based genome evolution. This study explores relationships between Rhynchospora Is Marked by Intense Numerical, Structural, karyotype differentiation and genome size variation in Rhynchospora, and contrasts it and Genome Size Changes. against the phylogeny of this holocentric group. Front. Plant Sci. 11:536507. doi: 10.3389/fpls.2020.536507 Keywords: C-CMA/DAPI banding, chromosome numbers, DNA C-value, flow cytometry, karyotype diversity Frontiers in Plant Science | www.frontiersin.org1 September 2020 | Volume 11 | Article 536507 Burchardt et al. Differentiation of Holocentric Karyotypes in Rhynchospora INTRODUCTION Juncaceae (Malheiros et al., 1947), Droseraceae (Kondo et al., 1994) and Convolvulaceae (Pazy and Plitmann, 1987; Pazy and The size, morphology and composition of chromosomes have been Plitmann, 1994). useful parameters for comparing karyotypes of phylogenetically A number of cytogenetic studies compared Rhynchospora related species, and to resolve some taxonomic conflicts (Guerra, karyotypes (Luceño et al., 1998a; Vanzela and Guerra, 2000; 2000). These features have been widely regarded as drivers of Vanzela et al., 2000; Vanzela et al., 2003; Sousa et al., 2011; evolutionary processes (Comai, 2005; Doyle et al., 2008), as they are Michelan et al., 2012; Cabral et al., 2014; Marques et al., 2015; the result of duplication or deletion of entire chromosomes, Ribeiro et al., 2017; Ribeiro et al., 2018), but none compared polyploidy, fission, fusion, and/or chromosome translocation karyotype diversity with heterochromatin distribution and DNA (Greilhuber, 1995; Luceño and Guerra, 1996; Schubert C-value variation together, encompassing different clades. The and Lysak, 2011). We focus on karyotype evolution of genus Rhynchospora is the third largest clade in Cyperaceae Rhynchosporeae, a monophyletic clade in the Cyperaceae that (Araújo et al., 2012), with ca. 350 species distributed worldwide presents holocentric chromosomes, a trait that supposedly (Buddenhagen et al., 2017). Chromosome numbers vary from originated independently in four distinct clades of plants 2n =4inR. tenuis (Vanzela et al., 1996)to2n =62inR. faurieri (Melters et al., 2012). (Hoshino, 1987), although 2n = 10 is the most common number. Greilhuber (1995) considered holocentric chromosomes to be a Reports suggest a wide diversity with odd and even numbers, like synapomorphy of the Cyperid clade (Thurniaceae, Juncaceae and 2n = 4, 5, 8, 10, 12, 18, 20, 24, 26, 30, 36, 37, 45, 48, 50, and 58 Cyperaceae), and this characteristic has been accepted for (Luceño et al., 1998a; Luceño et al., 1998b; Vanzela et al., 2000; Rhynchospora since then (Vanzela et al., 2000; Vanzela and Arguelho et al., 2012; Ribeiro et al., 2018), and this high Colaço, 2002; Arguelho et al., 2012). However, Guerra et al. variability can also be observed within a single species, e.g. R. (2019) reported that Juncus L., a genus regarded as exclusively globosa (2n = 24, 36, 37, 45, 48, 50, and 58). holocentric, contains monocentric species. Also recently it was Rhynchospora has been used as a model for detailed studies reported that Prionium serratum (Thurniaceae) is also aiming to characterize holocentric chromosome structure and monocentric (Baez et al., 2020). More detailed work in this area adaptations taking place in these organisms (Cabral et al., 2014; is needed to provide insights into the evolution of holocentric Marques et al., 2015; Marques et al., 2016; Rocha et al., 2016). A chromosomes in Cyperales, such as whether it arose independently prior study examining the interspecificrelationshipsina in each of the major clades. phylogenetic context using cytogenetic data and DNA content In holocentric chromosomes, kinetochore proteins are has suggested polyploidy as the main driver of karyotype and arranged along the chromosomes and their kinetic activity genome evolution in Rhynchospora (Ribeiro et al., 2018). Despite appears to be distributed along almost the entire chromatid this and the high diversity of the genus, there are few studies surface (Melters et al., 2012; Heckmann and Houben, 2013). In approaching phylogenetic relationships with genomes and this case, any fragments produced by chromosome fission/ karyotype data. The most comprehensive analysis of the genus fusion may segregate regularly, making them more likely to was based on a traditional herbarium based taxonomic study of be inherited during cell division, and this can lead to increases 211 species (Kükenthal, 1949; Kükenthal, 1950a; Kükenthal, and decreases in chromosome numbers, giving rise to dysploidy 1950b; Kükenthal, 1951). (Mola and Papeschi, 2006; Arguelho et al., 2012). In contrast, In order to perform a comprehensive assessment of evolutionary fissioneventsinmonocentricchromosomesmaygenerate forces that have a role in Rhynchospora karyotype differentiation, acentric fragments that are unable to segregate normally and the number of Brazilian populations and species was expanded and are lost during cell division (Carrano and Heddle, 1973; phylogenetically compared, including never studied species. Efforts Escudero et al., 2015). were intended to compare intra- and interspecificvariationsin Cyperaceae members are well known for having large chromosome number, as well as to estimate DNA C-values and C- chromosome number variation associated with chromosome CMA/DAPI bands distribution. Data were compared and analyzed rearrangements, and Carex L. has the highest record of in a phylogenetic context, including samples from 14 different chromosome fission and fusion (Hipp, 2007; Roalson, 2008; taxonomic sections of the genus. Our data provide a window into Hipp et al., 2009). The increase in chromosome number by the group’s intraspecific variation, which helps to support polyploidy has also been proposed in genera such as Eleocharis polyploidy and dysploidy as the major drivers of genome and R.Br. (Da Silva et al., 2010; Zedek et al., 2010) and Rhynchospora karyotype evolution in Rhynchospora, and indicate the importance Vahl (Vanzela et al., 2000). High chromosome numbers were of wide sampling to include possible inter and intraspecific also found in Cyperus cyperoides Kuntze (n = 112; Tejavathi, variations in holocentric karyotypes. 1988), C. esculentus L. (n = 104; Sharma, 1970), Carex hirta L. (n =56–57; Luceño, 1994), and Rhynchospora faurieri Franch. (n = 31; Hoshino, 1987). But, the reduction below the probable basic MATERIALS AND METHODS chromosome