DOCSLIB.ORG

Ribosomal RNA Genes Evolution in Tragopogon: a Story of New and Old World Allotetraploids and the Synthetic Lines

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Ribosomal RNA Genes Evolution in Tragopogon: a Story of New and Old World Allotetraploids and the Synthetic Lines Malinska & al. • Evolution of rDNA in Tragopogon TAXON 60 (2) • April 2011: 348–354 Ribosomal RNA genes evolution in Tragopogon: A story of New and Old World allotetraploids and the synthetic lines Hana Malinska,1 Jennifer A. Tate,2 Evgeny Mavrodiev,2 Roman Matyasek,1 K. Yoong Lim,3 Andrew R. Leitch,3 Douglas E. Soltis,2 Pamela S. Soltis4 & Ales Kovarik1 1 Institute of Biophysics, Academy of Sciences of the Czech Republic, v.v.i, Laboratory of Molecular Epigenetics, Královopolská 135, 61265 Brno, Czech Republic 2 Department of Botany, University of Florida, Gainesville, Florida 32611, U.S.A. 3 School of Biological Sciences, Queen Mary, University of London, E1 4NS, U.K. 4 Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611, U.S.A. Authors for correspondence: Hana Malinska, [email protected] and Ales Kovarik, [email protected] Abstract Tragopogon mirus Ownbey and Tragopogon miscellus Ownbey are recent allotetraploids that have formed recurrently within the last 80 years, following the introduction of the diploids T. dubius Scop., T. pratensis L. and T. porrifolius L. from Europe to North America. In some areas, the progenitor diploids still occur along with expanding populations of the allotetra- ploids, and the polyploids at those locations likely represent descendents of the nearby diploids. In most natural populations of T. mirus and T. miscellus, there are far fewer rDNA units of the common parent (T. dubius) than there are of the other diploid parent and in some rarely occurring individuals, one parental locus was >90% deleted. Nevertheless, in contrast to several ancient Old World allotetraploids, gene copies from both parents are readily detected by molecular methods in both T. mirus and T. miscellus. In one population of T. mirus and herbarium specimens collected at the time of species origin the gene ratios were balanced. Several lineages of T. mirus and T. miscellus were recently successfully resynthesized from diploid species. Among 181 synthetic individuals analyzed, we observed frequent deviations from copy­number additivity; that is in most cases, the T. dubius homeologs were reduced in copy number. At the epigenetic level, the genes of T. dubius origin dominate expression in most natural and synthetic allopolyploids. The fact that some rDNA genotypes seen in 80­year­old allopolyploids are already evident in the first generation of synthetic lines supports the hypothesis that the extent and tempo of rDNA homogenization in older allopolyploids is largely influenced by genetic and epigenetic changes in the early generations. Thus, T. mirus and T. miscellus that formed repeatedly in the wild within the last century represent a unique system to study the early stages of genome evolution following interspecific hybridization and genome duplication. This review summarizes recent works on the rDNA chromosomal organization, repeat and loci inheritance and gene expression. Keywords allopolyploid; homogenization; nucleolar dominance; ribosomal DNA; Tragopogon INTRODUCTION problems (Hadac, 1989; Ainouche & al., 2004). The success of newly formed angiosperm polyploids is partly attributable to In 1970, Susumu Ohno promoted the idea that gene and their highly plastic genome structure, as manifested by devia- genome duplications are the principle creative force in evolu- tions from Mendelian inheritance patterns of genetic loci and tion (Ohno, 1970). Perhaps no other group of living organisms chromosome aberrations (Leitch & Leitch, 2008). supports his hypothesis better than land plants. Chromosome Previous studies on natural and synthetic allopolyploids counts and other approaches suggest that between 30% and have shown that united parental genomes undergo active, fast, 100% of angiosperm species are polyploids (Masterson, 1994; and in some cases reproducible and directed processes of ge- Bennett, 2004; Soltis & al., 2009). Genomic studies have re- nome reorganization, probably due to intergenomic interactions vealed that all plant genomes sequenced to date have undergone (Soltis & Soltis, 1995). Reorganizations include both genetic one or more genome wide duplications in their evolutionary and epigenetic changes, which are observable after just a few history (Cui & al., 2006; Fawcett & al., 2009; Van de Peer & generations and even in F1 hybrids (e.g., Dadejova & al., 2007; al., 2009). Interspecific hybridization followed by multiplica- Kopecky & al., 2008; for review, see Chen & Ni, 2006). Most tion of parental chromosome sets is called allopolyploidy and genetic changes involve sequence loss or elimination often is believed to be a major driving force of angiosperm species associated with genome downsizing (Pestsova & al., 1998; evolution (Soltis & Soltis, 1995). Many economically important Kashkush & al., 2002), intergenomic chromosomal transloca- crops (e.g., wheat, oilseed rape, cotton, coffee, banana, tobacco) tions (Kenton & al., 1993), or the expansion of genome­specific are relatively recent allopolyploids (Leitch & Leitch, 2008). transposons (Zhao & al., 1998). Epigenetic silencing of parental The formation of allopolyploid species is, however, not always genes caused by the modification of chromatin is believed to beneficial since rapidly expanding populations of invasive allo­ reconcile regulatory incompatibilities between parental subge- polyploid weeds may cause severe ecological and economic nomes (Adams & Wendel, 2005). In contrast to the evolution of 348 TAXON 60 (2) • April 2011: 348–354 Malinska & al. • Evolution of rDNA in Tragopogon single­copy genes, members of multigene families do not often 2008). Eukaryotes regulate the effective dosage of their rRNA evolve independently, but in a concerted manner. In multigene genes, expressing fewer than half of the genes at the same families, limited sequence variability is often observed among time (Neves & al., 2005). Likewise, genetic hybrids displaying individual copies. Despite this high intraspecific homogeneity, nucleolar dominance transcribe rRNA genes inherited from interspecific divergence is not affected. This phenomenon has one parent, but silence the other parental set (Volkov & al., been called concerted evolution (Arnheim & al., 1980). The 2007). Interplay of DNA methylation, histone modification, underlying molecular processes are unequal crossing over and and chromatin­remodeling activities establishes silencing in gene conversion. The degree of homogenization is thus a result rDNA loci (Preuss & Pikaard, 2007). of the interplay between homogenization processes and novel The evolution of rDNA has stimulated much research. Ex- base substitutions (Schlotterer & Tautz, 1994). pression patterns of rRNA genes have been studied at inter­ In plants, nuclear ribosomal DNA (rDNA) units oc- phase by observing the behavior of nucleoli (Leitch, 2000). cur in tandem arrays at one or several loci (for review see Epigenetic processes can lead to inactivation of entire rDNA Hemleben & Zentgraf, 1994). These rRNA genes, frequently arrays (nucleolar dominance, Honjo & Reeder, 1973; Dadejova used as phylogeny markers, are organized on chromosomes & al., 2007; Preuss & Pikaard, 2007). Sequences can undergo as long arrays of tandemly arranged units. Each large 35S concerted evolution involving sequence homogenization (Do- rDNA unit contains the 18S, 5.8S and 26S rRNA genes, the ver, 1982; Wendel & al., 1995). Finally, the sequence data from internal transcribed spacers (ITS), and the intergenic spacer the internally transcribed spacers (nuclear ribosomal ITS) are (IGS) (Fig. 1). The large polycistronic 35S transcript is endo- regularly used to construct phylogenetic trees (Nieto Feliner nucleotically processed to produce mature rRNA molecules. & Rossello, 2007; Poczai & Hyvonen, 2010). The 5S genes encoding 120 nt transcripts are usually, but not In this review we will summarize the data from previous always (Garcia & al., 2009), located at different chromosomal and ongoing studies in recently formed Tragopogon allotetra- loci than 35S rDNA. The genic regions are highly conserved ploids, focusing on rDNA evolution. even between distally related species, whereas the intra and intergenic regions are highly variable. For example, the se- quence polymorphisms within IGS and ITS are sufficient to THE ORIGIN OF TRAGOPOGON resolve species relationships within most genera (e.g., Lihova ALLOTETRAPLOIDS & al., 2004; for review, see Alvarez & Wendel, 2003). The IGS, which contains the transcriptional start site as well as Tragopogon (Asteraceae) comprises approximately 100– genetic and epigenetic features that influence the regulation 150 species native to Eurasia. Most of them are diploids (2n = of the downstream genes, diverges rapidly, and substantial 12), but at least twelve species are ancient polyploids (2n = 24, differences in structure may occur even within a species (Ben- 36, 56–58) with generally unknown parentages (Mavrodiev nett & Smith, 1991; Skalicka & al., 2003; Komarova & al., & al., 2008). Fig. 1. The chromosomal and genomic structure of rDNA. Clusters of active rRNA genes are often located at the terminal part of the chromo- some, which is cytogenetically revealed as a secondary constriction (upper part). Note, two decondensed domains (arrows) are flanked by knobs of highly condensed rDNA chromatin. Each cluster is composed of hundreds to thousands of units arranged head to tail in tandem. Each unit is composed of conserved genic regions encoding 18S­5.8S­26S rRNA that are separated by the internally transcribed spacers (ITS1,
Load more

Recommended publications
  • Extensive Chromosomal Variation in a Recently Formed Natural Allopolyploid Species, Tragopogon Miscellus (Asteraceae)
    Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae) Michael Chestera, Joseph P. Gallaghera, V. Vaughan Symondsb, Ana Veruska Cruz da Silvac,d, Evgeny V. Mavrodievd, Andrew R. Leitche, Pamela S. Soltisd, and Douglas E. Soltisa,1 aDepartment of Biology, University of Florida, Gainesville, FL 32611; bInstitute of Molecular Biosciences, Massey University, Palmerston North, 4442, New Zealand; cEmbrapa Tabuleiros Costeiros, CEP 49025-040, Aracaju-SE, Brazil; dFlorida Museum of Natural History, University of Florida, Gainesville, FL 32611; and eSchool of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, United Kingdom Edited by James A. Birchler, University of Missouri, Columbia, MO, and approved December 6, 2011 (received for review July 22, 2011) Polyploidy, or whole genome duplication, has played a major role after whole genome duplication (18). In some cases, the regularity in the evolution of many eukaryotic lineages. Although the of meiosis was found to increase rapidly in experimental neo- prevalence of polyploidy in plants is well documented, the molec- allopolyploids that were initially chromosomally unstable (21, ular and cytological consequences are understood largely from 22); for example, after just five selfed generations, Nicotiana newly formed polyploids (neopolyploids) that have been grown neoallotetraploids displayed bivalent pairing and >99% stainable experimentally. Classical cytological and molecular cytogenetic pollen (22).
    [Show full text]
  • The Pennsylvania State University
    The Pennsylvania State University The Graduate School Intercollege Graduate Degree Program in Plant Biology PHYLOGENOMIC ANALYSIS OF ANCIENT GENOME DUPLICATIONS IN THE HISTORY OF PLANTS A Dissertation in Plant Biology by Yuannian Jiao © 2011 Yuannian Jiao Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2011 The dissertation of Yuannian Jiao was reviewed and approved* by the following: Claude dePamphilis Professor of Biology Dissertation Advisor Chair of Committee Hong Ma Professor of Biology John Carlson Professor of Molecular Genetics Webb Miller Professor of Comparative Genomics and Bioinformatics Naomi Altman Professor of Statistics Teh-hui Kao Chair of Plant Biology Graduate Program *Signatures are on file in the Graduate School iii ABSTRACT Whole-genome duplication (WGD), or polyploidy, followed by gene loss and diploidization, has generally been viewed as a primary source of material for the origin of evolutionary novelties. Most flowering plants have been shown to be ancient polyploids that have undergone one or more rounds of WGDs early in their evolution, and many lineages have since undergone additional, independent and more recent genome duplications. It was suggested that the paleopolyploidy events were crucial to the radiation and success of angiosperms, but evidence for proposed ancient genome duplications remains equivocal. Plant genomes are highly dynamic and usually go through intense structural rearrangements and gene loss following duplication. Old(er) WGDs can not
    [Show full text]
  • Evidence from Analysis of Synthetic Arabidopsis Allohexaploids
    INVESTIGATION Allopolyploidization Lays the Foundation for Evolution of Distinct Populations: Evidence From Analysis of Synthetic Arabidopsis Allohexaploids Starr C. Matsushita,* Anand P. Tyagi,*,† Gerad M. Thornton,* J. Chris Pires,‡ and Andreas Madlung*,1 *Department of Biology, University of Puget Sound, Tacoma, Washington, 98416, †School of Biological and Chemical Sciences, University of the South Pacific, Suva, Fiji, and ‡Division of Biological Sciences, University of Missouri, Columbia, Missouri, 65211-7310 ABSTRACT Polyploidization is an important mechanism for introducing diversity into a population and promoting evolutionary change. It is believed that most, if not all, angiosperms have undergone whole genome duplication events in their evolutionary history, which has led to changes in genome structure, gene regulation, and chromosome maintenance. Previous studies have shown that polyploidy can coincide with meiotic abnormalities and somatic cytogenetic mosaics in Arabidopsis allotetraploids, but it is unclear whether this phenomenon can contribute to novel diversity or act as a mechanism for speciation. In this study we tested the hypothesis that mosaic aneuploidy contributes to the formation of incipient diversity in neoallopolyploids. We generated a population of synthesized Arabi- dopsis allohexaploids and monitored karyotypic and phenotypic variation in this population over the first seven generations. We found evidence of sibling line-specific chromosome number variations and rapidly diverging phenotypes between lines, including
    [Show full text]
  • (Under the Direction of JOHN M. BURKE) ABSTRACT the Chapters of This Dissertation Are Designed to Investigate Speciation in T
    POPULATION GENETIC STUDIES OF SPECIATION IN THE PLANT GENUS STEPHANOMERIA (ASTERACEA) by NATASHA ANN SHERMAN (Under the Direction of JOHN M. BURKE) ABSTRACT The chapters of this dissertation are designed to investigate speciation in the plant genus Stephanomeria. Genetic markers were developed, and population genetic studies performed. In the first study, the goal was to investigate: the putative homoploid hybrid origin of Stephanomeria diegensis; whether this species arose once or on multiple occasions; and which subspecies of the parental taxa were involved in the original speciation event. The data presented support a hybrid origin of S. diegensis. In addition, the results showed the S. diegensis most likely arose once, and that S. exigua ssp. exigua or S. exigua ssp. deanei were involved in the formation. It was not possible to identify the subspecies of S. virgata involved. The second study investigates the allopolyploid origin of S. elata. The number of origins was investigated, as was the level of differentiation between two recognizable morphotypes, termed the Northern and Southern morphotype. This work identified three origins, with two origins found in the Southern morphotype and one in the Northern morphotype. The third study analyzed population genetic diversity in a disjunct population of S. exigua ssp. coronaria termed the Frenchglen population. This population is of particular interest because it is a peripheral isolate that gave rise to the endangered S. malheurensis. The Frenchglen population was found to be genetically robust, and unique from populations from the balance of the range of S. exigua ssp. coronaria. INDEX WORDS: speciation, hybridization, population genetic, homoploid, allopolyploid, peripatric, peripheral isolate POPULATION GENETIC STUDIES OF SPECIATION IN THE PLANT GENUS STEPHANOMERIA (ASTERACEAE) by Natasha Ann Sherman B.S.
    [Show full text]
  • Polyploid Plants Have Faster Rates of Multivariate Niche Differentiation Than Their Diploid Relatives
    Ecology Letters, (2020) 23: 68–78 doi: 10.1111/ele.13402 LETTER Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives Abstract Anthony E. Baniaga,1* Polyploid speciation entails substantial and rapid postzygotic reproductive isolation of nascent Hannah E. Marx,1,2 Nils Arrigo1,3 species that are initially sympatric with one or both parents. Despite strong postzygotic isolation, and Michael S. Barker1 ecological niche differentiation has long been thought to be important for polyploid success. Using biogeographic data from across vascular plants, we tested whether the climatic niches of The peer review history for this arti- polyploid species are more differentiated than their diploid relatives and if the climatic niches of cle is available at https://publons. polyploid species differentiated faster than those of related diploids. We found that polyploids are com/publon/10.1111/ele.13402. often more climatically differentiated from their diploid parents than the diploids are from each other. Consistent with this pattern, we estimated that polyploid species generally have higher rates of multivariate niche differentiation than their diploid relatives. In contrast to recent analyses, our results confirm that ecological niche differentiation is an important component of polyploid speci- ation and that niche differentiation is often significantly faster in polyploids. Keywords Climatic niche, niche breadth, polyploid, speciation, sympatric speciation. Ecology Letters (2020) 23: 68–78 isolation from their progenitors, while also sympatric and INTRODUCTION competing with either one or both parental species (Ramsey Among vascular plants, polyploidy or whole genome duplica- & Schemske 1998, 2002). Mathematical models indicate that tion (WGD) is associated with an estimated 15–30% of speci- polyploid establishment is promoted by high selfing rates, ation events (Wood et al.
    [Show full text]
  • BMC Plant Biology Biomed Central
    BMC Plant Biology BioMed Central Research article Open Access On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae) Jennifer A Tate*1, Prashant Joshi1, Kerry A Soltis2, Pamela S Soltis3,4 and Douglas E Soltis2,4 Address: 1Institute of Molecular BioSciences, Massey University, Palmerston North, New Zealand, 2Department of Biology, University of Florida, Gainesville, Florida, USA, 3Florida Museum of Natural History, University of Florida, Gainesville, Florida, USA and 4Genetics Institute, University of Florida, Gainesville, Florida, USA Email: Jennifer A Tate* - [email protected]; Prashant Joshi - [email protected]; Kerry A Soltis - [email protected]; Pamela S Soltis - [email protected]; Douglas E Soltis - [email protected] * Corresponding author Published: 27 June 2009 Received: 5 May 2009 Accepted: 27 June 2009 BMC Plant Biology 2009, 9:80 doi:10.1186/1471-2229-9-80 This article is available from: http://www.biomedcentral.com/1471-2229/9/80 © 2009 Tate et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Polyploidy (whole-genome duplication) is an important speciation mechanism, particularly in plants. Gene loss, silencing, and the formation of novel gene complexes are some of the consequences that the new polyploid genome may experience. Despite the recurrent nature of polyploidy, little is known about the genomic outcome of independent polyploidization events.
    [Show full text]
  • Symposium 74 Evolution
    Downloaded from symposium.cshlp.org on April 23, 2015 - Published by Cold Spring Harbor Laboratory Press On the Origins of Species: Does Evolution Repeat Itself in Polyploid Populations of Independent Origin? D.E. SOLTIS,1,2 R.J.A. BUGGS,1 W.B. BARBAZUK,1,2 P.S. SCHNABLE,3 AND P.S. SOLTIS2,4 1Department of Biology, University of Florida, Gainesville, Florida 32611; 2Genetics Institute, University of Florida, Gainesville, Florida 32610; 3Center for Plant Genomics, Iowa State University, Ames, Iowa 50011; 4Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 Correspondence: [email protected] Multiple origins of the same polyploid species pose the question: Does evolution repeat itself in these independently formed lineages? Tragopogon is a unique evolutionary model for the study of recent and recurrent allopolyploidy. The allotetraploids T. mirus (T. dubius x T. porrifolius) and T. miscellus (T. dubius x T. pratensis) formed repeatedly following the introduction of three diploids to the United States. Concerted evolution has consistently occurred in the same direction (resulting in loss of T. dubius rDNA copies). Both allotetraploids exhibit homeolog loss, with the same genes consistently showing loss, and homeologs of T. dubius preferentially lost in both allotetraploids. We have also documented repeated patterns of tissue-spe- cific silencing in multiple populations of T. miscellus. Hence, some aspects of genome evolution may be “hardwired,” although the general pattern of loss is stochastic within any given population. On the basis of the study of F1 hybrids and syn- thetics, duplicate gene loss and silencing do not occur immediately following hybridization or polyploidization, but gradually and haphazardly.
    [Show full text]
  • The Role of Genetic and Genomic Attributes in the Success of Polyploids
    Colloquium The role of genetic and genomic attributes in the success of polyploids Pamela S. Soltis* and Douglas E. Soltis School of Biological Sciences, Washington State University, Pullman, WA 99164-4236 In 1950, G. Ledyard Stebbins devoted two chapters of his book polyploid origin, as noted by Stebbins (1). In contrast, although Variation and Evolution in Plants (Columbia Univ. Press, New York) genome doubling has been reported from other major groups of to polyploidy, one on occurrence and nature and one on distribu- eukaryotes (reviewed in ref. 6), it is not nearly as common in tion and significance. Fifty years later, many of the questions these groups as it is in plants. Stebbins posed have not been answered, and many new questions The question often has arisen as to why polyploids are so have arisen. In this paper, we review some of the genetic attributes common and so successful, and several possible explanations of polyploids that have been suggested to account for the tremen- have been proposed. Stebbins (1) considered vegetative re- dous success of polyploid plants. Based on a limited number of production and the perennial habit to be important factors studies, we conclude: (i) Polyploids, both individuals and popula- promoting the establishment of polyploids, along with an tions, generally maintain higher levels of heterozygosity than do outcrossing mating system to allow for hybridization (between their diploid progenitors. (ii) Polyploids exhibit less inbreeding species, subspecies, races, populations, etc.) in the formation depression than do their diploid parents and can therefore tolerate of the polyploid. Perhaps most important to Stebbins (1) was higher levels of selfing; polyploid ferns indeed have higher levels the availability of new ecological niches.
    [Show full text]
  • Evolution and Expression of Homeologous Loci in Tragopogon Miscellus (Asteraceae), a Recent and Reciprocally Formed Allopolyploid
    Copyright Ó 2006 by the Genetics Society of America DOI: 10.1534/genetics.106.057646 Evolution and Expression of Homeologous Loci in Tragopogon miscellus (Asteraceae), a Recent and Reciprocally Formed Allopolyploid Jennifer A. Tate,*,1 Zhongfu Ni,† Anne-Cathrine Scheen,‡ Jin Koh,* Candace A. Gilbert,* David Lefkowitz,* Z. Jeffrey Chen,† Pamela S. Soltis§ and Douglas E. Soltis* *Department of Botany, University of Florida, Gainesville, Florida 32611, †Institute for Cellular and Molecular Biology, University of Texas, Austin, Texas 78712, ‡Natural History Museum, University of Oslo, N-0318 Oslo, Norway and §Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 Manuscript received March 1, 2006 Accepted for publication April 20, 2006 ABSTRACT On both recent and ancient time scales, polyploidy (genome doubling) has been a significant evolu- tionary force in plants. Here, we examined multiple individuals from reciprocally formed populations of Tragopogon miscellus, an allotetraploid that formed repeatedly within the last 80 years from the diploids T. dubius and T. pratensis. Using cDNA–AFLPs followed by genomic and cDNA cleaved amplified polymorphic sequence (CAPS) analyses, we found differences in the evolution and expression of homeologous loci in T. miscellus. Fragment variation within T. miscellus, possibly attributable to reciprocal formation, comprised 0.6% of the cDNA–AFLP bands. Genomic and cDNA CAPS analyses of 10 candidate genes revealed that only one ‘‘transcript-derived fragment’’ (TDF44) showed differential expression of parental homeologs in T. miscellus; the T. pratensis homeolog was preferentially expressed by most polyploids in both populations. Most of the cDNA–AFLP polymorphisms apparently resulted from loss of parental fragments in the polyploids.
    [Show full text]
  • Evolution and Expression of Homoeologous Loci in Tragopogon Miscellus (Asteraceae), A
    Genetics: Published Articles Ahead of Print, published on April 28, 2006 as 10.1534/genetics.106.057646 Evolution and Expression of Homoeologous Loci in Tragopogon miscellus (Asteraceae), a Recent and Reciprocally Formed Allopolyploid Jennifer A. Tate * 1, Zhongfu Ni †, Anne-Cathrine Scheen ‡, Jin Koh *, Candace A. Gilbert*, David Lefkowitz*, Z. Jeffrey Chen †, Pamela S. Soltis § and Douglas E. Soltis* * Department of Botany, University of Florida, Gainesville, Florida 32611 † Institute for Cellular and Molecular Biology, The University of Texas at Austin, Austin, Texas 78712 ‡ The Natural History Museum, University of Oslo, N-0318, Oslo, Norway § Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 1 Present address: Institute of Molecular Biosciences, Massey University, Palmerston North, New Zealand Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. DQ267218-DQ267256 2 Running head: Genome evolution in Tragopogon miscellus Key words: allopolyploidy, cDNA-AFLP, genome evolution, homoeolog, Tragopogon Corresponding authors: Jennifer A. Tate, Institute of Molecular Biosciences, Massey University, Private Bag 11-222, Palmerston North, New Zealand. Phone: (06) 350 5515, FAX: (06) 350 5688, E-mail: [email protected]; Douglas E. Soltis, Department of Botany, University of Florida, Gainesville, FL 32611. Phone: (352) 392-1721, FAX: (352) 846-2154, E-mail: [email protected] 3 Abstract On both recent and ancient time scales, polyploidy (genome doubling) has been a significant evolutionary force in plants. Here, we examined multiple individuals from reciprocally formed populations of Tragopogon miscellus, an allotetraploid that formed repeatedly within the last 80 years from the diploids T. dubius and T.
    [Show full text]
  • Gradual Evolution of Allopolyploidy in Arabidopsis Suecica
    ARTICLES https://doi.org/10.1038/s41559-021-01525-w Gradual evolution of allopolyploidy in Arabidopsis suecica Robin Burns 1, Terezie Mandáková2, Joanna Gunis 1, Luz Mayela Soto-Jiménez 1, Chang Liu3, Martin A. Lysak 2, Polina Yu. Novikova 4,5 ✉ and Magnus Nordborg 1 ✉ Most diploid organisms have polyploid ancestors. The evolutionary process of polyploidization is poorly understood but has frequently been conjectured to involve some form of ‘genome shock’, such as genome reorganization and subgenome expres- sion dominance. Here we study polyploidization in Arabidopsis suecica, a post-glacial allopolyploid species formed via hybrid- ization of Arabidopsis thaliana and Arabidopsis arenosa. We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from all species. Despite a divergence around 6 million years ago (Ma) between the ancestral species and differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is colinear with the ancestral genomes; there is no subgenome dominance in expression; and transposon dynamics appear stable. However, we find changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly to prevent aneuploidy and undesirable homeologous exchanges that are observed in synthetic A. suecica, and the A. arenosa subgenome shows upregulation of cyto-nuclear pro- cesses, possibly in response to the new cytoplasmic environment of A. suecica, with plastids maternally inherited from A. thaliana. These changes are not seen in synthetic hybrids, and thus are likely to represent subsequent evolution. ncient polyploidization or whole-genome duplication is a Genomic changes have also been reported in natural allopoly- hallmark of most higher-organism genomes1,2, including ploids such as Tragopogon miscellus66,67, Mimulus pergrinus17 and Aour own3,4.
    [Show full text]
  • Cytonuclear Coordination Is Not Immediate Upon Allopolyploid Formation in Tragopogon Miscellus (Asteraceae) Allopolyploids
    RESEARCH ARTICLE Cytonuclear Coordination Is Not Immediate upon Allopolyploid Formation in Tragopogon miscellus (Asteraceae) Allopolyploids Tina Sehrish1, V. Vaughan Symonds1, Douglas E. Soltis2,3,4, Pamela S. Soltis3,4, Jennifer A. Tate1* 1 Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand, 2 Department of Biology, University of Florida, Gainesville, Florida, United States of America, 3 Florida Museum of Natural History, University of Florida, Gainesville, Florida, United States of America, 4 Genetics Institute, University of Florida, Gainesville, Florida, United States of America * [email protected] Abstract Allopolyploids, formed by hybridization and chromosome doubling, face the immediate chal- lenge of having duplicated nuclear genomes that interact with the haploid and maternally inher- OPEN ACCESS ited cytoplasmic (plastid and mitochondrial) genomes. Most of our knowledge of the genomic Citation: Sehrish T, Symonds VV, Soltis DE, Soltis consequences of allopolyploidy has focused on the fate of the duplicated nuclear genes with- PS, Tate JA (2015) Cytonuclear Coordination Is Not Immediate upon Allopolyploid Formation in out regard to their potential interactions with cytoplasmic genomes. As a step toward under- Tragopogon miscellus (Asteraceae) Allopolyploids. standing the fates of nuclear-encoded subunits that are plastid-targeted, here we examine the PLoS ONE 10(12): e0144339. doi:10.1371/journal. retention and expression of the gene encoding the small subunit of Ribulose-1, 5-bisphosphate pone.0144339 carboxylase/oxygenase (Rubisco; rbcS) in multiple populations of allotetraploid Tragopogon Editor: Khalil Kashkush, Ben-Gurion University, miscellus (Asteraceae). These polyploids formed recently (~80 years ago) and repeatedly from ISRAEL T. dubius and T. pratensis in the northwestern United States.
    [Show full text]