Inference of Evolution of Vertebrate Genomes and Chromosomes from Genomic and Cytogenetic Analyses Using Amphibians
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Chromosome Science 24: 3-12, 2021 Uno 3 Review Article Inference of evolution of vertebrate genomes and chromosomes from genomic and cytogenetic analyses using amphibians Yoshinobu Uno Received: December 28, 2020 / Accepted: January 15, 2021 © 2021 by the Society of Chromosome Research Abstract this species can produce a large number of eggs all year round, and the sizes of eggs and embryos are large enough Amphibians, which first adapted to terrestrial life in to allow microsurgical manipulation and injection. This vertebrates, appeared around 350 million years ago frog was the experimental animal used by John Gurdon, (Mya) after the common ancestors of tetrapods (am- who was awarded the Nobel Prize for Medicine or Physiol- phibians, reptiles, birds, and mammals) diverged from ogy for his groundbreaking study on nuclear reprogram- ray-finned fishes around 410 Mya, and are therefore ming. Specifically, he showed that the nuclei from special- important model animals for understanding vertebrate ized X. laevis cells could be reprogrammed to give rise to evolution. To date, there are many cytogenetic reports a complete animal (Gurdon, 1962). However, X. laevis is of amphibians. Moreover, recent improvements in tech- difficult to apply with respect to genetic material because niques for cytogenetic and genomic analyses help accel- of an allotetraploid species (see section: Polyploid evolu- erate the accumulation of the cytogenetic and genomic tion in amphibians) and longer generation times than the data from amphibians. Inferred from recent genomic and other vertebrate models, including mice and zebrafish. cytogenetic analyses using amphibians, I review karyo- Since the 1990s, researchers have widely used the diploid type and chromosome evolution, including sex chromo- species related to X. laevis, the Western clawed frog (Xeno- somes, polyploidy, and origins of microchromosomes, in pus [formerly Silurana] tropicalis, Pipidae, Anura), whose not only amphibians but also entire vertebrates. generation time is shorter than X. laevis, as a novel animal model for biological research, including genetic analyses. Salamanders have contributed to biological research based Keywords: amphibians, chromosome, genome, evolu- on the discovery of the Spemann organizer (Spemann and tion, vertebrates Mangold, 1924). The Mexican axolotl (Ambystoma mexi- canum, Ambystomatidae, Caudata) is commonly used in Overview of Amphibians many regeneration laboratories to uncover the remarkable The class Amphibia occupies a phylogenetic position regenerative capability of this animal. between Actinopterygii (ray-finned fishes) and Amniota Since the 1980s, decreases in amphibian populations ow- (reptiles, birds, and mammals), and the ancestors of Tet- ing to invasive fungi and habitat destruction have been ob- rapoda split into the two main lineages of Amphibia and served around the world, which is one of the most critical Amniota roughly 350 million years ago (Mya) (Kumar et threats to global biodiversity (Alroy, 2015; O’Hanlon et al., al., 2017). The extant amphibians comprise three orders: 2018). Some researchers have estimated that almost one- Anura (frogs and toads), Caudata/Urodela (salamanders), third of amphibians are threatened with extinction (Stuart and Gymnophiona (caecilians), which contain 54, 10, and et al., 2004); therefore, urgent action is needed to prevent 10 families, respectively, and the number of extant amphib- further declines and the extinction crisis in amphibians. ian species is approximately 8,200, of which nearly 88% Genome analyses using whole-genome sequences in con- are anurans (AmphibiaWeb, 2020) (as of November 2020) servation biology are known as powerful tools to highlight (Figure 1). Some amphibian species have been widely used the biological relationships of wildlife species at the ge- as experimental animals for life science research. The Afri- nome level and evaluate the potential response to chang- can clawed frog (Xenopus laevis, Pipidae, Anura) has been a ing environments (Steiner et al., 2013; Homola et al., 2019). particularly excellent animal model in developmental, cel- Revealing genome and chromosomal information on am- lular, and molecular biological research since the 1950s. X. phibians could contribute to not only a deep understanding laevis has unique advantages for experiments. For instance, of the evolution of vertebrate genomes and chromosomes but also the conservation of biological diversity in amphib- ians, many of which are threatened by extinction. Yoshinobu Uno (*) This review describes the characterizations of karyotypes Department of Life Sciences, Graduate School of Arts and Sciences, and genomes in amphibians and the amphibian sequenced The University of Tokyo, Tokyo, Japan. whole genomes published to date. Next, we present novel E-mail: [email protected] knowledge of genomic and chromosomal evolution in ver- Tel: +81-3-5454-6739 tebrates, including sex chromosomes, polyploid, and karyo- 4 Genomic and cytogenetic analyses using amphibians type evolution obtained by recent genomic and cytogenetic 2002; Matsui et al., 2006; Sessions, 2008; Venu et al., 2011) analyses using amphibians. (Figure 1). In particular, the karyotypes of anurans and sal- amanders have been the subject of numerous cytogenetic Karyotypes and genome sizes of amphibians studies, and karyotype data are available for most family Among Amphibia, karyotypes of diploid species have groups. Collectively, the karyotypes of diploid amphibian been reported for 1,193 (14.5%) of the ~8,200 known spe- species are commonly characterized by 20–26 bi-armed cies, namely 963 anurans, 209 salamanders, and 21 caeci- chromosomes. Some karyotype reports suggest that poly- lians (as of November 2020) (Morescalchi, 1973; Wake and ploidy may have been involved in some families (Schmid et Case, 1975; Kuramoto, 1990; Venkatachalaiah and Venu, al., 2015) (see section: Polyploid evolution in amphibians). Figure 1. Chromosome number variation among 1,193 diploid species in Amphibia. The numbers of species with diploid chromosome numbers and with reported karyotypes were extracted from previous cytogenet- ic studies (Morescalchi, 1973; Wake and Case, 1975; Kuramoto, 1990; Venkatachalaiah and Venu, 2002; Matsui et al., 2006; Sessions, 2008; Venu et al., 2011). The numbers of extant amphibian species in individual suborders or families are shown in the parentheses based on an existing resource (AmphibiaWeb, 2020). The phylogenetic relationship is based on the existing literature (Wake and Koo, 2018; AmphibiaWeb, 2020). The divergence times between the three orders, Anura (frogs and toads), Caudata/Urodela (sala- manders), and Gymnophiona (caecilians), are cited from the existing literature (Kumar et al., 2017). Mya, million years ago. Uno 5 Amphibians are also characterized by extremely large ge- Sex chromosome evolution in amphibians nomes compared to other taxa of vertebrates and extensive Mammalian species exhibit a male-heterogametic ge- variation in genome size (C-value: picograms of DNA in netic sex-determination system with XX/XY sex chromo- haploid nuclei), which transcends variation in chromosome somes, and birds do female-heterogametic determination number and shape (Liedtke et al., 2018; Gregory, 2020). with ZZ/ZW sex chromosomes (Takagi and Sasaki, 1974; The genome sizes range from 0.95 to 11.50 pg, from 13.89 Vorontsov et al., 1980; Belterman and Boer, 1984). Both to 120.56 pg, and from 2.94 to 11.78 pg in Anura, Caudata, male heterogamety and female heterogamety have been and Gymnophiona, respectively. Crucially, the larger ge- found in reptiles (Olmo and Signorino, 2005). Most reptiles nome sizes compared to other vertebrates have prevented and all birds and mammals have differentiated sex chromo- whole-genome sequencing of amphibians. some pairs. On the other hand, teleost fishes and amphib- ians also exhibit both male heterogamety and female het- Whole-genome sequencing of amphibians erogamety, and most of these species have morphologically Genome sequencing projects are now ongoing for many undifferentiated sex chromosomes. Sex-determining genes vertebrate species, and the available information provides in several teleost fishes were identified using genetic and a new perspective on genome and chromosome evolution cytogenetic analyses, and these findings indicated that the in vertebrates. The draft genome assembly of X. tropicalis sex-determining genes and genetic linkages of sex chromo- was the first to be reported for amphibians in 2010 (Hell- somes were different not only within orders but also be- sten et al., 2010). A de novo genome of the Tibetan frog tween related species within genera (Kikuchi and Hamagu- (Nanorana parkeri, Dicroglossidae, Anura) was published chi, 2013; Bachtrog et al., 2014). This phenomenon results as the second draft genome assembly in amphibians (Sun from switches in the chromosome pairs used for sex deter- et al., 2015). The genomes of the two frogs were smaller mination, termed turnover of sex chromosomes. Sex chro- (1.7 Gb and 2.3 Gb, respectively) than those mammals (ap- mosomes are relatively young in organisms in which sex proximately 3 Gb) and sequenced using whole-genome chromosome turnover occurs; thus, sex chromosomes have shotgun methods based on Sanger sequencing or short- insufficient time to substantially differentiate from one an- read sequencing. Draft genome assemblies of organisms other. Accumulation of the cytogenetic and genomic data with larger genome sizes than these animals sequenced