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REVIEW COMMUNICATIONS
GENETICS
Cotton genome evolution and features of its structural and functional organization
Ksenia Strygina, Elena Khlestkina, and Larisa Podolnaya
Federal Research Center N. I. Vavilov All-Russian Institute of Plant Genetic Resources, Bol'shaya Morskaya ul., 42-44, Saint Petersburg, 190000, Russian Federation
Address correspondence and requests for materials to Ksenia Strygina, [email protected]
Abstract
Allotetraploid cotton Gossypium hirsutum L. is not only an important crop, but also a model organism used to study such processes as polyploidization, plant genome evolution and the influence of polyploidy on gene expression. The present article provides a review of studies devoted to the taxonomy of the genus Gossypium, the evolution of the genomes of its representatives (including 45 diploid and 7 allotetraploid species), and the functional divergence of duplicated copies of the same genes in allotetraploid species. The discussion concerns the areas of individual species' origin, as well as the reasons of the high variation in genome size (from ~880 Mb to ~2400 Mb), which was influenced by both full-genome duplications and the spread of mobile genetic elements. The data support the fact that the expression of genes in allotetraploid cotton changes as a result of polyploidization, and that one of the two subgenomes dominates in the formation of one or another trait. The considered data shed light on the features of the evolution of plant genes and genomes. Keywords: Allopolyploid genome, cotton, evolution, functional divergence, gene duplication, Gossypium, homoeologous genes, mobile genetic elements.
1. Genus Gossypium L.
Citation: Strygina, K., Khlestkina, E., and Podolnaya, L. 2020. Cotton genome evolution and features of its structural and functional organization. Bio. Comm. 65(1): 15-27. https://doi.org/10.21638/ spbu03.2020.102
Author's information: Ksenia Strygina, PhD, Researcher, orcid.org/0000-0001-6938-1348; Elena Khlestkina, Dr. of Sci. in Biology, Professor RAS, Head of Laboratory, orcid.org/0000-0002-8470-8254; Larisa Podolnaya, PhD, Leading Researcher, orcid. org/0000-0002-4962-1989
Manuscript Editor: Alla Krasikova, Department of Cytology and Histology, Faculty of Biology, Saint Petersburg State University, Saint Petersburg, Russia
Received: September 2, 2019;
Revised: December 16, 2019;
Accepted: January 12, 2020;
Copyright: © 2020 Strygina et al. This is an open-access article distributed under the terms of the License Agreement with Saint Petersburg State University, which permits to the authors unrestricted distribution, and self-archiving free of charge.
Funding: The present review was carried out within VIR project No. 0481-2019-0001.
Competing interests: The authors have declared that no competing interests exist.
Cotton (genus Gossypium L.) belongs to the tribe Gossypieae Alef., which comprises nine genera (Fryxell, 1968, 1978; Phuphathanaphong, 2006). Five genera include a small number of species; they are monotypic and are characterized by narrow distribution areas: Cephalohibiscus Ulbr. (one species; New Guinea, Solomon Islands), Gossypioides Skovst. ex J. B. Hutch. (two species; East Africa, Madagascar), Kokia Lewton (six species; Hawaii), Lebronnecia Fosberg (one species; Marquesas Islands) and Thepparatia Phuph. (one species; northern Thailand). The other four genera are larger and represent groups with moderately wide geographical ranges: Cienfuegosia Cav. (25 species; neotropical realm, part of Africa), Hampea Schltdl. (21 species; neotropical realm), Thespesia Sol. ex Correa (17 species; tropics) and the largest and most widespread genus Gossypium L. (52 species). These representatives grow in the tropical and subtropical regions of the Old and New Worlds (Fig. 1) (Fryxell, Craven and Stewart, 1992; Wendel et al., 2009).
Despite wide distribution and morphological diversity, the genus Gossypium represents a single phylogenetic group (Fryxell et al., 1992; Wendel and Gro-ver, 2015). The closest relatives of cotton are the Hawaiian endemic genus Kokia and the Afro-Madagascan genus Gossypioides (Seelanan, Schnabel and Wendel, 1997). Their divergence occurred during the Miocene 10-15 million years ago (MYA) with the subsequent spread of Gossypium over almost all continents (Fig. 2) (Wendel et al., 2009; Wendel and Grover, 2015).
As the genus Gossypium was undergoing its formation (5-10 MYA) and spreading to various environments, the genome of Gossypium was undergoing significant changes and rearrangements (Fig. 2) (Hendrix and Stewart, 2005). It is reflected in such phenotypic features as the type of ontogenesis, plant life-form,
Fig. 1. Distribution of the genus Gossypium. Yellow indicates the distribution of the Gossypium subgenus representatives (A, B, E, F genomes); green — subgenus Sturtia representatives (C, G, K genomes); purple — subgenus Houzingenia representatives (D genome); blue — subgenus Karpas representatives (AD genome). Photos of G. arboreum (AA), G. raimondii (DD) and G. hirsutum (AADD) cotton samples from the herbarium collection of the N. I.Vavilov All-Russian Institute of Plant Genetic Resources.
corolla color, leaf shape, seed shape, distribution mode, etc. According to the generally accepted system by P. A. Fryxell (1992), supplemented by newly described species, the genus Gossypium includes 45 diploid (2n = 2x = 26) and 7 allotetraploid (2n = 4x = 52) species (Tab. 1) (Fryxell, 1992; Fryxell et al., 1992; Grover et al., 2014; Yu et al., 2014; Gallagher et al., 2017). The main centers of genus diversity are the arid areas of Australia, Africa, Arabia, the Indian subcontinent, the Galapagos and Hawaiian Islands, and Central and South Americas (Fig. 1) (Fryxell et al., 1992; Wendel et al., 2009).
Based on the analysis of morphological features, the nature of distribution areas, cytogenetic and molecular genetic data and the relative fertility of interspecific hybrids, cotton species fall into eight genomic groups (A-G and K) united into four subgenera; one of these groups is represented by AD allotetraploid representatives (Tab. 1) (Webber, 1938; Endrizzi, Turcotte and Kohel, 1985; Fryxell, 1992; Wendel and Grover, 2015). The three subgenera that include diploid species have separate distribution areas, namely Africa/Arabia (A, B, E and F genomes), Australia (C, G and K genomes) and America (D genome) (Fig. 1, Tab. 1) (Wendel and Cronn, 2003). The monophyletic origin of the allotet-raploid group (AD genome) in the regions of the New World is associated with the spread of the A genome donor, related to G. arboreum L. or G. herbaceum L., from Africa or Asia over long distances to the New World, and subsequent hybridization (about 1-1.5 MYA) with the
American representative of the D genomic group, genetically close to G. raimondii Ulbr. (Fig. 1) (Skovsted, 1933, 1934; Lemeshev, 1991; Wendel and Albert, 1992; Wendel and Cronn, 2003; Paterson et al., 2012; Lu et al., 2018).
1.1. Diploid species of the genus Gossypium
Subgenus Gossypium Tod. (A, B, E, F). According to the last taxonomic interpretation, the subgenus Gossypium Tod. includes 14 species from Africa and Arabia (Fryxell, 1992). These species exhibit significant cytogenetic diversity that corresponds to the A, B, E, and F genomic groups (Tab. 1, Fig. 2) (Seelanan et al., 1997; Wendel and Albert, 1992). It is supposed that such a variation in genomes compared to the relative uniformity of cotton found in the New World (see below) may indicate the African origin of the genus Gossypium (Wendel and Grover, 2015).
To date, the most well-studied is the A genomic group, which includes two cultivated cotton species — G. herbaceum L. and G. arboreum L. (Wendel, Olson and Stewart, 1989). The B genomic group is represented by four African species, while the F genomic group is represented by only one species — G. longicalyx Hutch. and Lee (Tab. 1). Its cytogenetic and morphological differences from other Gossypium members are probably explained by its geographical isolation (Fryxell, 1971; Vollesen, 1987; Wendel and Grover, 2015).
Fig. 2. A modern look at the phylogeny of the genus Gossypium. Genome sizes, number of whole-genome duplications (WGD) and genome divergence time (MYA — million years ago) are based on the works by Wendel and Cronn, 2003; Hendrix and Stewart, 2005; Wendel and Grover, 2015; Lu et al., 2018.
The E genome encompasses three well-studied species and five poorly studied species (the so-called G. so-malense complex) (Tab. 1) (Vollesen, 1987; Golubets, 1991). Of these species, only G. somalense has been studied cytogenetically; other species of the group have been described from several herbarium specimens, and therefore their individuality is doubtful (Tab. 1). The problem is that the distribution area of these species is located in the Horn of Africa, where it is not possible to organize collecting missions.
Regarding G. trifurcatum Vollesen, which also grows in Somalia and has been described only from an herbarium specimen, its taxonomic status is unclear. Fryxell (1992) separated this species into an individual Serrata section. This species may belong to both B and E genomes (Tab. 1) (Wendel and Grover, 2015).
Subgenus Sturtia (R. Br.) Tod. (C, G, K). The Australian subgenus Sturtia (R. Br.) Tod. includes three genomic groups (C, G and K) represented by 4, 3 and 11 diploid cotton species, respectively (Fig. 2, Tab. 1) (Fryxell, 1978; Wendel et al., 2009; Tiwari, Zhang and Stewart, 2014; Wendel and Grover, 2015). The taxonomy of species in this group still needs to be refined (Podol-naya, 1991). Nevertheless, their division into three ge-nomic groups according to DNA sequence data (Seelan-an et al., 1997) is consistent with their formal separation into the Sturtia (C genome), Hibiscoidea (G genome) and Grandicalyx (K genome) taxonomic sections (Fryxell, 1978; Tiwari et al., 2014).
Most species of the subgenus Sturtia are sympatric in their areas of distribution and occur exclusively in the northern region of Australia (Seelanan et al., 1999; Wendel, Stewart and Rettig, 1991). The species from the C and G genomic groups are available in many genetic resources collections around the world and have been thoroughly studied. Despite this, the tendency for hybridization and genetic material introgression in the C genome species poses certain complications (Seelanan et al., 1999; Cronn and Wendel, 2003; Tiwari et al., 2014).
The taxonomic status of the K genome representatives is unclear due to insufficient knowledge (Fryxell, 1978; Seelanan et al., 1997, 1999; Tiwari et al., 2014). In terms of the nature of the distribution area, as well as many morphological characters, including the seedlings structure, life-form and peculiarities of seed distribution, the species of the Grandicalyx section differ sharply from other representatives of the subgenus Sturtia. On this basis, suggestions are made to change the rank of the taxon (Podolnaya, 1991). However, representatives of this section are almost absent in collections, and it complicates the research (Campbell et al., 2010).
Subgenus Houzingenia Fryx. (D). The subgenus Houzingenia Fryx. is the best-studied group represented by thirteen D genomic diploids from the New World (Fig. 2, Tab. 1) (Seelanan et al., 1997; Ulloa, 2014; Wendel and Grover, 2015 Grover et al., 2018). These species have unusually small genomes for the genus Gossypium (Fig. 2) (Hendrix and Stewart, 2005). Not a single rep-
Table 1. Taxonomy of the genus Gossypium in accordance with CottonGen database (Yu et al., 2014). Cultivated cotton species are bolded in the table
Subgenus Genomic group Species Genome Geographical distribution
A G. herbaceum L. G. arboreum L. Ai A2 Africa, Asia Asia
B G. anomalum Wawr. and Peyer G. triphyllum (Harv. and Sand.) Hochr. G. capitis-viridis (Harv. and Sand.) Hochr. G. trifurcatum Vollesen Bi B2 B3 B* Africa Africa Cape Verde Islands Africa
Gossypium Tod. E G. stocksii Mast. ex. Hook. G. somalense (Gurke) Hutch. G. areysianum (Defl.) Hutch. G. incanum (Schwartz) Hillc. G. benadirense Mattei G. bricchettii (Ulbr.) Vollesen G. vollesenii Fryx. m rn rn 4 3 Arabia Arabia Arabia Arabia Arabia Arabia Arabia
F G. longicalyx Hutch. and Lee Fi Arabia
C G. sturtianum J. H.Willis G. nandewarense (Derera) Fryx. G. robinsonii F.Muell. G. pilosum Fryxell Ci C(1-n) C2 Cio Australia Australia Australia Australia
G G. bickii Prokh. G. australe F.Muell. G. nelsonii Fryxell Gi G2 G3 Australia Australia Australia
Sturtia (R. Br.) Tod. K G. costulatum Tod. G. populifolium (Benth.) Tod. G. cunninghamiiTod. G. pulchellum (C. A. Gardner) Fryxell G. anapoidesJ. M. Stewart, Craven, Brubaker and Wendel G. enthyle Fryxell et al. G. exiguum Fryxell et al. G. londonderriense Fryxell et al. G. marchantii Fryxell et al. G. nobile Fryxell et al. G. rotundifolium Fryxell et al. K1 K2 K3 K4 KG K7 K8 K9 Kio Kii Ki2 Australia Australia Australia Australia Australia Australia Australia Australia Australia Australia Australia
Houzingenia Fryx. D G. thurberi Tod. G. armourianum Kearney G. harknessii Brandegee G. davidsonii Kellogg G. klotzschianum Andersson G. aridum (Rose and Standl.) Skovst. G. raimondii Ulbr. G.gossypioides (Ulbr.) Standl. G. lobatum Gentry G. trilobum (Moc. and Sess. ex DC.) Skov. G. laxum L. Ll. Phillips G. turneri Fryxell G. schwendimanii Fryxell and S. D. Koch Di D(2-1) D(2-2) D(3-d) D(3-k) D4 D5 Dg D7 D8 D9 Dio Dii Mexico and Southwestern USA Mexico Mexico Mexico Galapagos Islands Mexico Peru Mexico Mexico Mexico Mexico Mexico Mexico
Karpas Raf. AD G. hirsutum L. G. barbadense L. G. tomentosum Nutt. ex Seem. G. mustelinum Miers ex G. Watt G. darwinii G. Watt G. ekmanianum Wittmack G. stephensiiJ. Gallagher et al. (AD)i (AD)2 (AD)3 (AD)4 (AD)5 (AD)6 (AD)7 Southern Mexico Northwestern Southern America Hawaii Brazil Galapagos Islands Dominican Republic Wake Atoll, Pacific Ocean
resentative of this group is capable of producing textile fiber.
The origin of the D genomic group is associated with the spread of a Gossypium ancestral form from Africa over long distances about 5-10 MYA. Probably, it spread to western Mexico — the center of D genomic
diversity (Wendel and Grover, 2015). The appearance of endemic species in Peru (G. raimondii) and the Galapagos Islands (G. klotzschianum) is associated with the later spread of the D genome ancestor to these territories, probably during the Pleistocene (Wendel and Percival, 1990).
1.2. Polyploid species of the genus Gossypium
Subgenus Karpas Raf. (AD). The American polyploid species of cotton represent a monophyletic allotetra-ploid group containing two genomes — the A genome from Africa or Asia, close to the existing G. herbaceum and G. arboreum, and the D genome, close to G. raimon-dii (Fig. 1, 2) (Endrizzi et al., 1985; Small and Wendel, 1999; Paterson et al., 2012). By now, seven species have been described (Tab. 1). Two of them, G. ekmanianum and G. stephensii, have been recently discovered as endemics of the Dominican Republic and Wake Atoll in the Pacific, respectively (Grover et al., 2014; Gallagher et al., 2017). Two other species, G. hirsutum and G. barbadense, are cultivated species of cotton and are of great commercial importance today (Fang, 2018).
Thus, representatives of the genus Gossypium, including 45 diploids and 7 allotetraploids, fall into four subgenera: Gossypium (A, B, E, F genomes), Sturtia (C, G, K genomes), Houzingenia (D genome) and Karpas (AD genomes). The status of individual taxa in the genus Gossypium is still unclear, especially within the subgenera Gossypium and Sturtia. The study of representatives of these taxa is very difficult due to the inaccessibility of their growing areas, the poor representation of representatives in collections and the tendency to produce interspecific hybrids. This indicates the temporary nature of the majority of the taxonomy of Gossypium species.
2. The evolution of the cotton genome
The morphology of chromosomes is similar among the closely related species, and it is reflected in their ability to form interspecific hybrids that exhibit normal meiotic pairing of chromosomes and high fertility of F1 hybrids. The species of each of the genomic groups of the genus Gossypium have the same basic chromosome number (n = 13), however, the DNA content in each genome varies significantly — from ~880 Mb (D genome; 2C = 1.81 pg) to ~2400 Mb (K genome; 2C = 5.26 pg) (Fig. 2) (Hendrix and Stewart, 2005). It is believed that such a change in DNA content has been caused by the modification of repetitive DNA sequences (Geever, Katterman and Endrizzi, 1989). Along with that, the variation of the amount of DNA in diploid species offers a good model system for studying the causes of the genome size variation.
2.1. Polyploidization
Polyploidization is an important process in plant spe-ciation. It underlies the ample diversity of angiosperms (Alix, Gérard, Schwarzacher and Heslop-Harrison, 2017). The assumption that diploid cotton is a paleo-polyploid organism was first made about 90 years ago
when studying the behavior of chromosomes in the metaphase of meiosis (Denham, 1924; Lawrence, 1931; Davie, 1933; Skovsted, 1933). It was later shown that multiple duplicated segments of chromosomes found in the genomes of diploid species of cotton demonstrate that the ancestor of Gossypium underwent ancient polyploidization cycles with subsequent genome rearrangements and diploidization (Brubaker, Paterson and Wendel, 1999; Cronn, Zhao, Paterson and Wendel, 1996; Paterson, 2009; Paterson et al., 2012; Jiao and Paterson, 2014; Renny-Byfield et al., 2014; Renny-Byfield, Gong, Gallagher and Wendel, 2015; Rong et al., 2010). In addition to three acts of genome duplication that occurred in the ancestor of all flowering plants, the diploid ancestor of cotton underwent an additional five to six duplications shortly after divergence from the ancestor of Theo-broma cacao L. about 60 MYA (Fig. 2) (Bowers, Chapman, Rong and Paterson, 2003; Paterson et al., 2012; Renny-Byfield et al., 2015). Thus, modern cottons are at least paleooctaploids.
2.2. Mobile genetic elements
An increase in the number of mobile genetic elements (MGEs) along with polyploidization is probably one of the main factors determining the size of the plant genome (San Miguel and Bennetzen, 1998; Zhao et al., 1998; Bennetzen, Ma and Devos, 2005; Hawkins et al., 2006; Ozkan et al., 2010). The comparative analysis of Gossypium genomes with T. cacao and Arabidopsis thaliana (L.) Heynh. showed that the genomes of Gossypium species contain a higher number of MGEs (Wu et al., 2017). This may indicate that in addition to the full-genome duplication, a change in the genome size in the genus Gossypium is associated with the abundance of MGEs, in particular, Long Terminal Repeat (LTR) ret-rotransposons (Wu et al., 2017).
Based on the comparative analysis of the nucleotide sequences in the genomes of diploid species G. raimon-dii (D5 genome, 885 Mb) and G. arboreum (A2 genome, 1746 Mb), as well as of the allotetraploid species G. hirsutum ((AD)1 genome, 2173 Mb) (Paterson et al., 2012; Wang et al., 2012; Page et al., 2013; Kim, 2015; Li et al., 2015), it was found that the fraction of MGEs in the genomes of G. arboreum, G. raimondii and G. hirsutum is 57.09 %, 67.64 % and 67.36 %, respectively (Dillehay, Rossen, Andres and Williams, 2007; Wang et al., 2012). Moreover, A and AD genomes carry a significantly larger number of LTR retrotransposons than the D genome (Tab. 2). It was shown that the LTR-Copia sequences had been accumulating at a higher rate in the Gossy-pium species with the smallest genome (G. raimondii), while the LTR-Gypsy sequences are common in the species with larger genomes (Hawkins et al., 2006; Page et al., 2013). At the same time, it was found that one LTR-
Table 2. MGEs content in genomes of G. arboreum (A2 genome), G. raimondii (D5 genome) and G. hirsutum ((AD)i genome) (according to Wang et al., 2015)
MGE G. arboreum, % of genome G. raimondii, % of genome G. hirsutum, % of genome
LINE 1.20 1.50 1.56
SINE 0.01 0.09 0.03
LTR-Gypsy 55.80 33.80 52.54
LTR-Copia 5.50 11.10 8.36
Others 5.13 10.60 4.87
Total 67.64 57.09 67.36
Gypsy group, GORGE3 (Gossypium retrotransposable gypsy-like element), had undergone mass distribution in large cotton genomes to become the main reason for their size change (Hawkins et al., 2006).
MGEs and the fiber-forming ability. The most valuable feature of a number of species in the Gossypium genus is the ability to form unicellular fibers (trichomes) of different size on the seed surface (Kim, 2015). In cultivated species, these fibers are used for spinning. Among the different types of cotton capable of forming fiber, there are significant differences in its properties, since the two genomes, A and D, in the genus Gossypium make an unequal contribution to the development of fiber (see below) (Paterson et al., 2012; Xu et al., 2015). Thus, the allotetraploid G. hirsutum produces fibers longer than 3 cm, and the diploid G. arboreum produces 1.3-1.5 cm long fibers (Li et al., 2015). However, there are more fiber quality-related sites in the D subgenome in G. hirsutum than in the A subgenome, despite the fact that the relative of the D genome progenitor G. raimondii does not produce spinning fiber (Jiang, Wright, El-Zik and Paterson, 1998).
Over the past two decades, many genes that are involved in the regulation of growth and development of cotton fibers have been revealed (Shi et al., 2006; Wu et al., 2006; Taliercio and Boykin, 2007; Wu et al., 2007; Wang et al., 2010; Zhang et al., 2010; Walford, Wu, Llewellyn and Dennis, 2011; Kim, 2015). Along with that, it turned out that a large number of MGEs in Gossypium genomes are located close (within 5 kbp) to the fiber development genes, which allows supposing that these genetic elements could contribute to this process (Wang et al., 2012; Li et al., 2014, 2015; Kun Wang, Huang and Zhu, 2016; Wu et al., 2017). For example, the promoter region of the gene encoding GhMYB25 transcription factor, which is necessary for fiber development, has shown the LTR-Copia retrotransposon insertion (3928 bp) only in the D subgenome (Fig. 3). That positively correlates with a higher expression of the D genome homoeolog in G. hirsutum (Zhang et al., 2010; Walford et al., 2011; Wang et al., 2016). A similar mutation was noted for the ethylene
response factor (ERF) gene involved in the development of trichomes: the LINE retrotransposon insertion into the GhERF promoter in the D subgenome causes an increase in the expression level of this homoeolog compared to its A genomic copy (Shi et al., 2006; Qin et al., 2007; Wang et al., 2016).
A new look at the evolution of the genus Gossypium. It was previously believed that diploid forms of cotton carrying the A genome appeared less than 5 MYA after the divergence from the ancestor of the F genome forms (Wendel and Albert, 1992). Allotetraploid species were thought to have formed as a result of interspecific hybridization about 1-2 MYA (Wendel and Albert, 1992).
In 2018, a new family of LTR elements named CICR (Chinese Institute of Cotton Research) was identified in the genus Gossypium (Lu et al., 2018). It was shown that these MGEs are widespread in all chromosomes of the A and B genomes, but are almost absent in the genomes C-G (Cui et al., 2016; Lu et al., 2018). The analysis of CICR showed that the A and D genomes diverged at least 4 MYA (before the appearance of CICR), which coincides with the results of previous studies on the divergence time of the ancestors of these genomes about 5-10 MYA (Fig. 2) (Wendel and Albert, 1992; Senchina et al., 2003; Liu et al., 2015; Zhang et al., 2015). The divergence of the ancestors of the C-G genomes occurred probably about 3.5-4 MYA, i.e., approximately during the appearance of CICR elements (Lu et al., 2018). Besides, according to the distribution of these mobile elements, the A and B genomes are the closest to each other among the genomes of the genus Gossypium, having diverged about 2.5 MYA (Lu et al., 2018). It contradicts the previous information that the F genome is more similar to the A than to the B genome (Fig. 2) (Grover et al., 2004).
The formation of allotetraploid cotton about 1-1.5 MYA as a result of hybridization between the A and D genome ancestors coincides with the results of previous studies (Wendel, 1989; Wendel and Albert, 1992; Wendel and Cronn, 2003; Senchina et al., 2003; Li
et al., 2015; Zhang et al., 2015). However, it is assumed that allotetraploid cotton was formed after the CICR family silencing, since these MGEs were preserved in the A subgenome, though not transferred to the D subgenome (Lu et al., 2018).
Thus, the insertions of MGEs and their polymorphism among genomes and subgenomes could be a key factor in the evolution of cotton, as well as in the process of artificial selection of traits that determine fiber properties.
3. Expression of homoeologous genes in cotton
The key point in the evolution of genomes of polyploid organisms relates to the regulation of intergenomic interactions (including the nuclear-cytoplasmic ones), on the one hand, and normalization of the consequences of the gene duplication, on the other hand (Panchy, Lehti-Shiu and Shiu, 2016; Sattler, Carvalho and Clarindo, 2016).
The fusion of the A and D genomes of the allotet-raploid cotton ancestors into the genome of one organism with the A genome cytoplasm caused a change in the level and pattern of expression of genes from both genomes due to new interactions. As a consequence, the expression of some homoeologous genes underwent significant changes due to the merging of regulating factors and their target genes (Riddle and Birchler, 2003; Birchler, Riddle, Auger and Veitia, 2005; Chen, 2007; Panchy et al., 2016; Sattler et al., 2016). On the other hand, the suppression of some homoeologous genes expression occurred as a compensation of the change in gene dosage that accompanied polyploidy (Osborn et al., 2003; Birchler et al., 2005; Sattler et al., 2016).
3.1. Changes in the homoeologous genes expression
The first evidence that polyploidy within the genus Gos-sypium is accompanied by vast changes in the expression of genes appeared from the studies of 40 homoeologous genes in different organs of G. hirsutum (Adams, Cronn, Percifield and Wendel, 2003). Almost one-third of the studied genes demonstrated changes in expression towards a significant increase in the activity of one of the homoeologs and a decrease in the expression of the other. Special attention should be given to the genes that demonstrated organ-specific expression: while one of the genes in the homoeologous pair expressed itself in the organs of one type, the other gene was active only in the other organs (Adams, Cronn, Percifield and Wendel, 2003).
When studying the activity of the duplicated genes, it was also established that patterns of the homoeolo-
gous copies' expression were environment-sensitive. It was shown that the homoeologous genes of G. hirsutum demonstrate different levels of expression in different tissues under the influence of such abiotic stresses as an increase or decrease in temperature, deficiency or excess of water, and an increased content of salts (Liu and Adams, 2007; Dong and Adams, 2011). Probably, the differential expression of homoeologous genes in response to a stress or an environmental signal may be a factor that facilitates the preservation of the duplicated genes' functional state in the polyploid organism.
3.2. Expression of genes in synthetic cotton hybrids
The changes caused by distant hybridization at the early stages of allopolyploid organism formation should differ from those changes that took place in its subsequent evolution. In order to differentiate these changes, in a number of articles the expression of homoeologous genes was studied when comparing the synthetically created allopolyploids (or F1 hybrids) with the natural allopolyploid cotton species (Adams et al., 2003; Adams, Percifield and Wendel, 2004; Flagel, Udall, Nettleton and Wendel, 2008; Chaudhary et al., 2009). For example, a comparison of gene activity in the F1 hybrid, artificially produced by crossing G. arboreum and G. raimondii, and that in the natural G. hirsutum allopolyploid has shown that about 24 % of the genes with differential expression have demonstrated a similar change in expression in the F1 hybrid and in the natural allopolyploid, if compared with the parent forms (Flagel et al., 2008). The remaining 76 % of the genes of G. hirsutum with the expression changed in comparison with G. arboreum and G. rai-mondii could be determined by both the accumulated mutations and by the sub- or non-functionality of the duplicated genes (Flagel et al., 2008).
Thus, the merging of genomes plays an important, but only partial role in changing the pattern of expression of the homoeologous genes in the genus Gossy-pium, while the level of expression and tissue specificity of the genes demonstrate that specific patterns of the homoeologous genes expression can appear in both de novo created synthetic hybrids and remain in natural al-lopolyploids.
3.3. Dominance of allopolyploid cotton subgenomes
In allopolyploid plant forms resulting from interspecific hybridization, one of the parent subgenomes is dominant as a rule, i.e., it preserves the expression of homoeologous genes at a level similar to that of the genes' activity in the parent organism in relation to other homoeologs (Wang et al., 2006; Rapp, Udall and Wendel, 2009; Buggs et al.,
Fig. 3. Regulation of expression and dominance of homoeologous genes of allotetraploid cotton. Explanation is given in the text.
2010; Chang et al., 2010; Flagel and Wendel, 2010; Wood-house et al., 2010; Schnable, Springer and Freeling, 2011; Tang et al., 2012). Interestingly, such an expression profile is characteristic of the genes with both increased and decreased expression levels, so that the same diploid parent genome can be either dominant or recessive, depending on the particular combination (Rapp et al., 2009).
The dominance of a subgenome can manifest itself in a situation when the maternal genes of the nuclear genome and the plastome co-adapted to each other can be expressed and the paternal homoeologous copies silenced. An example of this kind has been described for the RuBisCO genes (Gong et al., 2012). The RuBisCO enzyme (4.1.1.39; ribulose-1.5-bisphosphate carboxylase/ oxygenase), which catalyzes the addition of CO2 to ri-bulose-1.5-bisphosphate in the Calvin cycle, consists of small subunits (SSU) encoded by nuclear genes, and of large subunits (LSU) encoded by plastome genes (Fig. 3) (Rodermel et al., 1996). The genes of the maternal A genome were shown to dominate in polyploid cotton, i.e., both the nuclear genes of the small rbcS subunits, and the genes of the large rbcL subunits transmitted from the mother, which may demonstrate co-evolution of genes of large and small subunits (Gong et al., 2012).
The subgenome dominance could also be associated with natural selection, which in the course of evolution eliminates various problems with regulating trait manifestation, caused by the fusion of genomes (Yoo, Szadkowski and Wendel, 2013). For instance, the shift in the expression of genes involved in fiber formation in al-lotetraploid cotton is directed towards the D genome as a rule (Flagel et al., 2008; Hovav et al., 2008; Guan, Song and Chen, 2014). Since the D genome donors are inca-
pable of producing fiber, it is quite likely that negative regulators, such as microRNAs and transcriptional repressors, suppress the expression of genes related to fiber formation in the D genome, compared to the A genome.
The homoeologous regulatory genes of the R2R3-MYB type — GhMYB2A and GhMYB2D — could serve as an example. They are homoeologs of the A. thaliana GLABROUS1 (GL1) gene involved in trichome formation (Fig. 3) (Wang et al., 2004; Ishida, Kurata, Okada and Wada, 2008; Pesch and Hùlskamp, 2009; Guan and Pang et al., 2014). It has been demonstrated that more mRNAs of the GhMYB2D gene than of GhMYB2A are synthesized during the initiation of cotton fiber formation (Guan and Pang et al., 2014). However, only GhMYB2A is involved in the process of fiber formation, since the products of GhMYB2D are the targets for miR828 and miR858 microRNAs (Fig. 3) (Pang et al., 2009; Guan and Pang et al., 2014).
Besides, it turned out that in A. thaliana gl1 -mutants, i.e., mutants incapable of forming trichomes, the overexpression of GhMYB2A restores the mutant phe-notype (Guan and Pang et al., 2014). Normally, the overexpression of GhMYB2D does not restore the gl1 pheno-type, but in the case of the miR828-binding site mutation, trichomes development is restored in gl1 -mutants (Guan and Pang et al., 2014). Thus, these studies suppose not only functional divergence between GhMYB2A and GhMYB2D in cotton, but also an important role of microRNAs in the process of fiber formation.
In total, the studies show that gene expression in polyploid cotton changes in comparison with its diploid predecessors, and unequal expression of one of the two homoeologs is a rule rather than an exception.
Conclusion
The review summarizes the results of works devoted to the studies on phylogenetic relationships in the genus Gossypium, evolution of genomes within this genus, regulation of homoeologous genes' expression and dominance of allotetraploid cotton subgenomes. Despite the large amount of available data, the status of individual taxa in the Gossypium genus is still unclear, especially within the Gossypium and Sturtia subgenera, due to their poor representation in collections, inaccessibility of the territories where representatives of these taxa occur and the tendency to produce interspecific hybrids. Studies of the distribution patterns of repeating DNA elements, such as MGEs, can shed light on the evolution of genomes in the genus Gossypium and on the time of their divergence. On the other hand, the analysis of MGEs polymorphism could help to reveal the genes that control fiber development in cotton. Further studies, combined with the available data, will offer ample opportunities for producing cotton varieties with the desired properties.
Acknowledgments
The present review was carried out within VIR project No. 0481-2019-0001.
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