The Influence of Long-Term Retransposon Activity in Gossypium Genome Evolution  

Mengting Luo
Chen J.H., and Luo M.T., 2024, The influence of long-term retransposon activity in Gossypium genome evolution, Cotton Genomics and Genetics, 15(5): 249-258 (doi: 10.5376/cgg.2024.15.0024)
Author    Correspondence author
Cotton Genomics and Genetics, 2024, Vol. 15, No. 5   
Received: 14 Sep., 2024    Accepted: 16 Oct., 2024    Published: 23 Oct., 2024
© 2024 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

As a complex polyploid species, transposon activity has played a crucial role in the evolution of the cotton genome, influencing gene function, genome stability, and environmental adaptability. This study summarizes the major types of transposons present in the cotton genome and their distribution, exploring how transposon activity has shaped the structure and function of the cotton genome through genome expansion, chromosomal rearrangements, and gene duplication. Additionally, the role of transposons in the regulation of gene expression, gene capture, and environmental adaptability is analyzed in detail. The study reveals that transposon activity has driven the evolution of cotton fiber traits and has significantly impacted its stress resistance and disease resistance. Furthermore, transposons have played a key role in cotton domestication and polyploid genome formation. Understanding the long-term impact of transposon activity on cotton genome evolution and its role in regulating gene expression, promoting gene innovation, and adaptive evolution provides a theoretical foundation for the application of transposons in cotton genetic improvement, highlighting the potential of transposons as tools for genome editing in precision breeding.

Keywords
Cotton; Transposons; Genome evolution; Gene expression regulation; Precision breeding

1 Introduction

Cotton is one of the most economically significant crops globally, providing the primary natural fiber used in the textile industry. The genus Gossypium encompasses several species with complex polyploid genome structures, which have evolved through processes such as whole-genome duplication and allopolyploidization (Chen et al., 2020; Huang et al., 2021). These polyploid genomes are characterized by the presence of multiple sets of chromosomes, which contribute to their genetic diversity and adaptability.

 

Transposons, or transposable elements (TEs), are DNA sequences that can change their position within the genome. They are widespread in plant genomes and play a crucial role in shaping genome structure and function (Li and Cai, 2024). TE amplification has been recognized as a driving force behind genome size expansion and the evolution of higher-order chromatin structures in plants (Wang et al., 2021). In cotton, transposons have been implicated in genome diversification, gene-family expansion, and the regulation of gene expression (Chen et al., 2020; Huang et al., 2021).

 

The long-term activity of transposons has had profound effects on the evolution of the cotton genome. Polyploidization events, such as the combination of the A and D genomes in allotetraploid cotton, have been accompanied by bursts of transposon activity that have driven genomic changes (Page et al., 2016; Huang et al., 2021). These changes include gene loss, structural rearrangements, and the accumulation of repetitive sequences, which have contributed to the asymmetric evolution of the subgenomes (Zhang et al., 2015; Pan et al., 2020). Understanding the impact of transposon activity on cotton genome evolution is essential for unraveling the complexities of cotton genetics and improving breeding strategies.

 

This study comprehensively explores the impact of long-term transposon activity on the evolution of the cotton genome, aiming to elucidate the mechanisms by which transposons have shaped the cotton genome and highlight their role in the diversification and adaptation of cotton species. This research will not only deepen the understanding of cotton genome evolution but also provide valuable insights for future efforts in genetic recombination, epigenetic regulation modification, and targeted crop improvement for specific genes.

 

2 Types of Transposons in the Cotton Genome

2.1 Major transposon families in the cotton genome

The cotton genome, like many plant genomes, contains a variety of transposable elements (TEs) that play significant roles in its evolution and adaptation. The major families of transposons in the cotton genome include retrotransposons and DNA transposons. Retrotransposons are further divided into long terminal repeat (LTR) and non-LTR types. LTR retrotransposons, such as Ty1/Copia and Ty3/Gypsy, are the most abundant and influential in shaping the genome structure (Liu et al., 2018; Papolu et al., 2022). These elements replicate through an RNA intermediate, which is reverse transcribed and inserted back into the genome, leading to genome expansion and increased genetic diversity (Fukai et al., 2022; Hu et al., 2022). Non-LTR retrotransposons, including LINE-1 elements, also contribute to genome dynamics but are less prevalent in plants compared to LTR retrotransposons (Hancks and Kazazian, 2012).

 

DNA transposons, which move directly through a DNA intermediate, are another significant class of TEs in the cotton genome. These elements can excise themselves from one location and insert into another, causing mutations and genomic rearrangements (Casacuberta and Santiago, 2003). Both retrotransposons and DNA transposons are crucial for the genomic plasticity and adaptability of cotton.

 

2.2 Distribution of transposons in the cotton genome

The distribution of transposons in the cotton genome is non-random and varies among different families. LTR retrotransposons, for instance, are often found in pericentromeric regions where recombination is suppressed (Du et al., 2010). This localization helps in maintaining genome stability while allowing for occasional bursts of transposition that can drive evolution and adaptation (Papolu et al., 2022). In cotton, LTR retrotransposons from the progenitor D genome are more prevalent in the D-subgenome, while those from the progenitor A genome are more common in the A-subgenome (Liu et al., 2018). This subgenomic distribution pattern suggests a historical retention of transposon activity post-polyploidization.

 

The proportion of different transposon families in the cotton genome also varies. LTR retrotransposons constitute a significant portion of the genome, with some families having thousands of copies, while others are less abundant but still impactful (Liu et al., 2018). The distribution characteristics of each LTR retrotransposon family can influence the overall genome size and structure, contributing to the diversity observed within the cotton species.

 

2.3 Diversity of transposons in different subspecies of cotton

Comparative analysis of transposon composition in upland cotton (Gossypium hirsutum) and sea island cotton (Gossypium barbadense) reveals notable differences between these subspecies. Upland cotton, which is widely cultivated for its fiber, shows a higher diversity and abundance of LTR retrotransposons compared to sea island cotton (Liu et al., 2018). This diversity is likely a result of the different evolutionary pressures and breeding histories experienced by these subspecies.

 

In Gossypium hirsutum, the presence of diverse LTR retrotransposon families contributes to its adaptability and resilience, making it a robust crop for various environmental conditions (Liu et al., 2018). On the other hand, Gossypium barbadense, known for its superior fiber quality, has a more streamlined transposon composition, which may be associated with its specialized cultivation and breeding for specific traits.

 

3 Regulatory Mechanisms of Transposon Activity in Cotton

3.1 Autonomous and non-autonomous transposon activity in the cotton genome

Autonomous transposons, such as Long INterspersed Element-1 (LINE-1 or L1), are capable of self-replication and movement within the genome, whereas non-autonomous transposons rely on the enzymatic machinery of autonomous elements for their mobilization. In cotton, both types of transposons contribute to genetic diversity and genome evolution. Autonomous transposons can create new insertions and structural variations, which can have significant impacts on gene function and regulation (Hancks and Kazazian, 2012; Huang et al., 2012). Non-autonomous transposons, although unable to move independently, can still influence genome architecture by utilizing the transposition machinery of autonomous elements, thereby contributing to genomic rearrangements and the creation of novel regulatory elements (Faino et al., 2016; Liu et al., 2017).

 

3.2 Genome stability and transposon suppression mechanisms

Plants have evolved sophisticated epigenetic mechanisms to suppress excessive transposon activity and maintain genome stability. DNA methylation and small interfering RNA (siRNA)-mediated silencing are two primary methods by which plants control transposon activity. DNA methylation involves the addition of methyl groups to cytosine residues in transposon sequences, leading to transcriptional repression. siRNA-mediated silencing involves the production of small RNA molecules that guide the degradation or translational repression of transposon transcripts (Lisch, 2009; Liu et al., 2017; Huang et al., 2021). These mechanisms are crucial for preventing the potentially deleterious effects of unchecked transposon activity, such as insertional mutagenesis and genome instability (Lisch, 2009; Pradhan and Ramakrishna, 2021).

 

3.3 Induction of transposon activity by environmental stress

Environmental stress conditions, such as drought, temperature extremes, and pathogen attack, can induce transposon activity in the cotton genome. This stress-induced activation of transposons can lead to increased genetic variation and rapid adaptation to changing environments. For instance, transposons can mediate genomic rearrangements and create new regulatory elements that may enhance stress tolerance or other adaptive traits (Lisch, 2009; Faino et al., 2016; Sharma and Peterson, 2022). The activation of transposons under stress conditions highlights their role as dynamic elements that can drive genome evolution and contribute to the plasticity of the cotton genome (Chuong et al., 2016; Branco and Chuong, 2020).

 

4 Effects of Transposon Activity on Cotton Genome Structure

4.1 Genome expansion and contraction

Transposon activity plays a significant role in the expansion and contraction of the cotton genome. The amplification of transposable elements (TEs) has been identified as a driving force behind genome size variation among different cotton species. For instance, comparative genome analyses of Gossypium rotundifolium (K2), G. arboreum (A2), and G. raimondii (D5) reveal substantial differences in genome sizes, which are attributed to lineage-specific TE amplification. The genome sizes of these species are 2.44 Gb, 1.62 Gb, and 750.19 Mb, respectively, indicating that TE activity has contributed to the large genome size differences observed (Wang et al., 2021). Additionally, the bursts of transposable elements have been linked to the expansion of the A-genome in cotton, further emphasizing the role of TEs in genome size dynamics (Huang et al., 2021).

 

4.2 Chromosomal rearrangements and gene positioning

Transposon-mediated changes can lead to significant chromosomal rearrangements, including translocations, inversions, and the formation of duplicated regions. These rearrangements can alter gene positioning and affect the overall chromosomal architecture. In cotton, the recent amplification of TEs has been associated with the formation of lineage-specific topologically associating domain (TAD) boundaries. Only 42% of TAD boundaries are conserved among the three studied cotton genomes, indicating that TE activity has played a role in reshaping chromosome structures (Wang et al., 2021). Furthermore, polyploidy in cotton has induced recombination suppression, which correlates with altered epigenetic landscapes. This suppression can be overcome by wild introgression, suggesting that transposon activity and polyploidy together influence chromosomal rearrangements and gene positioning (Chen et al., 2020).

 

The reshaping of chromosome structures in cotton due to active transposon regions is evident in the comparative genome analyses of Gossypium species. The study highlights that approximately 17% of syntenic genes exhibit changes in chromatin status between active (‘A’) and inactive (‘B’) compartments. TE amplification has been linked to an increase in the proportion of the A compartment in gene regions, affecting around 7 000 genes in K2 and A2 relative to D5. This indicates that active transposon regions have a profound impact on the chromosomal architecture and gene positioning in the cotton genome (Wang et al., 2021).

 

4.3 Repetitive sequences and gene copy number variation

Transposon activity also leads to gene duplications or deletions, affecting copy number variation in cotton genes. The diversification of polyploid cotton genomes has been driven by subgenomic transposon exchanges, which equilibrate genome size and contribute to gene-family diversification. These exchanges result in differential evolutionary trajectories and homoeolog expression divergence among polyploid lineages. The impact of transposon activity on gene copy number variation is further evidenced by the diversification of gene families and the expression divergence observed in polyploid cotton species (Chen et al., 2020).

 

Additionally, the burst-like amplification of transposons has promoted the expansion of the A genome, leading to changes in gene copy numbers and influencing the overall genomic landscape. Huang et al. (2021) found that the evolutionary process of the AD genome cotton was closely related to the hybridization between A and D genome cotton, with widespread and far-reaching geographic distribution (Figure 1). Furthermore, the morphological differences in seed fibers (cotton fibers) are also linked to the evolutionary adaptability of cotton species. Transposon activity has played a key role in structural variations of the cotton genome. By facilitating gene duplication or loss, transposons can impact cotton traits and fiber quality. This provides significant insights into the complexity and diversity of the cotton genome structure and lays the groundwork for future breeding improvements.

 

 

 

5 Regulatory Effects of Transposon Activity on Cotton Gene Expression

5.1 Effects of transposon insertion in gene regulatory regions

Transposon insertions in promoters or enhancers can significantly alter gene expression patterns. These insertions can introduce novel regulatory elements or disrupt existing ones, leading to changes in the transcriptional activity of adjacent genes. For instance, transposons can provide new cis-acting regulatory sites that function as enhancers or alternative promoters, thereby modifying the expression patterns of nearby genes (Pavlicev et al., 2015; Hirsch and Springer, 2017; Sharma and Peterson, 2022).

 

A notable example of transposon-induced gene expression changes is observed in the stress-resistance genes of cotton. Transposon insertions in the promoters of these genes can enhance their expression, particularly under stress conditions. This phenomenon has been documented in other plant species as well, where transposon insertions in stress-response gene promoters lead to increased gene activity, thereby aiding in the plant's adaptation to environmental stress. For example, the Tf1 transposon in Schizosaccharomyces pombe preferentially integrates into the promoters of stress-response genes, enhancing their expression and promoting cell survival under stress (Guo and Levin, H. 2010; Feng et al., 2012).

 

5.2 Transposons and epigenetic regulation

Transposon insertions can also regulate gene expression through epigenetic mechanisms such as DNA methylation and histone modifications. These insertions can alter the chromatin structure, making it more or less accessible to the transcriptional machinery. For instance, transposons can introduce histone modifications like H3K4me3, H3K9ac, and H3K27ac, which are associated with active chromatin states, or H3K27me3 and H3K9me3, which are linked to repressive chromatin states. These modifications can either activate or silence gene expression depending on the context of the insertion (Igolkina et al., 2019; Cao et al., 2023).

 

5.3 Non-coding RNA regulation derived from transposons

Transposons can generate small RNAs, such as siRNAs and piRNAs, which play crucial roles in gene silencing and regulation. These small RNAs are derived from transposon sequences and can target complementary mRNA transcripts for degradation or translational repression. This mechanism is a vital part of the plant's defense against transposon activity and helps maintain genomic stability (Hirsch and Springer, 2017; Su et al., 2020). For example, in maize, transposons can induce the production of small RNAs that regulate the expression of genes involved in various biological processes, including stress responses and developmental pathways (Su et al., 2020).

 

6 Contribution of Transposon Activity to Cotton Trait Evolution

6.1 Transposon-mediated formation of new gene functions

Transposons, or transposable elements (TEs), are known to play a significant role in the formation of new gene functions through mechanisms such as gene capture and genome rearrangements. These processes can drive the evolution of cotton traits by creating novel genetic variations that can be selected for advantageous traits.

 

Transposons can capture gene sequences and incorporate them into new genomic contexts, leading to the formation of new functional genes. This process, known as exon shuffling, allows for the creation of genes with novel functionalities by combining existing gene segments in new ways. For instance, DNA transposons have been shown to provide a recurrent supply of exons and splice sites, which can be incorporated into host genomes to form new protein-coding genes (Cosby et al., 2020). This mechanism has been observed in various organisms and is a powerful driver of genetic innovation.

 

In cotton, transposon-mediated genome rearrangements are closely linked to the evolution of fiber development-related genes. Comparative genome analysis of different cotton species has shown that transposon amplification has driven significant genome size differences and changes in chromatin structure, which in turn affect gene expression (Wang et al., 2021). Figure 2 illustrates the differences in length distribution of various TE families in the K2, A2, and D5 genomes, indicating that transposable elements are major drivers of genome size variation, highlighting their important role in the evolution of the Gossypium genome. These rearrangements may lead to the formation of new gene functions related to fiber development, improving cotton fiber quality and yield.

 

6.2 Transposons and environmental adaptability

Transposon activity can enhance cotton's adaptability to environmental stress conditions such as drought and salinity. By modulating gene expression and creating genetic diversity, transposons enable cotton plants to better cope with adverse environmental conditions. Transposons can influence the transcriptional activity of neighboring genes by altering the epigenomic profile of the region or by changing the relative position of regulatory elements (Ariel and Manavella, 2021). This can lead to the upregulation of stress-resistant genes, providing cotton plants with an adaptive advantage under stressful conditions.

 

In plants, transposon-derived noncoding RNAs have been shown to play a role in the regulation of gene expression under stress conditions. These noncoding RNAs can interact with protein partners, sequester active small RNAs, and form duplexes with DNA or other RNA molecules, thereby modulating the expression of stress-responsive genes (Ariel and Manavella, 2021). This mechanism allows cotton plants to rapidly adapt to changing environmental conditions by enhancing the expression of genes that confer resistance to drought and salinity.

 

6.3 The role of transposons in cotton disease resistance

Transposon activity promotes diversity and rapid evolution of cotton disease resistance genes, enabling cotton plants to better defend against pathogens. The dynamic nature of transposons allows for the continuous generation of genetic variations, which can be selected for enhanced disease resistance. Transposons can drive the evolution of disease resistance genes by creating new gene combinations and regulatory elements. For example, transposons have been shown to contribute to the evolution of virulence genes in pathogens by mediating genomic rearrangements and duplications (Faino et al., 2016). This process can similarly enhance the diversity and adaptability of disease resistance genes in cotton.

 

Comparative genome analyses have highlighted the role of transposon-mediated genome expansion in shaping the 3D genomic architecture of cotton. This expansion is associated with changes in chromatin status and the formation of lineage-specific topologically associating domain (TAD) boundaries, which can influence gene expression. These findings suggest that transposon activity is a key driver of genetic diversity and rapid evolution in cotton, particularly in the context of disease resistance.

 

7 Contribution of Transposons to Cotton Domestication and Polyploidization

7.1 The role of transposons in cotton domestication

A comparison between wild and cultivated cotton reveals the significant contribution of transposons to genomic changes during domestication. Transposable elements (TEs) have been shown to drive genome size expansion and contribute to the regulatory evolution of domesticated cotton. For instance, the amplification of TEs has been linked to changes in chromatin structure and gene expression, which are crucial for the development of desirable traits in cultivated cotton (Bao et al., 2019; Wang et al., 2021).

 

During the domestication of cotton, certain fiber quality and yield traits have been positively selected, and this selection is mediated by transposon activity. The asymmetric evolution observed in the A and D subgenomes of allotetraploid cotton (Gossypium hirsutum) highlights the role of TEs in this process. The A subgenome, in particular, has undergone more structural rearrangements and TE insertions, which are associated with the selection of genes for fiber improvement (Zhang et al., 2015; Fang et al., 2017). This suggests that TEs have played a pivotal role in the domestication process by facilitating the selection of advantageous traits.

 

Huang et al. (2021) found that the evolutionary process of cotton was significantly influenced by transposon activity, particularly during the formation of allotetraploids. Transposons may cause structural changes in the genome by moving, duplicating, or deleting specific genes (Figure 3). These genetic changes contributed to the selection of certain traits during the domestication of cotton, such as improvements in fiber length and quality. Studying transposon activity can provide better insights into genome plasticity and its potential in cotton breeding.

 

 

 

7.2 The role of transposons in cotton polyploid formation

Transposons accelerate genome evolution during polyploidization through genome rearrangements and chromosome duplication. Polyploidization often induces bursts of transposition, which can lead to rapid genomic and epigenetic restructuring. This is particularly evident in the case of allotetraploid cotton, where the merger and doubling of genomes have resulted in significant TE activity (Hu et al., 2010; Vicient and Casacuberta, 2017). These transposon-induced changes contribute to the dynamic nature of polyploid genomes, facilitating the rapid adaptation and evolution of polyploid cotton species.

 

7.3 Transposon behavior in polyploid cotton

The differential activity of transposons in different subgenomes of polyploid cotton has a profound impact on trait evolution. In allotetraploid cotton, the A and D subgenomes exhibit distinct patterns of TE activity, which influence gene expression and trait development. For example, the A subgenome shows more frequent TE insertions and structural rearrangements, which are linked to the evolution of fiber quality traits. In contrast, the D subgenome is associated with stress tolerance traits (Zhang et al., 2015; Fang et al., 2017). This differential transposon activity underscores the complex interplay between TEs and genome evolution in polyploid cotton, driving the diversification of traits that are essential for cotton improvement.

 

8 Future Research Directions

8.1 Application of high-throughput sequencing technologies in transposon research

The advent of third-generation sequencing technologies, such as Oxford Nanopore Technologies, has significantly advanced our understanding of transposon activity in the cotton genome. For instance, comparative genome analyses of different cotton species have revealed the extent of lineage-specific transposable element (TE) amplification and its role in genome size expansion and chromatin structure evolution (Wang et al., 2021). These high-throughput sequencing technologies, combined with genome-wide association studies (GWAS), can provide a more detailed and comprehensive analysis of transposon activity, enabling researchers to identify specific TEs associated with important agronomic traits (Ding, 2024). This approach will facilitate the fine-scale mapping of transposon insertions and their functional impacts on the cotton genome.

 

8.2 Integrating transposon and functional genome studies

Exploring the complex associations between transposons and the functional genome of cotton is crucial for understanding their roles in trait regulation. Recent studies have shown that polyploidy and subgenomic transposon exchanges contribute to genome diversification and the evolution of gene families in cotton (Chen et al., 2020). These exchanges can lead to differential gene expression and epigenetic modifications, which are essential for trait development and adaptation. By integrating transposon research with functional genomics, scientists can uncover the regulatory networks and epigenetic landscapes influenced by TEs, providing insights into how these elements drive trait variation and evolution in cotton.

 

8.3 Potential of combining transposon activity with precision breeding

Regulating transposon activity through genome editing technologies, such as CRISPR/Cas9, holds great potential for advancing precision breeding in cotton. The ability to manipulate TEs can lead to targeted modifications in the genome, enhancing desirable traits such as fiber quality, pest resistance, and stress tolerance. For example, the manipulation of specific transposons involved in the ethylene production pathway has been shown to regulate fiber elongation in cotton (Huang et al., 2021). By combining transposon activity regulation with precision breeding techniques, researchers can develop new cotton varieties with improved traits, ultimately contributing to sustainable cotton production and crop improvement.

 

Acknowledgments

Thank you Ms. B. Chen provided assistance during the process of literature review and analysis.

 

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

 

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Cotton Genomics and Genetics
• Volume 15
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