Comparative study of pine reference genomes reveals transposable element interconnected gene networks

Abstract

Background: Sequencing the giga-genomes of several pine species belonging to the ancient gymnosperm clade has enabled comparative genomic analyses of these widely distributed outcrossing tree species. Initial sequence studies have revealed the wide distribution and extraordinary diversity of transposable elements (TEs) that occupy the large intergenic spaces. Our previous investigations revealed significant variations of class I TEs within pine subpopulations, but inoculation with pathogen induced correlated expression of TE families in pine seedlings, suggesting TE co-localisation with stress-responsive genes. In this study, we analyzed the distribution of TEs in gene regions of the assembled genomes of Pinus taeda and Pinus lambertiana using high-performance computing resources.Results: The quality of draft genomes and the genome annotation have significant consequences for the investigation of TEs and these aspects are discussed. Several TE families were identified in both species genomes frequently inserted into genes or their flanks. The non-autonomous MITE3321 family found in gene flanking regions and provide TATA boxes, several ARR1, DOF, WRKY and GT-binding sites, which are important signals in plant transcription activation and stress-response regulation. Distribution of MITE3321 across gene non-coding regions suggests action of selective pressure on this sequences and formation of gene sub-networks, depending on the location of MITE insertions. DNA TE DTX184 could potentially form microRNAs or provide its target site, thereby connect about 200 important stress-responsive genes in both pine species. Several retrotransposons propagated in gene regions were also identified, such as Copia-1813 containing important light-responsive regulative sequences, however full- length structures of low-copy-number TEs couldn’t be verified in the current genome assemblies. Only rare gene homologs carried similar insertions, indicating that most transposition events occurred after separation of investigated pine species. Node genes that contain many types of interspersed repeats were identified and observed in multiple potential transposable element associated networks.Conclusions: This study demonstrated the increased accumulation of TEs in the introns of stress-responsive genes of pines and the probability of rewiring them in responsive networks and sub-networks interconnected with node genes containing multiple TEs. Many such regulatory influences could lead to the adaptive environmental response clines that are characteristic of naturally spread pine populations.

Epigenetics: a catalyst of plant immunity against pathogens

“…Similarly, 67% of insertions by the non‐LTR retrotransposon Au SINE in wheat are associated with genes, including defence‐related genes, with the majority of insertions within introns (Keidar et al ., 2018). In pine, TE insertions have been shown to be enriched within defence genes, including NONEXPRESSOR OF PATHOGENESIS‐RELATED PROTEINS‐1 , which controls SA signalling and SAR (Voronova et al ., 2020). In rice, CHG/H3K9me2‐enriched introns are present in 11% of all genes (Espinas et al ., 2020).…”

Distinct composition and amplification dynamics of transposable elements in sacred lotus (Nelumbo nucifera Gaertn.)

“…Average introns in model plants are rather small (Wendel et al., 2002); accordingly, they contain limited amounts of TEs. Prevalence of large introns has been reported for several gymnosperm species, with giant genomes ranging from 10 to 31 Gb (Guan et al., 2016; Nystedt et al., 2013; Stival Sena et al., 2014; Voronova et al., 2020; Zimin et al., 2014; Zimin et al., 2017). In addition, a few angiosperm plants have been reported with large introns (average size 2 kb or longer), including Phalaenopsis equestris , Liriodendron chinense , and Ceratophyllum demersum (Cai et al., 2015; Chen et al., 2019; Yang et al., 2020), yet the composition and enrichment of TEs were not well studied in these species.…”

“…For example, in humans, a large TE fraction is located in the introns of genes, leading to the expansion of genic regions (Lander et al., 2001; Sela et al., 2007). In plants, the prevalence of large introns is predominantly observed in gymnosperms with very large genome sizes of 10 Gb or more (Guan et al., 2016; Nystedt et al., 2013; Stival Sena et al., 2014; Voronova et al., 2020; Zimin et al., 2017). In contrast, most sequenced angiosperms have relatively compact genic regions.…”

Stress-responsive retrotransposable elements in conifers

“…Few cases of recent transposition have been reported to date (Tamura et al, 2015;Stevens et al, 2016). Although direct evidence of changes in gene regulation in conifers has not been reported, the production of whole-genome sequences permitted a comprehensive analysis of the distribution of LTR-RTs in the genic regions of loblolly pine and sugar pine (Voronova et al, 2020). Those researchers constructed a conifer-specific TE-derived repeat database of 9,107 representative sequences acquired from PIER v.2.0 (Pine Interspersed Element Resource) (Neale et al, 2014).…”

“…Whereas no clear enriched biological function was detected among genes with insertions of identical TEs in their gene-flanking regions, genes with identical TE insertions within their introns were involved in defense and regulative response processes. Voronova et al (2020) also focused on the function of genes with multiple TE insertions. Such genes have many Gene Ontology (GO) terms, and the authors speculated that they are involved in many cellular processes and are essential for the response to the environment.…”