Evolution of TE-initiated ELEs Generates Subgenome-biased Spike Specificity in Common Wheat

Common wheat (Triticum aestivum, AABBDD) represents a quintessential example of an allohexaploid species, having arisen through a series of two sequential hybridization events. This complex genomic structure combines the distinct genetic traits of its three diploid progenitors, endowing the species with considerable genomic plasticity and the capacity for broad environmental adaptation. As a consequence, Triticum aestivum has been cultivated extensively and forms a corner stone of the global food supply.

 

From an evolutionary standpoint, the combinatione of divergent genomes furnishes a wealth of genetic material, which underpins the evolution of polyploids and contributes to phenotypic versatility. However, the intricate molecular mechanisms that drive these processes remain enigmatic. Research indicates that the divergence of wheat subgenomes is largely attributable to species-specific amplification of transposable elements (TEs) in the ancestral diploid species.

 

In this study, the research team, employing a combination of high-throughput experimental methodologies and computational analyses, unearthed a plethora of distal regulatory elements derived from TEs, which exert a significant influence on the transcriptional regulation of subgenomes.

 

The research collaboration led by Professor XUE Yongbiao from the Institute of Genetics and Developmental Biology (IGDB) of the Chinese Academy of Sciences, Professor ZHANG Yijing from the Institute of Plant Biology at the School of Life Sciences, Fudan University, Professor DONG Zhicheng from the School of Life Sciences at Guangzhou University, and Professor Jungnam Cho from the Department of Biosciences of Durham University, has developed an innovative computational pipeline utilizing CAGE-seq in conjunction with multidimensional epigenomic datasets to pinpoint the initiation sites of both coding and non-coding transcripts. Their findings reveal a substantial number of nascent strand non-coding RNAs derived from TEs, predominantly situated within the long terminal repeat (LTR) regulatory domains, and exhibiting characteristics of active chromatin states associated with regulatory elements.

 

Through a comparative analysis of subgenome expression profiles across various tissues, the researchers identified a TE family with a subgenome-biased amplification pattern that displayed a pronounced tissue-specific expression of nascent strand RNAs. This particular TE family underwent specific expansion in the diploid ancestor of the A subgenome. Employing RNA interference and overexpression techniques, the study demonstrated that aberrant expression of nascent strand RNAs from this TE family induces morphological alterations in the wheat spike, and these changes may be linked to the domestication of wheat inflorescence architecture (Figure). Although the resultant knockout of TE-derived nascent strand RNAs also induces DNA methylation at the corresponding loci, it remains uncertain whether these phenotypic variations are a direct consequence of TE regulatory element function or are mediated through nascent strand RNAs.

 

Nonetheless, this investigation posits that the predictive analysis of regulatory element functionality via nascent strand RNAs offers novel methodological paradigms for the functional elucidation of remote regulatory elements within the expansive wheat genome. Specifically, the study provides new insights into the correlation between the plethora of transposable elements and the functional evolutionary dynamics of polyploidy in wheat.

 

This study entitled "Transposable element-initiated enhancer-like elements generate the subgenome biased spike specificity of polyploid wheat," has been published in Nature Communications on the 17th of November, 2023 (DOI: 10.1038/s41467-023-42771-9). This study was funded by the National Natural Science Foundation of China.

 

 

 

Contact:

Prof. XUE Yongbiao

Institute of Genetics and Developmental Biology, Chinese Academy of Sciences

Email: ybxue@genetics.ac.cn

 

Prof. ZHANG Yijing

Institute of Plant Biology, School of Life Sciences, Fudan University

Email: zhangyijing@fudan.edu.cn

 

Prof. DONG Zhicheng

School of Life Sciences, Guangzhou University

e-mail: zc_dong@gzhu.edu.cn

 

Prof. Jungnam Cho

Department of Biosciences, Durham University

e-mail: jungnam.cho@durham.ac.uk