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Plant Cell. 2019 Mar;31(3):563-578. doi: 10.1105/tpc.18.00601. Epub 2019 Feb 13.

Evolutionary Origins of Pseudogenes and Their Association with Regulatory Sequences in Plants.

Xie J1,2,3, Li Y1,2,3, Liu X2,3, Zhao Y1,2,3, Li B1,2,3,4, Ingvarsson PK5, Zhang D6,2,3.

Author information

1
Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, People's Republic of China.
2
National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, People's Republic of China.
3
Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, People's Republic of China.
4
Department of Forestry, North Carolina State University, Raleigh, North Carolina 27695-8203.
5
Linnean Center for Plant Biology, Department of Plant Biology, Swedish University of Agricultural Sciences, Box 7080, SE-750 07 Uppsala, Sweden.
6
Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, People's Republic of China deqiangzhang@bjfu.edu.cn.

Abstract

Pseudogenes (Ψs), nonfunctional relatives of functional genes, form by duplication or retrotransposition, and loss of gene function by disabling mutations. Evolutionary analysis provides clues to Ψ origins and effects on gene regulation. However, few systematic studies of plant Ψs have been conducted, hampering comparative analyses. Here, we examined the origin, evolution, and expression patterns of Ψs and their relationships with noncoding sequences in seven angiosperm plants. We identified ∼250,000 Ψs, most of which are more lineage specific than protein-coding genes. The distribution of Ψs on the chromosome indicates that genome recombination may contribute to Ψ elimination. Most Ψs evolve rapidly in terms of sequence and expression levels, showing tissue- or stage-specific expression patterns. We found that a surprisingly large fraction of nontransposable element regulatory noncoding RNAs (microRNAs and long noncoding RNAs) originate from transcription of Ψ proximal upstream regions. We also found that transcription factor binding sites preferentially occur in putative Ψ proximal upstream regions compared with random intergenic regions, suggesting that Ψs have conditioned genome evolution by providing transcription factor binding sites that serve as promoters and enhancers. We therefore propose that rapid rewiring of Ψ transcriptional regulatory regions is a major mechanism driving the origin of novel regulatory modules.

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