Celine, a long interspersed nuclear element retrotransposon, colonizes in the centromeres of poplar chromosomes

Author:

Xin Haoyang12ORCID,Wang Yiduo3ORCID,Zhang Wenli3ORCID,Bao Yu4ORCID,Neumann Pavel5ORCID,Ning Yihang1,Zhang Tao4ORCID,Wu Yufeng3ORCID,Jiang Ning67ORCID,Jiang Jiming267ORCID,Xi Mengli1ORCID

Affiliation:

1. State Key Laboratory of Tree Genetics and Breeding/Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University , Nanjing 210037 , China

2. Department of Plant Biology, Michigan State University , East Lansing, MI 48824 , USA

3. The State Key Laboratory of Crop Genetics and Germplasm Enhancement/Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University , Nanjing 210095 , China

4. Jiangsu Key Laboratory of Crop Genetics and Physiology/Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding/Co-Innovation Centre for Modern Production Technology of Grain Crops/Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University , Yangzhou 225009 , China

5. Biology Centre, Czech Academy of Sciences, Institute of Plant Molecular Biology , České Budějovice 37005 , Czech Republic

6. Department of Horticulture, Michigan State University , East Lansing, MI 48824 , USA

7. Michigan State University AgBioResearch , East Lansing, MI 48824 , USA

Abstract

Abstract Centromeres in most multicellular eukaryotes are composed of long arrays of repetitive DNA sequences. Interestingly, several transposable elements, including the well-known long terminal repeat centromeric retrotransposon of maize (CRM), were found to be enriched in functional centromeres marked by the centromeric histone H3 (CENH3). Here, we report a centromeric long interspersed nuclear element (LINE), Celine, in Populus species. Celine has colonized preferentially in the CENH3-associated chromatin of every poplar chromosome, with 84% of the Celine elements localized in the CENH3-binding domains. In contrast, only 51% of the CRM elements were bound to CENH3 domains in Populus trichocarpa. These results suggest different centromere targeting mechanisms employed by Celine and CRM elements. Nevertheless, the high target specificity seems to be detrimental to further amplification of the Celine elements, leading to a shorter life span and patchy distribution among plant species compared with the CRM elements. Using a phylogenetically guided approach, we were able to identify Celine-like LINE elements in tea plant (Camellia sinensis) and green ash tree (Fraxinus pennsylvanica). The centromeric localization of these Celine-like LINEs was confirmed in both species. We demonstrate that the centromere targeting property of Celine-like LINEs is of primitive origin and has been conserved among distantly related plant species.

Funder

National Science Foundation

United States Department of Agriculture National Institute of Food and Agriculture and AgBioResearch at Michigan State University

NSF

National Natural Science Foundation of China

Publisher

Oxford University Press (OUP)

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