High-quality assembled and annotated genomes of Nicotiana tabacum and Nicotiana benthamiana reveal chromosome evolution and changes in defense arsenals

Jubin Wang; Qingling Zhang; Jeffrey Tung; Xi Zhang; Dan Liu; Yingtian Deng; Zhendong Tian; Huilan Chen; Taotao Wang; Weixiao Yin; Bo Li; Zhibing Lai; Savithramma P Dinesh-Kumar; Barbara Baker; Feng Li

doi:10.1016/j.molp.2024.01.008

High-quality assembled and annotated genomes of Nicotiana tabacum and Nicotiana benthamiana reveal chromosome evolution and changes in defense arsenals

Mol Plant. 2024 Mar 4;17(3):423-437. doi: 10.1016/j.molp.2024.01.008. Epub 2024 Jan 24.

Authors

Jubin Wang¹, Qingling Zhang², Jeffrey Tung³, Xi Zhang⁴, Dan Liu⁴, Yingtian Deng⁴, Zhendong Tian⁵, Huilan Chen⁴, Taotao Wang⁴, Weixiao Yin⁶, Bo Li⁷, Zhibing Lai⁸, Savithramma P Dinesh-Kumar⁹, Barbara Baker¹⁰, Feng Li¹¹

Affiliations

¹ National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, Hubei 430070, China; The Key Laboratory of Horticultural Plant Genetic and Improvement of Jiangxi Province, Institute of Biological Resources, Jiangxi Academy of Sciences, Nanchang 330299, China.
² National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Institute of Vegetables and Flowers, Jiangxi Academy of Agricultural Sciences, Nanchang 330200, China.
³ Plant Gene Expression Center, Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94706, USA.
⁴ National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, Hubei 430070, China.
⁵ National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China.
⁶ College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China.
⁷ College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China.
⁸ College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China.
⁹ Department of Plant Biology and The Genome Center, College of Biological Sciences, University of California, Davis, Davis, CA 95616, USA.
¹⁰ Plant Gene Expression Center, Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94706, USA. Electronic address: bbaker@berkeley.edu.
¹¹ National Key Laboratory for Germplasm Innovation and Utilization for Fruit and Vegetable Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, Hubei 430070, China; Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China. Electronic address: chdlifeng@mail.hzau.edu.cn.

PMID: 38273657
DOI: 10.1016/j.molp.2024.01.008

Abstract

Nicotiana tabacum and Nicotiana benthamiana are widely used models in plant biology research. However, genomic studies of these species have lagged. Here we report the chromosome-level reference genome assemblies for N. benthamiana and N. tabacum with an estimated 99.5% and 99.8% completeness, respectively. Sensitive transcription start and termination site sequencing methods were developed and used for accurate gene annotation in N. tabacum. Comparative analyses revealed evidence for the parental origins and chromosome structural changes, leading to hybrid genome formation of each species. Interestingly, the antiviral silencing genes RDR1, RDR6, DCL2, DCL3, and AGO2 were lost from one or both subgenomes in N. benthamiana, while both homeologs were kept in N. tabacum. Furthermore, the N. benthamiana genome encodes fewer immune receptors and signaling components than that of N. tabacum. These findings uncover possible reasons underlying the hypersusceptible nature of N. benthamiana. We developed the user-friendly Nicomics (http://lifenglab.hzau.edu.cn/Nicomics/) web server to facilitate better use of Nicotiana genomic resources as well as gene structure and expression analyses.

Keywords: NLR; Nicotiana benthamiana; Nicotiana tabacum; disease resistance; evolution; genomics.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Chromosomes*
Genes, Plant
Genomics
Molecular Sequence Annotation
Nicotiana* / genetics