Long noncoding RNAs underlie multiple domestication traits and leafhopper resistance in soybean

Weidong Wang; Jingbo Duan; Xutong Wang; Xingxing Feng; Liyang Chen; Chancelor B Clark; Stephen A Swarm; Jinbin Wang; Sen Lin; Randall L Nelson; Blake C Meyers; Xianzhong Feng; Jianxin Ma

doi:10.1038/s41588-024-01738-2

Long noncoding RNAs underlie multiple domestication traits and leafhopper resistance in soybean

Nat Genet. 2024 Apr 29. doi: 10.1038/s41588-024-01738-2. Online ahead of print.

Authors

Weidong Wang^#^{1

2

3}, Jingbo Duan^#^{1

2}, Xutong Wang^#^{1

2

4}, Xingxing Feng^#⁵, Liyang Chen^{1

2}, Chancelor B Clark^{1

2}, Stephen A Swarm^{6

7}, Jinbin Wang^{1

2}, Sen Lin^{1

2}, Randall L Nelson⁶, Blake C Meyers⁸, Xianzhong Feng⁹, Jianxin Ma^{10

11}

Affiliations

¹ Department of Agronomy, Purdue University, West Lafayette, IN, USA.
² Center for Plant Biology, Purdue University, West Lafayette, IN, USA.
³ College of Agronomy and Biotechnology, China Agricultural University, Beijing, China.
⁴ College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China.
⁵ Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, China.
⁶ Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
⁷ Beck's Hybrids, Atlanta, IN, USA.
⁸ Genome Center and Department of Plant Sciences, University of California, Davis, Davis, CA, USA.
⁹ Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun, China. fengxianzhong@iga.ac.cn.
¹⁰ Department of Agronomy, Purdue University, West Lafayette, IN, USA. maj@purdue.edu.
¹¹ Center for Plant Biology, Purdue University, West Lafayette, IN, USA. maj@purdue.edu.

^# Contributed equally.

PMID: 38684899
DOI: 10.1038/s41588-024-01738-2

Abstract

The origin and functionality of long noncoding RNA (lncRNA) remain poorly understood. Here, we show that multiple quantitative trait loci modulating distinct domestication traits in soybeans are pleiotropic effects of a locus composed of two tandem lncRNA genes. These lncRNA genes, each containing two inverted repeats, originating from coding sequences of the MYB genes, function in wild soybeans by generating clusters of small RNA (sRNA) species that inhibit the expression of their MYB gene relatives through post-transcriptional regulation. By contrast, the expression of lncRNA genes in cultivated soybeans is severely repressed, and, consequently, the corresponding MYB genes are highly expressed, shaping multiple distinct domestication traits as well as leafhopper resistance. The inverted repeats were formed before the divergence of the Glycine genus from the Phaseolus-Vigna lineage and exhibit strong structure-function constraints. This study exemplifies a type of target for selection during plant domestication and identifies mechanisms of lncRNA formation and action.

Abstract

Grants and funding