Alternative splicing of lncRNA LAIR fine‐tunes the regulation of neighboring yield‐related gene LRK1 expression in rice

• Published in: The Plant journal : for cell and molecular biology Vol. 119; no. 4; pp. 1751 - 1766
• Main Authors: Wang, Ying, Cao, Liming, Liu, Mingyu, Yan, Peiwen, Niu, Fuan, Dong, Shiqing, Ma, Fuying, Lan, Dengyong, Zhang, Xinwei, Hu, Jian, Xin, Xiaoyun, Yang, Jinshui, Luo, Xiaojin
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.08.2024
• Subjects: Agricultural production; Alternative splicing; Annotations; Binding; Crop yield; Environmental changes; Environmental conditions; Epigenetics; fine‐tuning regulation; Gene expression; Gene polymorphism; Introns; Isoforms; LAIR; long noncoding RNA; LRK gene cluster; molecular polymorphism breeding; Non-coding RNA; Plant breeding; Polymorphism; Protein structure; Rice; rice yield; Secondary structure; stress response; rice yield; stress response; alternative splicing; fine‐tuning regulation; long noncoding RNA; LRK gene cluster; molecular polymorphism breeding; LAIR
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16882

SUMMARY The diversity in alternative splicing of long noncoding RNAs (lncRNAs) poses a challenge for functional annotation of lncRNAs. Moreover, little is known on the effects of alternatively spliced lncRNAs on crop yield. In this study, we cloned nine isoforms resulting from the alternative splicing of the lncRNA LAIR in rice. The LAIR isoforms are generated via alternative 5′/3′ splice sites and different combinations of specific introns. All LAIR isoforms activate the expression of the neighboring LRK1 gene and enhance yield‐related rice traits. In addition, there are slight differences in the binding ability of LAIR isoforms to the epigenetic modification‐related proteins OsMOF and OsWDR5, which affect the enrichment of H4K16ac and H3K4me3 at the LRK1 locus, and consequently fine‐tune the regulation of LRK1 expression and yield‐related traits. These differences in binding may be caused by polymorphic changes to the RNA secondary structure resulting from alternative splicing. It was also observed that the composition of LAIR isoforms was sensitive to abiotic stress. These findings suggest that the alternative splicing of LAIR leads to the formation of a functional transcript population that precisely regulates yield‐related gene expression, which may be relevant for phenotypic polymorphism‐based crop breeding under changing environmental conditions. Significance Statement Alternative splicing of lncRNA provides an important opportunity to understand the involvement of diversifies transcripts for gene precise regulatory. This study reveals the alternatively spliced LAIR isoforms leads to the formation of a dynamic functional scaffold transcript population that fine‐tune regulation of yield‐related gene expression, and shows potential for lncRNA alternative splicing application in crop phenotypic polymorphism breeding under changing environmental conditions.