title: Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice.
abstract: Transposable elements (TEs) and repetitive sequences make up over 35% of the rice (Oryza sativa) genome. The host regulates the activity of different TEs by different epigenetic mechanisms, including DNA methylation, histone H3K9 methylation, and histone H3K4 demethylation. TEs can also affect the expression of host genes. For example, miniature inverted repeat TEs (MITEs), dispersed high copy-number DNA TEs, can influence the expression of nearby genes. In plants, 24-nt small interfering RNAs (siRNAs) are mainly derived from repeats and TEs. However, the extent to which TEs, particularly MITEs associated with 24-nt siRNAs, affect gene expression remains elusive. Here, we show that the rice Dicer-like 3 homolog OsDCL3a is primarily responsible for 24-nt siRNA processing. Impairing OsDCL3a expression by RNA interference caused phenotypes affecting important agricultural traits; these phenotypes include dwarfism, larger flag leaf angle, and fewer secondary branches. We used small RNA deep sequencing to identify 535,054 24-nt siRNA clusters. Of these clusters, ∼82% were OsDCL3a-dependent and showed significant enrichment of MITEs. Reduction of OsDCL3a function reduced the 24-nt siRNAs predominantly from MITEs and elevated expression of nearby genes. OsDCL3a directly targets genes involved in gibberellin and brassinosteroid homeostasis; OsDCL3a deficiency may affect these genes, thus causing the phenotypes of dwarfism and enlarged flag leaf angle. Our work identifies OsDCL3a-dependent 24-nt siRNAs derived from MITEs as broadly functioning regulators for fine-tuning gene expression, which may reflect a conserved epigenetic mechanism in higher plants with genomes rich in dispersed repeats or TEs.
authors.affiliation: State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
authors.forename: Liya
authors.initials: L
authors.lastname: Wei
authors.forename: Lianfeng
authors.initials: L
authors.lastname: Gu
authors.forename: Xianwei
authors.initials: X
authors.lastname: Song
authors.forename: Xiekui
authors.initials: X
authors.lastname: Cui
authors.forename: Zhike
authors.initials: Z
authors.lastname: Lu
authors.forename: Ming
authors.initials: M
authors.lastname: Zhou
authors.forename: Lulu
authors.initials: L
authors.lastname: Wang
authors.forename: Fengyi
authors.initials: F
authors.lastname: Hu
authors.forename: Jixian
authors.initials: J
authors.lastname: Zhai
authors.forename: Blake C
authors.initials: BC
authors.lastname: Meyers
authors.forename: Xiaofeng
authors.initials: X
authors.lastname: Cao
mesh_terms: D001483:Base Sequence; D060406:Brassinosteroids / Q000378:metabolism; D047369:Chromatin Immunoprecipitation; D017931:DNA Primers / Q000235:genetics; D004251:DNA Transposable Elements / Q000235:genetics; D018506:Gene Expression Regulation, Plant / Q000235:genetics*; D005875:Gibberellins / Q000378:metabolism; D059014:High-Throughput Nucleotide Sequencing; D055029:Inverted Repeat Sequences / Q000235:genetics; D008969:Molecular Sequence Data; D012275:Oryza / Q000235:genetics* / Q000254:growth & development; D034741:RNA, Small Interfering / Q000235:genetics* / Q000378:metabolism; D060888:Real-Time Polymerase Chain Reaction; D043244:Ribonuclease III / Q000235:genetics*; D017423:Sequence Analysis, RNA
chemical_list: D060406:Brassinosteroids; D017931:DNA Primers; D004251:DNA Transposable Elements; D005875:Gibberellins; D034741:RNA, Small Interfering; D043244:Ribonuclease III
keywords: plant architecture; plant hormone; transposon