An official website of the United States government
ABSTRACT Long noncoding RNA (lncRNA) plays important roles in sexual development in eukaryotes. In filamentous fungi, however, little is known about the expression and roles of lncRNAs during fruiting body formation. By profiling developmental transcriptomes during the life cycle of the plant-pathogenic fungus Fusarium graminearum , we identified 547 lncRNAs whose expression was highly dynamic, with about 40% peaking at the meiotic stage. Many lncRNAs were found to be antisense to mRNAs, forming 300 sense-antisense pairs. Although small RNAs were produced from these overlapping loci, antisense lncRNAs appeared not to be involved in gene silencing pathways. Genome-wide analysis of small RNA clusters identified many silenced loci at the meiotic stage. However, we found transcriptionally active small RNA clusters, many of which were associated with lncRNAs. Also, we observed that many antisense lncRNAs and their respective sense transcripts were induced in parallel as the fruiting bodies matured. The nonsense-mediated decay (NMD) pathway is known to determine the fates of lncRNAs as well as mRNAs. Thus, we analyzed mutants defective in NMD and identified a subset of lncRNAs that were induced during sexual development but suppressed by NMD during vegetative growth. These results highlight the developmental stage-specific nature and functional potential of lncRNA expression in shaping the fungal fruiting bodies and provide fundamental resources for studying sexual stage-induced lncRNAs. IMPORTANCE Fusarium graminearum is the causal agent of the head blight on our major staple crops, wheat and corn. The fruiting body formation on the host plants is indispensable for the disease cycle and epidemics. Long noncoding RNA (lncRNA) molecules are emerging as key regulatory components for sexual development in animals and plants. To date, however, there is a paucity of information on the roles of lncRNAs in fungal fruiting body formation. Here we characterized hundreds of lncRNAs that exhibited developmental stage-specific expression patterns during fruiting body formation. Also, we discovered that many lncRNAs were induced in parallel with their overlapping transcripts on the opposite DNA strand during sexual development. Finally, we found a subset of lncRNAs that were regulated by an RNA surveillance system during vegetative growth. This research provides fundamental genomic resources that will spur further investigations on lncRNAs that may play important roles in shaping fungal fruiting bodies.
more »
« less
LncRNA FLAIL affects alternative splicing and represses flowering in Arabidopsis
Abstract How the noncoding genome affects cellular functions is a key biological question. A particular challenge is to distinguish the effects of noncoding DNA elements from long noncoding RNAs (lncRNAs) that coincide at the same loci. Here, we identified the flowering‐associated intergenic lncRNA (FLAIL) inArabidopsisthrough early floweringflailmutants. Expression ofFLAILRNA from a different chromosomal location in combination with strand‐specific RNA knockdown characterizedFLAILas a trans‐acting RNA molecule.FLAILdirectly binds to differentially expressed target genes that control flowering via RNA–DNA interactions through conserved sequence motifs.FLAILinteracts with protein and RNA components of the spliceosome to affect target mRNA expression through co‐transcriptional alternative splicing (AS) and linked chromatin regulation. In the absence ofFLAIL, splicing defects at the direct FLAIL target flowering gene LACCASE 8 (LAC8) correlated with reduced mRNA expression. Double mutant analyses support a model whereFLAIL‐mediated splicing of LAC8 promotes its mRNA expression and represses flowering. Our study suggests lncRNAs as accessory components of the spliceosome that regulate AS and gene expression to impact organismal development.
more »
« less
- Award ID(s):
- 2023310
- PAR ID:
- 10413290
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- The EMBO Journal
- Volume:
- 42
- Issue:
- 11
- ISSN:
- 0261-4189
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Summary Evolutionarily conserved DEK domain‐containing proteins have been implicated in multiple chromatin‐related processes, mRNA splicing and transcriptional regulation in eukaryotes.Here, we show that two DEK proteins, DEK3 and DEK4, control the floral transition inArabidopsis. DEK3 and DEK4 directly associate with chromatin of related flowering repressors,FLOWERING LOCUS C(FLC), and its two homologs,MADS AFFECTING FLOWERING4(MAF4) andMAF5, to promote their expression.The binding of DEK3 and DEK4 to a histone octamerin vivoaffects histone modifications atFLC,MAF4andMAF5loci. In addition, DEK3 and DEK4 interact with RNA polymerase II and promote the association of RNA polymerase II withFLC,MAF4andMAF5chromatin to promote their expression.Our results show that DEK3 and DEK4 directly interact with chromatin to facilitate the transcription of key flowering repressors and thus prevent precocious flowering inArabidopsis.more » « less
-
Light signals perceived by a group of photoreceptors have profound effects on the physiology, growth, and development of plants. The red/far-red light–absorbing phytochromes (phys) modulate these aspects by intricately regulating gene expression at multiple levels. Here, we report the identification and functional characterization of an RNA-binding splicing factor, SWAP1 (SUPPRESSOR-OF-WHITE-APRICOT/SURP RNA-BINDING DOMAIN-CONTAINING PROTEIN1). Loss-of-function swap1-1 mutant is hyposensitive to red light and exhibits a day length–independent early flowering phenotype. SWAP1 physically interacts with two other splicing factors, (SFPS) SPLICING FACTOR FOR PHYTOCHROME SIGNALING and (RRC1) REDUCED RED LIGHT RESPONSES IN CRY1CRY2 BACKGROUND 1 in a light-independent manner and forms a ternary complex. In addition, SWAP1 physically interacts with photoactivated phyB and colocalizes with nuclear phyB photobodies. Phenotypic analyses show that the swap1sfps , swap1rrc1, and sfpsrrc1 double mutants display hypocotyl lengths similar to that of the respective single mutants under red light, suggesting that they function in the same genetic pathway. The swap1sfps double and swap1sfpsrrc1 triple mutants display pleiotropic phenotypes, including sterility at the adult stage. Deep RNA sequencing (RNA-seq) analyses show that SWAP1 regulates the gene expression and pre–messenger RNA (mRNA) alternative splicing of a large number of genes, including those involved in plant responses to light signaling. A comparative analysis of alternative splicing among single, double, and triple mutants showed that all three splicing factors coordinately regulate the alternative splicing of a subset of genes. Our study uncovered the function of a splicing factor that modulates light-regulated alternative splicing by interacting with photoactivated phyB and other splicing factors.more » « less
-
Long noncoding RNAs (lncRNAs) are transcribed elements increasingly recognized for their roles in regulating gene expression. Thus far, however, we have little understanding of how lncRNAs contribute to evolution and adaptation. Here, we show that a conserved lncRNA,ivory, is an important color patterning gene in the buckeye butterflyJunonia coenia.ivoryoverlaps withcortex, a locus linked to multiple cases of crypsis and mimicry in Lepidoptera. Along with a companion paper by Livraghi et al., we argue thativory, notcortex, is the color pattern gene of interest at this locus. InJ. coenia, a cluster ofcis-regulatory elements (CREs) in the first intron ofivoryare genetically associated with natural variation in seasonal color pattern plasticity, and targeted deletions of these CREs phenocopy seasonal phenotypes. Deletions of differentivoryCREs produce other distinct phenotypes as well, including loss of melanic eyespot rings, and positive and negative changes in overall wing pigmentation. We show that the color pattern transcription factors Spineless, Bric-a-brac, and Ftz-f1 bind to theivorypromoter during wing pattern development, suggesting that they directly regulateivory. This case study demonstrates howcis-regulation of a single noncoding RNA can exert diverse and nuanced effects on the evolution and development of color patterns, including modulating seasonally plastic color patterns.more » « less
-
Light is one of the most important factors regulating plant gene expression patterns, metabolism, physiology, growth, and development. To explore how light may induce or alter transcript splicing, we conducted RNA-Seq-based transcriptome analyses by comparing the samples harvested as etiolated seedlings grown under continuous dark conditions vs. the light-treated green seedlings. The study aims to reveal differentially regulated protein-coding genes and novel long noncoding RNAs (lncRNAs), their light-induced alternative splicing, and their association with biological pathways. We identified 14,766 differentially expressed genes, of which 4369 genes showed alternative splicing. We observed that genes mapped to the plastid-localized methyl-erythritol-phosphate (MEP) pathway were light-upregulated compared to the cytosolic mevalonate (MVA) pathway genes. Many of these genes also undergo splicing. These pathways provide crucial metabolite precursors for the biosynthesis of secondary metabolic compounds needed for chloroplast biogenesis, the establishment of a successful photosynthetic apparatus, and photomorphogenesis. In the chromosome-wide survey of the light-induced transcriptome, we observed intron retention as the most predominant splicing event. In addition, we identified 1709 novel lncRNA transcripts in our transcriptome data. This study provides insights on light-regulated gene expression and alternative splicing in rice.more » « less
