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Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes.

ABSTRACT: MicroRNAs (miRNAs) are an extensive class of tiny RNA molecules that regulate the expression of target genes by means of complementary base pair interactions. Although the first miRNAs were discovered in Caenorhabditis elegans, >300 miRNAs were recently documented in animals and plants, both by cloning methods and computational predictions. We present a genome-wide computational approach to detect miRNA genes in the Arabidopsis thaliana genome. Our method is based on the conservation of short sequences between the genomes of Arabidopsis and rice (Oryza sativa) and on properties of the secondary structure of the miRNA precursor. The method was fine-tuned to take into account plant-specific properties, such as the variable length of the miRNA precursor sequences. In total, 91 potential miRNA genes were identified, of which 58 had at least one nearly perfect match with an Arabidopsis mRNA, constituting the potential targets of those miRNAs. In addition to already known transcription factors involved in plant development, the targets also comprised genes involved in several other cellular processes, such as sulfur assimilation and ubiquitin-dependent protein degradation. These findings considerably broaden the scope of miRNA functions in plants.

SUBMITTER: Bonnet E

PROVIDER: S-EPMC509231 | biostudies-literature | 2004 Aug

REPOSITORIES: biostudies-literature

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Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes.

Bonnet Eric E Wuyts Jan J Rouzé Pierre P Van de Peer Yves Y

Proceedings of the National Academy of Sciences of the United States of America 20040722 31

MicroRNAs (miRNAs) are an extensive class of tiny RNA molecules that regulate the expression of target genes by means of complementary base pair interactions. Although the first miRNAs were discovered in Caenorhabditis elegans, >300 miRNAs were recently documented in animals and plants, both by cloning methods and computational predictions. We present a genome-wide computational approach to detect miRNA genes in the Arabidopsis thaliana genome. Our method is based on the conservation of short se ...[more]

PMID: 15272084

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Project description:BACKGROUND: Calcium signaling plays a prominent role in plants for coordinating a wide range of developmental processes and responses to environmental cues. Stimulus-specific generation of intracellular calcium transients, decoding of calcium signatures, and transformation of the signal into cellular responses are integral modules of the transduction process. Several hundred proteins with functions in calcium signaling circuits have been identified, and the number of downstream targets of calcium sensors is expected to increase. We previously identified a novel, calmodulin-binding nuclear protein, IQD1, which stimulates glucosinolate accumulation and plant defense in Arabidopsis thaliana. Here, we present a comparative genome-wide analysis of a new class of putative calmodulin target proteins in Arabidopsis and rice. RESULTS: We identified and analyzed 33 and 29 IQD1-like genes in Arabidopsis thaliana and Oryza sativa, respectively. The encoded IQD proteins contain a plant-specific domain of 67 conserved amino acid residues, referred to as the IQ67 domain, which is characterized by a unique and repetitive arrangement of three different calmodulin recruitment motifs, known as the IQ, 1-5-10, and 1-8-14 motifs. We demonstrated calmodulin binding for IQD20, the smallest IQD protein in Arabidopsis, which consists of a C-terminal IQ67 domain and a short N-terminal extension. A striking feature of IQD proteins is the high isoelectric point (approximately 10.3) and frequency of serine residues (approximately 11%). We compared the Arabidopsis and rice IQD gene families in terms of gene structure, chromosome location, predicted protein properties and motifs, phylogenetic relationships, and evolutionary history. The existence of an IQD-like gene in bryophytes suggests that IQD proteins are an ancient family of calmodulin-binding proteins and arose during the early evolution of land plants. CONCLUSION: Comparative phylogenetic analyses indicate that the major IQD gene lineages originated before the monocot-eudicot divergence. The extant IQD loci in Arabidopsis primarily resulted from segmental duplication and reflect preferential retention of paralogous genes, which is characteristic for proteins with regulatory functions. Interaction of IQD1 and IQD20 with calmodulin and the presence of predicted calmodulin binding sites in all IQD family members suggest that IQD proteins are a new class of calmodulin targets. The basic isoelectric point of IQD proteins and their frequently predicted nuclear localization suggest that IQD proteins link calcium signaling pathways to the regulation of gene expression. Our comparative genomics analysis of IQD genes and encoded proteins in two model plant species provides the first step towards the functional dissection of this emerging family of putative calmodulin targets.

Project description:BackgroundArabidopsis thaliana is clearly established as the model plant species. Given the ever-growing demand for food, there is a need to translate the knowledge learned in Arabidopsis to agronomically important species, such as rice (Oryza sativa). To gain a comparative insight into the similarities and differences into how organs are built and how plants respond to stress, the transcriptomes of Arabidopsis and rice were compared at the level of gene orthology and functional categorisation.ResultsOrgan specific transcripts in rice and Arabidopsis display less overlap in terms of gene orthology compared to the orthology observed between both genomes. Although greater overlap in terms of functional classification was observed between root specific transcripts in rice and Arabidopsis, this did not extend to flower, leaf or seed specific transcripts. In contrast, the overall abiotic stress response transcriptome displayed a significantly greater overlap in terms of gene orthology compared to the orthology observed between both genomes. However, ~50% or less of these orthologues responded in a similar manner in both species. In fact, under cold and heat treatments as many or more orthologous genes responded in an opposite manner or were unchanged in one species compared to the other. Examples of transcripts that responded oppositely include several genes encoding proteins involved in stress and redox responses and non-symbiotic hemoglobins that play central roles in stress signalling pathways. The differences observed in the abiotic transcriptomes were mirrored in the presence of cis-acting regulatory elements in the promoter regions of stress responsive genes and the transcription factors that potentially bind these regulatory elements. Thus, both the abiotic transcriptome and its regulation differ between rice and Arabidopsis.ConclusionsThese results reveal significant divergence between Arabidopsis and rice, in terms of the abiotic stress response and its regulation. Both plants are shown to employ unique combinations of genes to achieve growth and stress responses. Comparison of these networks provides a more rational approach to translational studies that is based on the response observed in these two diverse plant models.

Dataset Information

Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes.

Publications

Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes.

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