Twenty-four-nt small interfering RNAs (siRNAs) maintain asymmetric DNA methylation at thousands of euchromatic transposable elements in plant genomes in a process called RNA-directed DNA methylation (RdDM). RdDM is dispensable for growth and development in Arabidopsis thaliana, but is required for reproduction in other plants, such as Brassica rapa. The 24-nt siRNAs are abundant in maternal reproductive tissue, due largely to overwhelming expression from a few loci in the ovule and developing seed coat, termed siren loci. A recent study showed that 24-nt siRNAs produced in the anther tapetal tissue can methylate male meiocyte genes in trans. Here we show that in B. rapa, a similar process takes place in female tissue. siRNAs are produced from gene fragments embedded in some siren loci, and these siRNAs can trigger methylation in trans at related protein-coding genes. This trans-methylation is associated with silencing of some target genes and may be responsible for seed abortion in RdDM mutants. Furthermore, we demonstrate that a consensus sequence in at least two families of DNA transposons is associated with abundant siren expression, most likely through recruitment of CLASSY3, a putative chromatin remodeller. This research describes a mechanism whereby RdDM influences gene expression and sheds light on the role of RdDM during plant reproduction.
Reproductive tissues are a rich source of small RNAs, including several classes of short interfering (si)RNAs that are restricted to this stage of development. In addition to Pol IV-dependent 24-nt siRNAs that trigger canonical RNA-directed DNA methylation (RdDM), abundant reproductive-specific siRNAs are produced from companion cells adjacent to the developing germ line or zygote and may move intercellularly before inducing methylation. In some cases, these siRNAs are produced via non-canonical biosynthesis mechanisms or from sequences with little similarity to transposons. While the precise role of these siRNAs and the methylation they trigger is unclear, they have been implicated in specifying a single megaspore mother cell, silencing transposons in the male germ line, mediating parental dosage conflict to ensure proper endosperm development, hypermethylation of mature embryos, and trans-chromosomal methylation in hybrids. In this review, we summarize the current knowledge of reproductive siRNAs, including their biosynthesis, transport, and function.
24-nt small interfering siRNAs maintain asymmetric DNA methylation at thousands of euchromatic transposable elements in plant genomes in a process call RNA-directed DNA Methylation (RdDM). Although this methylation occasionally causes transcriptional silencing of nearby protein-coding genes, direct targeting of methylation at coding sequences is rare. RdDM is dispensable for growth and development in Arabidopsis, but is required for reproduction in other plant species, such as Brassica rapa. 24-nt siRNAs are particularly abundant in reproductive tissue, due largely to overwhelming expression from a small number of loci in the ovule and developing seed coat, termed siren loci. Here we show that siRNAs are often produced from gene fragments embedded in siren loci, and that these siRNAs can trigger methylation in trans at related protein-coding genes. This trans-methylation is associated with transcriptional silencing of target genes and may be responsible for seed abortion in RdDM mutants. Furthermore, we demonstrate that a consensus sequence in at least two families of DNA transposons is associated with abundant siren expression, most likely through recruitment of the CLSY3 putative chromatin remodeller. This research describes a new mechanism whereby RdDM influences gene expression and sheds light on the role of RdDM during plant reproduction.
Locules are the seed-bearing structure of fruits. Multiple locules are associated with increased fruit size and seed set, and therefore control of locule number is an important agronomic trait. Locule number is controlled in part by the CLAVATA-WUSCHEL pathway. Disruption of either the CLAVATA1 receptor-like kinase or its ligand CLAVATA3 can cause larger floral meristems and an increased number of locules. In an EMS mutagenized population of Brassica rapa, we identified a mutant allele that raises the number of locules from 4 to a range of from 6 to 8. Linkage mapping and genetic analysis support that the mutant phenotype is due to a missense mutation in a CLAVATA 1 (CLV1) homolog. In addition to increased locule number, brclv1 individuals fail to terminate their floral meristems, resulting in internal gynoecia that negatively impact seed production.
Locules are the seed‐bearing structure of fruits. Multiple locules are associated with increased fruit size and seed set, and therefore, control of locule number is an important agronomic trait. Locule number is controlled in part by the CLAVATA‐WUSCHEL pathway. Disruption of either the CLAVATA1 receptor‐like kinase or its ligand CLAVATA3 can cause larger floral meristems and an increased number of locules. In an EMS mutagenized population of Brassica rapa , we identified a mutant allele that raises the number of locules from four to a range of from six to eight. Linkage mapping and genetic analysis support that the mutant phenotype is due to a missense mutation in a CLAVATA 1 ( CLV1 ) homolog. In addition to increased locule number, additional internal gynoecia are formed in brclv1 individuals, suggesting a failure to terminate floral meristem development, which results in decreased seed production.
In plants, de novo DNA methylation is guided by 24-nt short interfering (si)RNAs in a process called RNA-directed DNA methylation (RdDM). Primarily targeted at transposons, RdDM causes transcriptional silencing and can indirectly influence expression of neighboring genes. During reproduction, a small number of siRNA loci are dramatically upregulation in the maternally-derived seed coat, suggesting that RdDM might have a special function during reproduction. However, the developmental consequence of RdDM has been difficult to dissect because disruption of RdDM does not result in overt phenotypes in Arabidopsis thaliana, where the pathway has been most thoroughly studied. In contrast, Brassica rapa mutants lacking RdDM have a severe seed production defect, which is determined by the maternal sporophytic genotype. To explore the factors that underlie the different phenotypes of these closely-related species, we produced RdDM mutations in three additional members of the Brassicaceae family: Camelina sativa, Capsella rubella, and Capsella grandiflora. Among these three species, only mutations in Capsella grandiflora displayed a seed production defect similar to Brassica rapa mutants, suggesting that mating system is a key determinant for reproductive phenotypes in RdDM mutants.
Petal color is an important trait for both ornamental purposes and also for attracting pollinators. Here, we report a mutation ofBrassica rapaR-o-18 with pale yellow petals that we retrieved from an EMS population and namedwhiter shade of pale(wsp). Phenotypic segregation ratio of an F2 mapping population indicates the phenotype is controlled by a single recessive gene. Mapping data from the whole genome sequencing coupled with allele frequency analysis suggests the mutation is located in a ∼2 Mbp interval on chromosome 2. The interval contains a putative esterase/lipase/thioesterase protein previously demonstrated to account for floral color inB. rapa. We demonstrate thatwspcarries a G to A missense mutation causing an aspartate to asparagine substitution within the putative lysophospholipid acyltransferase domain.
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