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Imprinting but not cytonuclear interactions affects parent-of-origin effect on seed size in Arabidopsis hybrids

ABSTRACT: The parent-of-origin effect on seed size can result from imprinting or a combinational effect between cytoplasmic and nuclear genomes, but their relative contributions remain unknown. To discern these confounding effects, we generated cytoplasmic-nuclear substitution (CNS) lines using recurrent backcrossing in theArabidopsis thalianaecotypes Col-0 and C24. These CNS lines differ only in the nuclear genome (imprinting) or in the cytoplasm. The CNS reciprocal hybrids with the same cytoplasm display a ∼20% seed size difference as observed in the conventional hybrids. However, seed size is similar between the reciprocal cybrids with fixed imprinting. Transcriptome analyses in the endosperm of CNS hybrids using laser-capture microdissection have identified 104 maternally expressed genes (MEGs) and 90 paternally-expressed genes (PEGs). These imprinted genes are involved in pectin catabolism and cell wall modification in the endosperm.HDG9, an epiallele and one of 11 cross-specific imprinted genes, controls seed size. In the embryo, a handful of imprinted genes is found in the CNS hybrids but only one is expressed higher in the embryo than endosperm.AT4G13495encodes a long-noncoding RNA (lncRNA), but no obvious seed phenotype is observed in the lncRNA knockout lines.NRPD1, encoding the largest subunit of RNA Pol IV, is involved in the biogenesis of small interfering RNAs. Seed size and embryo is larger in the cross usingnrpd1as the maternal parent than in the reciprocal cross. In spite of limited ecotypes tested, these results suggest potential roles of imprinting andNRPD1-mediated small RNA pathway in seed size variation in hybrids.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE249562 | GEO | 2024/06/05

REPOSITORIES: GEO

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Project description:In plants, imprinted gene expression occurs in endosperm seed tissue and can be associated with differential DNA methylation between maternal and paternal alleles. Imprinting is theorized to have been selected for because of conflict between parental genomes in offspring, but most studies of imprinting have been conducted in Arabidopsis thaliana, an inbred primarily self-fertilizing species that should have limited parental conflict. We examined embryo and endosperm allele-specific expression and DNA methylation genome-wide in the wild outcrossing species Arabidopsis lyrata. Here we show that the majority of A. lyrata imprinted genes exhibit parentally-biased expression in A. thaliana, suggesting that there is evolutionary conservation in gene imprinting. Surprisingly, we discovered substantial interspecies differences in methylation features associated with paternally expressed imprinted genes (PEGs). Unlike A. thaliana, the maternal allele of many A. lyrata PEGs was hypermethylated in the CHG context. Increased maternal allele CHG methylation was associated with increased expression bias in favor of the paternal allele. We propose that CHG methylation maintains or reinforces repression of maternal alleles of PEGs. These data suggest that while the genes subject to imprinting are largely conserved, there is flexibility in the epigenetic mechanisms employed between closely related species to maintain monoallelic expression. This supports the idea that imprinting of specific genes is a functional phenomenon, and not simply a byproduct of seed epigenomic reprogramming. Examination of total gene expression, parent-of-origin specific allelic bias, or DNA methylation in embryo, endosperm, flower bud or seedcoat tissue from Arabidopsis lyrata accessions MN47 (MN), Karhumaki (Kar or KA), and crosses between them. High-throughput Illumina poly-A-selected mRNA-seq was used to identify imprinted genes in A. lyrata, and high-throughput Illumina whole genome bisulfite-sequencing was used to examine DNA methylation. mRNA-seq samples are designated MMxFF_T# where MM is the mother of the cross (either MN for MN47 or KA for Kar), FF is the father, T is the tissue (E for embryo, N for endosperm, S for seedcoat, b for buds), and # is the replicate numbers. Samples obtained from bisulfite sequencing follow the same naming but have suffix _BS and indicate cytosine methylation context (CpG, CHG, or CHH). For KAxMN bisulfite sequencing, additional files MMxFF_T#_BS_P_C.txt follow the same naming scheme but contain context-specific methylation data (C) from reads that mapped preferentially to one parent strain (P).