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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 the Arabidopsis thaliana ecotypes 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. AT4G13495 encodes 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 using nrpd1 as the maternal parent than in the reciprocal cross. In spite of limited ecotypes tested, these results suggest potential roles of imprinting and NRPD1-mediated small RNA pathway in seed size variation in hybrids.

SUBMITTER: June V

PROVIDER: S-EPMC10516054 | biostudies-literature | 2023 Sep

REPOSITORIES: biostudies-literature

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Imprinting but not cytonuclear interactions affects parent-of-origin effect on seed size in <i>Arabidopsis</i> hybrids.

June Viviana V Song Xiaoya X Jeffrey Chen Z Z

bioRxiv : the preprint server for biology 20230917

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 the <i>Arabidopsis thaliana</i> ecotypes 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 cytopla ...[more]

PMID: 37745544

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Project description:Dormancy and germination vigor are complex traits of primary importance for adaptation and agriculture. Intraspecific variation in cytoplasmic genomes and cytonuclear interactions were previously reported to affect germination in Arabidopsis using novel cytonuclear combinations that disrupt co-adaptation between natural variants of nuclear and cytoplasmic genomes. However, specific aspects of dormancy and germination vigor were not thoroughly explored, nor the parental contributions to the genetic effects. Here, we specifically assessed dormancy, germination performance and longevity of seeds from Arabidopsis plants with natural and new genomic compositions. All three traits were modified by cytonuclear reshuffling. Both depth and release rate of dormancy could be modified by a changing of cytoplasm. Significant changes on dormancy and germination performance due to specific cytonuclear interacting combinations mainly occurred in opposite directions, consistent with the idea that a single physiological consequence of the new genetic combination affected both traits oppositely. However, this was not always the case. Interestingly, the ability of parental accessions to contribute to significant cytonuclear interactions modifying the germination phenotype was different depending on whether they provided the nuclear or cytoplasmic genetic compartment. The observed deleterious effects of novel cytonuclear combinations (in comparison with the nuclear parent) were consistent with a contribution of cytonuclear interactions to germination adaptive phenotypes. More surprisingly, we also observed favorable effects of novel cytonuclear combinations, suggesting suboptimal genetic combinations exist in natural populations for these traits. Reduced sensitivity to exogenous ABA and faster endogenous ABA decay during germination were observed in a novel cytonuclear combination that also exhibited enhanced longevity and better germination performance, compared to its natural nuclear parent. Taken together, our results strongly support that cytoplasmic genomes represent an additional resource of natural variation for breeding seed vigor traits.

Dataset Information

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

Publications

Imprinting but not cytonuclear interactions affects parent-of-origin effect on seed size in <i>Arabidopsis</i> hybrids.

Similar Datasets

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