Abstract

The spontaneously emerging rogue phenotype in peas (Pisum sativum L.), characterized by narrow and pointed leaf stipula and leaflets, was the first identified case of the epigenetic phenomenon paramutation. The crosses of homozygous or heterozygous (e.g., F1) rogue plants with non-rogue (wild type) plants, produce exclusively rogue plants in the first and all subsequent generations. The fact that the wild phenotype disappears forever, is in clear contradiction with the Mendelian rules of inheritance, a situation that impedes the positional cloning of genes involved in this epigenetic phenomenon. One way of overcoming this obstacle is the identification of plant genotypes harboring naturally occurring or artificially induced neutral alleles, non-sensitive to paramutation. So far, such alleles have never been described for the pea rogue paramutation. Here, we report the induction via 1-ethyl-1-nitrosourea (ENU) mutagenesis of a non-rogue revertant mutant in the rogue cv. Progreta, and the completely unusual fixation of the induced non-rogue phenotype through several generations. The reversion of the methylation status of two previously identified differentially methylated genomic sequences in the induced non-rogue mutant, confirms that the rogue paramutation is accompanied by alterations in DNA methylation. Nevertheless, unexpectedly, the induced non-rogue mutant showed to be still sensitive to paramutation.

Highlights

  • The spontaneous emergence of off-type rogue plants in peas (Pisum sativum L.), characterized by pointed leaflets and leaf stipula, and the non-Mendelian inheritance of this new phenotype, were described for the first time in the beginning of the last century by Bateson and Pellew [1,2] and soon after confirmed by Brotherton [3,4].The progeny of crosses between rogue and non-rogue plants is exclusively constituted by “rogues”, a result that would indicate the genetic dominance of the rogue phenotype over the wild phenotype

  • To the observed in maize, naturally occurring non-paramutable, neutral, alleles have never been reported in peas, a circumstance that hampers the use of the positional cloning or genetic association strategies for isolation of gene(s) involved in rogue paramutation

  • To induce non-paramutable alleles of genes required for the establishment and/or maintenance of the paramutation in pea, we have implemented a 1-ethyl-1-nitrosourea (ENU) mutagenesis program using the rogue cv

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Summary

Introduction

The progeny of crosses between rogue and non-rogue (wild) plants is exclusively constituted by “rogues”, a result that would indicate the genetic dominance of the rogue phenotype over the wild phenotype. In the F2, and subsequent generations, the wild phenotype is never recovered. The cross of F1 (rogue) plants with wild type plants produces uniquely rogue plants and, again, the wild phenotype is never recovered in the subsequent generations. The heterozygous plants behave as homozygous, which suggest that in the presence of the rogue allele the non-rogue allele is epigenetically converted into rogue. This epigenetic allele alteration was the first reported case of a relatively rare phenomenon, later designated as paramutation [5]

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