Abstract

Cytoplasmic male sterility (CMS), encoded by the interacting mitochondrial and nuclear genes, causes pollen abortion or non-viability. CMS is widely used in agriculture and extensively studied in crops. Much less is known about CMS in wild species. We performed a comparative transcriptomic analysis of male sterile and fertile individuals of Silene vulgaris, a model plant for the study of gynodioecy, to reveal the genes responsible for pollen abortion in this species. We used RNA-seq datasets previously employed for the analysis of mitochondrial and plastid transcriptomes of female and hermaphrodite flower buds, making it possible to compare the transcriptomes derived from three genomes in the same RNA specimen. We assembled de novo transcriptomes for two haplotypes of S. vulgaris and identified differentially expressed genes between the females and hermaphrodites, associated with stress response or pollen development. The gene for alternative oxidase was downregulated in females. The genetic pathways controlling CMS in S. vulgaris are similar to those in crops. The high number of the differentially expressed nuclear genes contrasts with the uniformity of organellar transcriptomes across genders, which suggests these pathways are evolutionarily conserved and that selective mechanisms may shield organellar transcription against changes in the cytoplasmic transcriptome.

Highlights

  • Cytoplasmic male sterility (CMS) is a special case of mitochondrial–nuclear interaction in flowering plants, leading to the inability to produce viable pollen [1,2]

  • We revealed numerous nuclear-encoded differentially expressed (DE) genes between F and H flower buds of the gynodioecious species S. vulgaris

  • Our findings contrast with near-zero differences in gene expression in mitochondria or plastids of S. vulgaris, when estimated in the same RNA samples, suggesting the existence of a mechanism shielding organellar transcription against the changes in the cytoplasmic transcriptome

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Summary

Introduction

Cytoplasmic male sterility (CMS) is a special case of mitochondrial–nuclear interaction in flowering plants, leading to the inability to produce viable pollen [1,2]. CMS genes are often chimeric, composed of several pieces of other mitochondrial genes. Their expression is influenced by nuclear factors (Rf), capable of restoring male fertility [3]. Plant individuals not producing pollen develop a female (F) gender, and those with restored male fertility become hermaphrodites (H). These two genders—females and hermaphrodites—constitute the basis of the plant breeding system gynodioecy [4], the second most widespread angiosperm reproduction system after hermaphroditism [5,6]

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