Organelle genome assembly uncovers the dynamic genome reorganization and cytoplasmic male sterility associated genes in tomato

Abstract

To identify cytoplasmic male sterility (CMS)-associated genes in tomato, we determined the genome sequences of mitochondria and chloroplasts in three CMS tomato lines derived from independent asymmetric cell fusions, their nuclear and cytoplasmic donors, and male fertile weedy cultivated tomato and wild relatives. The structures of the CMS mitochondrial genomes were highly divergent from those of the nuclear and cytoplasmic donors, and genes of the donors were mixed up in these genomes. On the other hand, the structures of CMS chloroplast genomes were moderately conserved across the donors, but CMS chloroplast genes were unexpectedly likely derived from the nuclear donors. Comparative analysis of the structures and contents of organelle genes and transcriptome analysis identified three genes that were uniquely present in the CMS lines, but not in the donor or fertile lines. RNA-sequencing analysis indicated that these three genes transcriptionally expressed in anther, and identified different RNA editing levels in one gene, orf265, that was partially similar to ATP synthase subunit 8, between fertile and sterile lines. The orf265 was a highly potential candidate for CMS-associated gene. This study suggests that organelle reorganization mechanisms after cell fusion events differ between mitochondria and chloroplasts, and provides insight into the development of new F1 hybrid breeding programs employing the CMS system in tomato.

Comparison of Mitochondrial Genomes between a Cytoplasmic Male-Sterile Line and Its Restorer Line for Identifying Candidate CMS Genes in Gossypium hirsutum

“…The mtDNA sequences of SI3A and 0-613-2R were nearly identical to those of the 2074A and 2074S G. hirsutum CMS lines for which mitochondrial genomes were previously reported [ 27 ]. The differences in mitochondrial genome size between CMS and restorer lines may be caused by unique sequences, as has been observed in tomato and wheat [ 32 , 42 ]. Here, unique sequences in SI3Amt2 (21.3 kb) and SI3Amt3 (1.1 kb) were the main factors leading to the size difference between SI3A and 0-613-2R.…”