Cell-to-cell movement of mitochondria in plants

Abstract

We report cell-to-cell movement of mitochondria through a graft junction. Mitochondrial movement was discovered in an experiment designed to select for chloroplast transfer from Nicotiana sylvestris into Nicotiana tabacum cells. The alloplasmic N. tabacum line we used carries Nicotiana undulata cytoplasmic genomes, and its flowers are male sterile due to the foreign mitochondrial genome. Thus, rare mitochondrial DNA transfer from N. sylvestris to N. tabacum could be recognized by restoration of fertile flower anatomy. Analyses of the mitochondrial genomes revealed extensive recombination, tentatively linking male sterility to orf293, a mitochondrial gene causing homeotic conversion of anthers into petals. Demonstrating cell-to-cell movement of mitochondria reconstructs the evolutionary process of horizontal mitochondrial DNA transfer and enables modification of the mitochondrial genome by DNA transmitted from a sexually incompatible species. Conversion of anthers into petals is a visual marker that can be useful for mitochondrial transformation.

Plant grafting: insights into tissue regeneration

“…Another possible explanation for these phenomena is cell fusion since during fusions of plant cells lacking cell walls (called protoplasts) the cytoplasms often segregate non‐randomly (Evans, ). In cell fusions between two varieties of Nicotiana , chloroplasts are present only from one parent but mitochondria recombine with each other (Belliard & Pelletier, ) similar to what has been reported at the graft junction (Gurdon et al., ). Protoplast‐like protrusions form at the graft junction (Jeffree & Yeoman, ; Melnyk et al., ) and it is possible that cells from the graft parents fuse together at the graft junction.…”

“…Plasmodesmata can form between grafts of unrelated species (Kollmann & Glockmann, ) and might be important for promoting graft formation (Jeffree & Yeoman, ). Recent reports revealed that genetic material including nuclear, mitochondrial, and chloroplast genomes combine from the rootstock and scion at the graft junction to generate cells with genomes from both graft parents (Stegemann & Bock, ; Stegemann, Keuthe, Greiner, & Bock, ; Thyssen, Svab, & Maliga, ; Fuentes, Stegemann, Golczyk, Karcher, & Bock, ; Gurdon, Svab, Feng, Kumar, & Maliga, ). Fuentes et al.…”

Fission and Fusion of Plant Mitochondria, and Genome Maintenance

“…The mitochondrial genome of a cybrid between two plants in the nightshade family (tobacco and henbane [Hyoscyamus niger]) had more than 35 regions of recombination between homologous sequences, ranging from 100 to 9,000 bp (Sanchez-Puerta et al, 2015). Recombination and coexistence of the mitochondrial genes from different species also were observed in (1) plants generated from the junction of grafted tissues (Fuentes et al, 2014;Gurdon et al, 2016), (2) parasitic plants whose mitochondrial genomes contained some host plant fragments (Davis and Wurdack, 2004;Sanchez-Puerta et al, 2017), and even (3) host plants, in which fragments of parasitic plant mitochondrial genomes were observed in the host mitochondrial genomes (Mower et al, 2004). Furthermore, horizontal gene transfer between nonrelated plants is more frequently observed in mitochondrial genomes than in nuclear and plastid genomes (Bergthorsson et al, 2003).…”

Melatonin: A Mitochondrial Targeting Molecule Involving Mitochondrial Protection and Dynamics

“…For example, they still retain bacterial cyclic DNA. In addition, mitochondria and mitochondrial DNA can be horizontally transferred from cell to cell in mammalian cell culture systems and in plants [2,3,4]. There is, however, no definitive evidence to show whether this mitochondrial movement occurs in vivo in animals.…”