Comprehensive analysis of the mitochondrial genome of Populus tomentosa ‘GM107’ and the dynamic expression of mitochondrial ATP synthase genes

Populus exhibits an extensive ecogeographical distribution throughout the Northern Hemisphere, characterized by abundant interspecific hybrids. Specifically, P. tomentosa stands as a keystone tree species within the eastern Asian region, playing versatile and significant roles in forestry production, ecological engineering, and evolutionary research. Although reference mitochondrial genomes are available for multiple Populus species, our goal was to elucidate a high-fidelity mitochondrial genome for P. tomentosa ‘GM107’, which would serve as a foundational reference for investigations into maternal lineage and evolutionary analyses. Here, we present a high-quality genome assembly for P. tomentosa ‘GM107’. The mitochondrial genome is 849,808 bp in size, organized into two circular chromosomes with lengths of 790,710 bp (Mt86) and 59,098 bp (Mt85), containing total 76 genes consisting 50 protein-coding genes (PCGs), 23 tRNA genes, and 3 rRNA genes. Repeat sequences, RNA editing, horizontal gene transfer, and codon usage of the PCGs were identified. Phylogenetic analysis indicates that P. alba var. Pyramidalis, P. alba and P. adenopoda involved the complex origin and evolution of P. tomentosa. The transcriptomic profiling of root, stem, leaf, and petiole derived from P. tomentosa GM15, P. tomentosa ‘GM107’, P. tricocarpa and P. alba var. pyramidalis was unveiled through high-throughput RNA sequencing, and their mitochondrial gene expression levels were found to be similar and highly conserved. Specifically, we also investigated the spatiotemporal expression dynamics of ATP synthetase family, as well as the expression patterns of select genes (e.g., Atp1, Atp4, Atp6, Atp8, Atp9) implicated in early leaf development, maturation, and senescence in P. tomentosa ‘GM107’. The expression dynamics of the mitochondrial Atp genes were observed to undergo alterations in correlation with the aging process, with a notable decline in expression levels as senescence progresses. The findings contribute to a deeper understanding of parental origin and evolutionary underpinnings of P. tomentosa. Additionally, our findings provide a reference framework for future investigations into the intricate regulatory mechanisms that govern senescence in poplar species.