Format: ORAL

Hanchen Wang1, Deyi Wang2, Bingyi Shao1, Xiaohua Jin1

1 State Key Laboratory of Plant Diversity and Specialty Crops, Institute of Botany, Chinese Academy of Sciences, Beijing, China 2 Naturalis Biodiversity Center, Leiden, the Netherlands

The evolution of heterotrophy in plants has induced dramatic genomic alternations, such as for plastids, where extensive gene loss and size reduction are widely reported. Analogous to plastids are several extreme modifications discovered in mitochondrial genomes (mitogenomes) of parasitic plants. However, whether trophic reliance on symbiotic fungi (mycoheterotrophy) similarly results in mitogenomic alternations remains largely unknown. We present a comprehensive mitogenomic study for mycoheterotrophic plants based on 11 de novo assemblies of Gastrodia (Orchidaceae). These mitogenomes contain multiple chromosomes, range from 0.56 to 2.1 Mb in size, and exhibit several features are rarely, if ever, observed among other plants. Specifically, variations in chromosome copy number are universal, and in two assemblies, a chromosome exists at approximately 15 times higher abundance than the conspecific average, resulting in the most extreme chromosomal copy number variation among any mitogenomes so far. Insertions from plastid and fungal genomes are unexpectedly scant, in contrast to those potentially rampant, species-specific, non-coding sequences transferred from the nucleus and distant plant taxa. Yet, despite the 3.8-fold size variation and highly variable intergenic sequence components, these mitogenomes harbor an ordinary complement of genes and introns, and exhibit moderate substitution rates of coding sequences, with no genes acquired via horizontal transfer. Taken together, our findings suggest a minor role of mycoheterotrophic lifestyle on mitochondrial coding sequences, but the extreme copy number variation across mitochondrial chromosomes and unusual combinations of transferred sequences set new benchmarks for architectural and content variation seen in plant mitogenomes, and hints at unexplored mechanisms governing mitogenomic evolution of these extraordinary heterotrophic plants.