Low-frequency somatic mutations are heritable in plants

The Weismann theory (1) states that hereditary traits are transmitted exclusively from the germline. The theory is valid in many animals (15) where germline cells are set aside early in development (1). In plants, germline segregation is generally assumed to occur late in development (2,4,10), which leads to several predictions on the fate of mutations occurring in plant tissues: mutations have generally low frequency in plant tissues (8); mutations at high frequency have a higher chance of transmission; branching topology of the tree dictates mutation distribution (9); and, exposure to UV radiation increases mutagenesis (18). We produced new genomes for two tropical tree species from the Amazon rainforest and resequenced 60 tissue samples to identify 18,274 unique mutations, almost all at low tissue frequency. We show that: 1) low-frequency mutations are transmitted to the next generation; 2) mutation phylogenies deviate from the branching topology of the tree; and 3) mutation rates and mutation spectra are not demonstrably affected by differences in UV exposure. Altogether, our results suggest far more complex links between plant growth, ageing, UV exposure, and mutation rates than commonly thought.