A phylogenomic approach reveals a low somatic mutation rate in a long-lived plant

Abstract

Somatic mutations can have important effects on the life history, ecology, and evolution of plants, but the rate at which they accumulate is poorly understood and difficult to measure directly. Here, we develop a method to measure somatic mutations in individual plants and use it to estimate the somatic mutation rate in a large, long-lived, phenotypically mosaic Eucalyptus melliodora tree. Despite being 100 times larger than Arabidopsis, this tree has a per-generation mutation rate only ten times greater, which suggests that this species may have evolved mechanisms to reduce the mutation rate per unit of growth. This adds to a growing body of evidence that illuminates the correlated evolutionary shifts in mutation rate and life history in plants.

Lifetime genealogical divergence within plants leads to epigenetic mosaicism in the long-lived shrubLavandula latifolia(Lamiaceae)

“…Pairs of modules physically closer at tips of a tree are also historically and developmentally closer to their most recent common ancestor module than pairs of modules located farther away in the tree. These relationships, along with the regularly dichasial branching pattern that characterizes L. latifolia shrubs, justify our application of methods from phylogenetic research to assess genealogical signal and perform genealogical reconstructions of within-plant epigenetic changes (see also Orr et al ., 2020). These methods could be used for the same purpose on other woody perennials that follow Leeuwenberg’s model of architecture (see, e.g., Hamilton, 1985; Hallé, 1986; Navarro et al ., 2009; for tropical and non-tropical examples).…”

“…There is the advantageous difference that our genealogical trees are errorless pedigrees representing true relationships rather than uncertain inferential hypotheses as it usually happens with phylogenetic trees (Felsenstein, 2004). Methods borrowed from phylogenetic research were used to investigate the genealogical component of extant within-plant epigenetic mosaicism in L. latifolia shrubs (see Orr et al ., 2020, for a comparable approach). ‘Genealogical tree’, ‘genealogical character estimation’ and ‘genealogical signal’ will be used hereafter as the within-plant equivalents to ‘phylogenetic tree’, ‘ancestral character estimation’ and ‘phylogenetic signal’, respectively (Paradis, 2012; Münkemüller et al ., 2012).…”

“…Position in relation to external environmental gradients (light, air temperature) or internal developmental axes (nodal position on branches) are factors ordinarily contributing to within-plant variation in phenotypic traits (Herrera, 2009). Subindividual polymorphisms in chromosome number (aneusomaty; D’Amato, 1997) or the DNA sequence of nuclear (Wang et al ., 2019; Orr et al ., 2020) and plastid genomes (García et al ., 2004; Sun et al ., 2019) can also account for subindividual phenotypic heterogeneity (Whitham et al ., 1984). The phenotypic effects of these polymorphisms, however, have been investigated on few occasions.…”

“…The phenotypic effects of these polymorphisms, however, have been investigated on few occasions. Genetic heterogeneity caused by somatic mutations is unlikely to be a pervasive driver of within-plant heterogeneity in wild plants, given the paucity of well-documented genetic mosaics and the extremely low somatic mutation rates reported whenever such mosaics have been found (Padovan et al ., 2013; Ranade et al ., 2015; Schmid-Siegert et al ., 2017; Gerber, 2018; Wang et al ., 2019; Orr et al ., 2020). Somatic mutations altering nuclear or plastid DNA sequences are not, however, the only molecular mechanism with a capacity to produce genomic heterogeneity and induce phenotypic variation within individual plants.…”

“…Under this latter scenario, subindividual epigenetic heterogeneity at a given moment in a plant’s lifetime should be genealogically structured, representing the signature of past localized changes within the plant that were propagated and maintained through successive divisions of terminal meristems. This mechanism for internal epigenetic divergence by propagation of stable epimutations is essentially identical to that proposed previously to account for stable subindividual genetic mosaicism via propagation of somatic mutations (Whitham & Slobodchikoff, 1981; Buss, 1983a, b; Whitham et al ., 1984; Gill et al ., 1995; Schmid-Siegert et al ., 2017; Orr et al ., 2020).…”