Single‐nucleotide mosaicism in citrus: Estimations of somatic mutation rates and total number of variants

Abstract

Most of the hundreds of citrus varieties are derived from spontaneous mutations. We characterized the dynamics of single‐nucleotide mosaicism in a 36‐yr‐old clementine (Citrus ×clementina hort. ex Tanaka) tree, a commercial citrus whose vegetative behavior is known in detail. Whole‐genome sequencing identified 73 reliable somatic mutations, 48% of which were transitions from G/C to A/T, suggesting ultraviolet (UV) exposure as mutagen. The mutations accumulated in sectorized areas of the tree in a nested hierarchy determined by the branching pattern, although some variants detected in the basal parts were also found in the new growth and were fixed in some branches and leaves of much younger age. The estimate of mutation rates in our tree was 4.4 × 10−10 bp−1 yr−1, a rate in the range reported in other perennials. Assuming a perfect configuration and taking advantage of previous counts on the number of total leaves of typical clementine trees, these mutation determinations allowed to estimate for the first time the total number of variants present in a standard adult tree (1,500–5,000) and the somatic mutations generated in a typical leaf flush (0.92–1.19). From an evolutionary standpoint, the sectoral distribution of somatic mutations and the habit of periodic foliar renewal of long‐lived plants appear to increase genetic heterogeneity and, therefore, the adaptive role of somatic mutations reducing the mutational load and providing fitness benefits.

Branching architecture affects genetic diversity within an individual tree

“…Conversely, the shape of a phylogeny may enable to infer the dynamics of stem cell lineages that determines the heterogeneity within a SAM. Empirical studies have, in fact, reported both concordance and discrepancies between phylogenetic and physical shapes (Zahrdadníková et al, 2020; Perez-Roman et al, 2021; Satake et al 2023).…”

“…The presence of genetic variation within an individual has been reported in numerous tree species (Schmid-Siegert et al, 2017;Plomion et al, 2018;Wang et al, 2019;Hanlon et al, 2019;Orr et al, 2020;Hofmeister et al, 2020;Perez-Roman et al, 2021;Duan et al, 2022;Satake et al, 2023). Somatic mutations accumulated as trees age (Satake et al 2023) and were distributed following the branching architecture of a tree (Schmid-Siegert et al, 2017), and the phylogeny of somatic mutations in a single tree showed the same topology as the physical shape of a tree (Perez-Roman et al, 2021;Satake et al 2023). Genetic variation seemingly presented not only among branches but also among cells in a shoot apical meristem (hereafter SAM) of a single branch (Zahrdadníková et al, 2020;Duan et al, 2022;Schmitt et al, 2022).…”

“…Recent advances in genomic technology, such as next-generation sequencing, have facilitated the quantitative identification of somatic mutations in long-lived modular organisms like trees (Reusch et al, 2021). The presence of genetic variation within an individual has been reported in numerous tree species (Schmid-Siegert et al, 2017;Plomion et al, 2018;Wang et al, 2019;Hanlon et al, 2019;Orr et al, 2020;Hofmeister et al, 2020;Perez-Roman et al, 2021;Duan et al, 2022;Satake et al, 2023). Somatic mutations accumulated as trees age (Satake et al 2023) and were distributed following the branching architecture of a tree (Schmid-Siegert et al, 2017), and the phylogeny of somatic mutations in a single tree showed the same topology as the physical shape of a tree (Perez-Roman et al, 2021;Satake et al 2023).…”

“…Genetic variation seemingly presented not only among branches but also among cells in a shoot apical meristem (hereafter SAM) of a single branch (Zahrdadníková et al, 2020; Duan et al, 2022; Schmitt et al, 2022). Additionally, somatic mutations were mostly neutral within a tree (Orr et al, 2020; Perez-Roman et al, 2021; Duan et al, 2022; Satake et al, 2023). These mutations were transmitted to offspring (Plomion et al, 2018), and at the stage of seed production and seedling growth, they seem to have experienced natural selection (Ally et al, 2016; Satake et al, 2023).…”

Modelling somatic mutation accumulation and expansion in a long-lived tree with hierarchical modular architecture

“…3). Since no empirical studies to date have provided evidence of natural selection against somatic mutations within trees (Orr et al, 2019; Perez-Roman et al, 2021; Duan et al, 2022; Imai et al, 2023), we focused exclusively on the neutral mutations in our model.…”