The architecture of intra-organism mutation rate variation in plants

PLoS Biol. 2019 Apr 9;17(4):e3000191. doi: 10.1371/journal.pbio.3000191. eCollection 2019 Apr.

Abstract

Given the disposability of somatic tissue, selection can favor a higher mutation rate in the early segregating soma than in germline, as seen in some animals. Although in plants intra-organismic mutation rate heterogeneity is poorly resolved, the same selectionist logic can predict a lower rate in shoot than in root and in longer-lived terminal tissues (e.g., leaves) than in ontogenetically similar short-lived ones (e.g., petals), and that mutation rate heterogeneity should be deterministic with no significant differences between biological replicates. To address these expectations, we sequenced 754 genomes from various tissues of eight plant species. Consistent with a selectionist model, the rate of mutation accumulation per unit time in shoot apical meristem is lower than that in root apical tissues in perennials, in which a high proportion of mutations in shoots are themselves transmissible, but not in annuals, in which somatic mutations tend not to be transmissible. Similarly, the number of mutations accumulated in leaves is commonly lower than that within a petal of the same plant, and there is no more heterogeneity in accumulation rates between replicate branches than expected by chance. High mutation accumulation in runners of strawberry is, we argue, the exception that proves the rule, as mutation transmission patterns indicate that runner has a restricted germline. However, we also find that in vitro callus tissue has a higher mutation rate (per unit time) than the wild-grown comparator, suggesting nonadaptive mutational "fragility". As mutational fragility does not obviously explain why the shoot-root difference varies with plant longevity, we conclude that some mutation rate variation between tissues is consistent with selectionist theory but that a mechanistic null of mutational fragility should be considered.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Gene Expression Regulation, Plant / genetics*
  • Genes, Plant / genetics
  • Germ Cells
  • Mutation / genetics
  • Mutation Accumulation
  • Mutation Rate*
  • Plant Leaves / genetics
  • Plant Roots / genetics
  • Plant Shoots / genetics
  • Plants / genetics*

Grants and funding

This work was supported by a grant from the European Research Council (https://erc.europa.eu), grant ERC-2014-ADG 669207 to LDH and grants from the National Natural Science Foundation of China (http://www.nsfc.gov.cn/english/site_1/index.html), 91731308, 31601041, and 31671322 to LW, DT and SY. It was further supported by a grant (unnumbered) from Jiangsu Collaborative Innovation Center for Modern Crop Production to DT and SY. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.