The architecture of intra-organism mutation rate variation in plants

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 s...

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Published inPLoS biology Vol. 17; no. 4; p. e3000191
Main Authors Wang, Long, Ji, Yilun, Hu, Yingwen, Hu, Huaying, Jia, Xianqin, Jiang, Mengmeng, Zhang, Xiaohui, Zhao, Lina, Zhang, Yanchun, Jia, Yanxiao, Qin, Chao, Yu, Luyao, Huang, Ju, Yang, Sihai, Hurst, Laurence D, Tian, Dacheng
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 09.04.2019
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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.
AbstractList 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.
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. The rates of accumulation of mutations vary between different parts of a plant, with lower rates when mutations have greater potential longevity (such as in leaves) than in short-lived structures (such as petals). Whereas there has been considerable attention paid to understanding differences in the mutation rate between different species, much less is known about variation in the mutation rate within individuals of multicellular species. In animals, evidence suggests that the segregated germline has a lower mutation rate than somatic cells, which accords with an adaptive model of intra-organism mutation rate variation. Here, we consider related questions in plants, which, although not having an early segregated germline, present numerous opportunities to test such an adaptive model. In particular, such a model would predict a lower rate in shoots than in roots and in relatively long-lived leaves compared with ontogenetically related but more ephemeral petals. In addition, we expect that mutation rate variation should be deterministic, such that there is no more heterogeneity in mutation rates between similarly aged branches than expected by chance. By sequencing several hundred genomes for numerous different species, we find all predictions to be supported, with the proviso that the root—shoot difference is witnessed in perennials but not in an annual. This last difference we show to be explicable, as annuals transmit relatively few premeiotic mutations. Although the adaptive model is then parsimonious, we caution that the mutation rate in plants can be easily affected by local conditions, as evidenced by large differences between lab-grown callus and field-grown plants.
Audience Academic
Author Zhao, Lina
Jiang, Mengmeng
Yang, Sihai
Zhang, Xiaohui
Yu, Luyao
Ji, Yilun
Tian, Dacheng
Zhang, Yanchun
Wang, Long
Jia, Yanxiao
Qin, Chao
Huang, Ju
Hu, Yingwen
Hurst, Laurence D
Jia, Xianqin
Hu, Huaying
AuthorAffiliation 1 State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing, China
Institute of Science and Technology Austria (IST Austria), AUSTRIA
2 The Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30964866$$D View this record in MEDLINE/PubMed
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Copyright COPYRIGHT 2019 Public Library of Science
2019 Wang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2019 Wang et al 2019 Wang et al
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Snippet 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....
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SubjectTerms Accumulation
Biology and Life Sciences
Biotechnology
Branch banking
Callus
Cell division
Engineering and Technology
Fragility
Funding
Gene Expression Regulation, Plant - genetics
Genes, Plant - genetics
Genomes
Genomics
Germ Cells
Heterogeneity
Laboratories
Leaves
Life sciences
Meristems
Mutation
Mutation - genetics
Mutation Accumulation
Mutation Rate
Mutation rates
Observations
Pharmaceuticals
Plant genetics
Plant Leaves - genetics
Plant mutation
Plant Roots - genetics
Plant Shoots - genetics
Plant species
Plant tissues
Plants - genetics
Research and analysis methods
Shoots
Strawberries
Supervision
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Title The architecture of intra-organism mutation rate variation in plants
URI https://www.ncbi.nlm.nih.gov/pubmed/30964866
https://www.proquest.com/docview/2249971120
https://search.proquest.com/docview/2207157649
https://pubmed.ncbi.nlm.nih.gov/PMC6456163
https://doaj.org/article/d0ed4b2864b3417091406d2648d21237
http://dx.doi.org/10.1371/journal.pbio.3000191
Volume 17
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