Abstract
Plants are thought to lack an early segregating germline and often retain both asexual and sexual reproduction, both of which may allow somatic mutations to enter the gametes or clonal progeny, and thereby impact plant evolution. It is yet unclear how often these somatic mutations occur during plant development and what proportion is transmitted to their sexual or cloned offspring. Asexual "seedless" propagation has contributed greatly to the breeding in many fruit crops, such as citrus, grapes and bananas. Whether plants in these lineages experience substantial somatic mutation accumulation is unknown. To estimate the somatic mutation accumulation and inheritance among a clonal population of plant, here we assess somatic mutation accumulation in Musa basjoo, a diploid banana wild relative, using 30 whole-genome resequenced samples collected from five structures, including leaves, sheaths, panicle, roots and underground rhizome connecting three clonal individuals. We observed 18.5 high proportion de novo somatic mutations on average between each two adjacent clonal suckers, equivalent to ~ 2.48 × 10–8 per site per asexual generation, higher than the per site per sexual generation rates (< 1 × 10–8) reported in Arabidopsis and peach. Interestingly, most of these inter-ramet somatic mutations were shared simultaneously in different tissues of the same individual with a high level of variant allele fractions, suggesting that these somatic mutations arise early in ramet development and that each individual may develop only from a few apical stem cells. These results thus suggest substantial mutation accumulation in a wild relative of banana. Our work reveals the significance of somatic mutation in Musa basjoo genetics variations and contribute to the trait improvement breeding of bananas and other asexual clonal crops.
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Data availability
The sequencing reads have been submitted to the National Center for Biotechnology Information (NCBI) under BioProject PRJNA805381.
References
Adamek K, Jones AMP, Torkamaneh D (2021) Accumulation of somatic mutations leads to genetic mosaicism in cannabis. Plant Genome. https://doi.org/10.1002/tpg2.20169
Bebber DP (2019) Climate change effects on Black Sigatoka disease of banana. Philos Transact R Soc B 374:20180269. https://doi.org/10.1098/rstb.2018.0269
Broertjes C, van Harten AM (1985) Single cell origin of adventitious buds. Euphytica 34:93–95. https://doi.org/10.1007/BF00022867
Burian A, Barbier de Reuille P, Kuhlemeier C (2016) Patterns of stem cell divisions contribute to plant longevity. Curr Biol 26:1385–1394. https://doi.org/10.1016/j.cub.2016.03.067
Clarke JD (2009) Cetyltrimethyl Ammonium Bromide (CTAB) DNA Miniprep for Plant DNA Isolation. Cold Spring Harb Protoc. https://doi.org/10.1101/pdb.prot5177
DePristo MA, Banks E, Poplin R et al (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498. https://doi.org/10.1038/ng.806
Foster TM, Aranzana MJ (2018) Attention sports fans! The far-reaching contributions of bud sport mutants to horticulture and plant biology. Horticult Res 5:1–13. https://doi.org/10.1038/s41438-018-0062-x
Groot EP, Laux T (2016) Ageing: how do long-lived plants escape mutational meltdown? Curr Biol 26:R530–R532. https://doi.org/10.1016/j.cub.2016.05.049
Hanlon VCT, Otto SP, Aitken SN (2019) Somatic mutations substantially increase the per generation mutation rate in the conifer Picea sitchensis. Evol Lett 3:348–358. https://doi.org/10.1002/evl3.121
Hofmeister BT, Denkena J, Colomé-Tatché M et al (2020) A genome assembly and the somatic genetic and epigenetic mutation rate in a wild long-lived perennial Populus trichocarpa. Genome Biol 21:259. https://doi.org/10.1186/s13059-020-02162-5
Jankowicz-Cieslak J, Huynh OA, Brozynska M et al (2012) Induction, rapid fixation and retention of mutations in vegetatively propagated banana. Plant Biotechnol J 10:1056–1066. https://doi.org/10.1111/j.1467-7652.2012.00733.x
Jin J-J, Yu W-B, Yang J-B et al (2020) GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol 21:241. https://doi.org/10.1186/s13059-020-02154-5
Klekowski EJ (2003) Plant clonality, mutation, diplontic selection and mutational meltdown. Biol J Linn Soc 79:61–67. https://doi.org/10.1046/j.1095-8312.2003.00183.x
Klekowski EJ Jr, Godfrey PJ (1989) Ageing and mutation in plants. Nature 340:389–391. https://doi.org/10.1038/340389a0
Lanfear R (2018) Do plants have a segregated germline? PLoS Biol 16:e2005439. https://doi.org/10.1371/journal.pbio.2005439
Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404
Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:13033997 [q-bio]
Liu F, Movahedi A, Yang W et al (2021) The complete chloroplast genome and characteristics analysis of Musa basjoo Siebold. Mol Biol Rep. https://doi.org/10.1007/s11033-021-06702-5
Marcotrigiano M, Stewart RN (1984) All variegated plants are not chimeras. Science 223:505–505. https://doi.org/10.1126/science.223.4635.505-a
Marín DH, Romero RA, Guzmán M, Sutton TB (2003) Black sigatoka: an increasing threat to banana cultivation. Plant Dis 87:208–222. https://doi.org/10.1094/PDIS.2003.87.3.208
McKenna A, Hanna M, Banks E et al (2010) The genome analysis toolkit: a mapreduce framework for analyzing next-generation dna sequencing data. Genome Res 20:1297–1303. https://doi.org/10.1101/gr.107524.110
Munné-Bosch S (2020) Long-lived trees are not immortal. Trends Plant Sci 25:846–849. https://doi.org/10.1016/j.tplants.2020.06.006
Ordonez N, Seidl MF, Waalwijk C et al (2015) Worse comes to worst: bananas and panama disease—when plant and pathogen clones meet. PLoS Pathog 11:e1005197. https://doi.org/10.1371/journal.ppat.1005197
Orr AJ, Padovan A, Kainer D et al (2020) A phylogenomic approach reveals a low somatic mutation rate in a long-lived plant. Proc R Soc B 287:20192364. https://doi.org/10.1098/rspb.2019.2364
Ossowski S, Schneeberger K, Lucas-Lledó JI et al (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis Thaliana. Science 327:92–94. https://doi.org/10.1126/science.1180677
Perez-Roman E, Borredá C, López-García Usach A, Talon M (2021) Single-nucleotide mosaicism in citrus: Estimations of somatic mutation rates and total number of variants. Plant Genome. https://doi.org/10.1002/tpg2.20162
Pineda-Krch F (1999) On the potential for evolutionary change in meristematic cell lineages through intraorganismal selection. J Evol Biol 12:681–688. https://doi.org/10.1046/j.1420-9101.1999.00066.x
Plomion C, Aury J-M, Amselem J et al (2018) Oak genome reveals facets of long lifespan. Nature Plants 4:440–452. https://doi.org/10.1038/s41477-018-0172-3
Price MN, Dehal PS, Arkin AP (2010) FastTree 2 – approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. https://doi.org/10.1371/journal.pone.0009490
Ren Y, He Z, Liu P et al (2021) Somatic mutation analysis in salix suchowensis reveals early-segregated cell lineages. Mol Biol Evol 38:5292–5308. https://doi.org/10.1093/molbev/msab286
Reusch TBH, Baums IB, Werner B (2021) Evolution via somatic genetic variation in modular species. Trends Ecol Evol 36:1083–1092. https://doi.org/10.1016/j.tree.2021.08.011
Satina S, Blakeslee AF, Avery AG (1940) Demonstration of the three germ layers in the shoot apex of datura by means of induced polyploidy in periclinal chimeras. Am J Bot 27:895–905. https://doi.org/10.2307/2436558
Schmid-Siegert E, Sarkar N, Iseli C et al (2017) Low number of fixed somatic mutations in a long-lived oak tree. Nature Plants 3:926–929. https://doi.org/10.1038/s41477-017-0066-9
Schoen DJ, Schultz ST (2019) Somatic mutation and evolution in plants. Annu Rev Ecol Evol Syst 50:49–73. https://doi.org/10.1146/annurev-ecolsys-110218-024955
Scofield DG (2014) A definitive demonstration of fitness effects due to somatic mutation in a plant. Heredity 112:361–362. https://doi.org/10.1038/hdy.2013.114
Shamel AD, Pomeroy CS (1936) Bud mutations in horticultural crops. J Hered 27:487–494. https://doi.org/10.1093/oxfordjournals.jhered.a104171
Simberloff D, Leppanen C (2019) Plant somatic mutations in nature conferring insect and herbicide resistance. Pest Manag Sci 75:14–17. https://doi.org/10.1002/ps.5157
Szymkowiak EJ, Sussex IM (1996) What chimeras can tell us about plant development. Annu Rev Plant Physiol Plant Mol Biol 47:351–376. https://doi.org/10.1146/annurev.arplant.47.1.351
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192. https://doi.org/10.1093/bib/bbs017
Wang L, Ji Y, Hu Y et al (2019) The architecture of intra-organism mutation rate variation in plants. PLoS Biol 17:e3000191. https://doi.org/10.1371/journal.pbio.3000191
Wang L, Huang Y, Liu Z et al (2021a) Somatic variations led to the selection of acidic and acidless orange cultivars. Nat Plants. https://doi.org/10.1038/s41477-021-00941-x
Wang X, Wang A, Li Y, et al (2021b) A novel banana mutant “RF 1” (Musa spp. ABB, Pisang Awak Subgroup) for improved agronomic traits and enhanced cold tolerance and disease resistance. Front Plant Sci 12
Watson JM, Platzer A, Kazda A et al (2016) Germline replications and somatic mutation accumulation are independent of vegetative life span in Arabidopsis. Proc Natl Acad Sci USA 113:12226–12231. https://doi.org/10.1073/pnas.1609686113
White J (1979) The plant as a metapopulation. Annu Rev Ecol Syst 10:109–145. https://doi.org/10.1146/annurev.es.10.110179.000545
Wu W, Yang Y-L, He W-M et al (2016) Whole genome sequencing of a banana wild relative Musa itinerans provides insights into lineage-specific diversification of the Musa genus. Sci Rep. https://doi.org/10.1038/srep31586
Xie Z, Wang L, Wang L et al (2016) Mutation rate analysis via parent–progeny sequencing of the perennial peach. I. A low rate in woody perennials and a higher mutagenicity in hybrids. Proc R Soc B 283:20161016. https://doi.org/10.1098/rspb.2016.1016
Yang S, Wang L, Huang J et al (2015) Parent-progeny sequencing indicates higher mutation rates in heterozygotes. Nature 523:463–467. https://doi.org/10.1038/nature14649
Yu L, Boström C, Franzenburg S et al (2020) Somatic genetic drift and multilevel selection in a clonal seagrass. Nat Ecol Evol 4:952–962. https://doi.org/10.1038/s41559-020-1196-4
Zahradníková E, Ficek A, Brejová B et al (2020) Mosaicism in old trees and its patterns. Trees 34:357–370. https://doi.org/10.1007/s00468-019-01921-7
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This work was supported by the National Science Foundation of China (Grant Nos. 31970517, 31900195, and 31970236).
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DT, SY, LW and JH planned and designed the research. YJ, XC and SL performed experiments, conducted fieldwork, and analyzed data. SY, LW, BT and JH wrote the manuscript. YJ and XC contributed equally.
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Ji, Y., Chen, X., Lin, S. et al. High level of somatic mutations detected in a diploid banana wild relative Musa basjoo. Mol Genet Genomics 298, 67–77 (2023). https://doi.org/10.1007/s00438-022-01959-2
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DOI: https://doi.org/10.1007/s00438-022-01959-2