Tracing the Maternal Line in Glacial–Interglacial Migrations of Populus tremuloides: Finding Trees for Future Sustainable Forests by Searching in the Past

Maintaining and planting sustainable forests is fundamental in perpetuating the essential functions of these ecosystems. A central aspect of managing forests for future resilience is the consideration of past migration and evolution of trees using genetic and genomic data to ensure that functionally appropriate diversity is conserved and utilized. In our study, we generated and compared genetic and genomic data from the plastome to better understand phylogeography and molecular evolution in the tree species Populus tremuloides (aspen). With these analyses, we found evidence of divergence and migration between northern and southern sites. Additionally, evidence of deep incomplete plastome sorting across the Salicaceae was found when examining insertion–deletion (indel) sites associated with DNA repair. By examining these indels in plastomic genes with introns across Salicaceae, we found a strong correlation between the abundance of DNA repair with genomic position and transcript abundance. From our findings, we conclude that previously ignored plastomic data are essential in understanding phylogeography and the evolution of key metabolic processes for improved aspen forest planning. Given the propensity of aspen forests to host high levels of biodiversity, rapidly sequester carbon, absorb excess nitrogen, and efficiently regulate snowmelt, improvements to planning and conservation will be highly impactful.

[1]  S. Kelly,et al.  The Evolutionary Constraints on Angiosperm Chloroplast Adaptation , 2022, bioRxiv.

[2]  C. Tong,et al.  Investigation of genome-wide InDel distribution and segregation in Populus with restriction-site associated DNA sequencing data , 2022, Tropical Plant Biology.

[3]  Daniel B. Sloan,et al.  Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels , 2022, bioRxiv.

[4]  Zhixiang Zhang,et al.  Phylogenomics and Biogeography of Populus Based on Comprehensive Sampling Reveal Deep-Level Relationships and Multiple Intercontinental Dispersals , 2022, Frontiers in Plant Science.

[5]  P. Zheng,et al.  The History and Diversity of Rice Domestication as Resolved From 1464 Complete Plastid Genomes , 2021, Frontiers in Plant Science.

[6]  A. Scheben,et al.  Different DNA repair pathways are involved in single-strand break-induced genomic changes in plants. , 2021, The Plant cell.

[7]  Wei Gao,et al.  Chloroplast genomes in Populus (Salicaceae): comparisons from an intensively sampled genus reveal dynamic patterns of evolution , 2021, Scientific Reports.

[8]  A. Jacobson,et al.  Aspen Soils Retain More Dissolved Organic Carbon Than Conifer Soils in a Sorption Experiment , 2020, Frontiers in Forests and Global Change.

[9]  Itay Mayrose,et al.  A Probabilistic Model for Indel Evolution: Differentiating Insertions from Deletions , 2020, bioRxiv.

[10]  J. Linares,et al.  Understanding genetic diversity of relict forests. Linking long-term isolation legacies and current habitat fragmentation in Abies pinsapo Boiss , 2020, Forest Ecology and Management.

[11]  Abdullah,et al.  Correlations among oligonucleotide repeats, nucleotide substitutions, and insertion–deletion mutations in chloroplast genomes of plant family Malvaceae , 2020 .

[12]  Hongyan Liu,et al.  A global view of aspen: Conservation science for widespread keystone systems , 2020 .

[13]  V. S. Bogdanova Genetic and Molecular Genetic Basis of Nuclear-Plastid Incompatibilities , 2019, Plants.

[14]  S. DiFazio,et al.  Phylogenomics of the genus Populus reveals extensive interspecific gene flow and balancing selection. , 2019, The New phytologist.

[15]  B. Blonder,et al.  Remote sensing of ploidy level in quaking aspen (Populus tremuloides Michx.) , 2019, Journal of Ecology.

[16]  N. Ahmad,et al.  Plant Organelle Genome Replication , 2019, Plants.

[17]  S. Mirarab,et al.  Phylogenetic Signal of Indels and the Neoavian Radiation , 2019, Diversity.

[18]  Jianguo Zhang,et al.  Genetic analysis of admixture and hybrid patterns of Populus hopeiensis and P. tomentosa , 2019, Scientific Reports.

[19]  Vikram E. Chhatre,et al.  Adaptive introgression and maintenance of a trispecies hybrid complex in range‐edge populations of Populus , 2018, Molecular ecology.

[20]  Abramowicz Anna,et al.  Splicing mutations in human genetic disorders: examples, detection, and confirmation , 2018, Journal of Applied Genetics.

[21]  J. Cavender-Bares,et al.  Genetic, morphological, and spectral characterization of relictual Niobrara River hybrid aspens (Populus × smithii). , 2017, American journal of botany.

[22]  A. Hamann,et al.  Post-glacial biogeography of trembling aspen inferred from habitat models and genetic variance in quantitative traits , 2017, Scientific Reports.

[23]  Y. Bergeron,et al.  Fine-scale assessment of genetic diversity of trembling aspen in northwestern North America , 2016, BMC Evolutionary Biology.

[24]  H. Puchta,et al.  Repair of adjacent single-strand breaks is often accompanied by the formation of tandem sequence duplications in plant genomes , 2016, Proceedings of the National Academy of Sciences.

[25]  J. Rockström,et al.  Planetary boundaries: Guiding human development on a changing planet , 2015, Science.

[26]  C. Hefer,et al.  Whole plastome sequencing reveals deep plastid divergence and cytonuclear discordance between closely related balsam poplars, Populus balsamifera and P. trichocarpa (Salicaceae). , 2014, The New phytologist.

[27]  S. Dayanandan,et al.  Phylogeny Reconstruction and Hybrid Analysis of Populus (Salicaceae) Based on Nucleotide Sequences of Multiple Single-Copy Nuclear Genes and Plastid Fragments , 2014, PloS one.

[28]  R. Ryel,et al.  Continental‐scale assessment of genetic diversity and population structure in quaking aspen (Populus tremuloides) , 2013 .

[29]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[30]  Dale N. Richardson,et al.  Deciphering the Plant Splicing Code: Experimental and Computational Approaches for Predicting Alternative Splicing and Splicing Regulatory Elements , 2012, Front. Plant Sci..

[31]  A. Hampe,et al.  Climate Relicts: Past, Present, Future , 2011 .

[32]  A. Hamann,et al.  Assisted migration to address climate change: recommendations for aspen reforestation in western Canada. , 2011, Ecological applications : a publication of the Ecological Society of America.

[33]  D. Macaya-Sanz,et al.  Genetic analysis of post-mating reproductive barriers in hybridizing European Populus species , 2011, Heredity.

[34]  A. R. Pluess Pursuing glacier retreat: genetic structure of a rapidly expanding Larix decidua population , 2011, Molecular ecology.

[35]  P. Meirmans,et al.  Repeated unidirectional introgression towards Populus balsamifera in contact zones of exotic and native poplars , 2010, Molecular ecology.

[36]  R. Lindroth,et al.  Rising concentrations of atmospheric CO2 have increased growth in natural stands of quaking aspen (Populus tremuloides) , 2009 .

[37]  R. Cartwright Problems and solutions for estimating indel rates and length distributions. , 2009, Molecular biology and evolution.

[38]  R. Hudson,et al.  Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes , 2008, Nature.

[39]  E. LaMalfa,et al.  Differential Snowpack Accumulation and Water Dynamics in Aspen and Conifer Communities: Implications for Water Yield and Ecosystem Function , 2008, Ecosystems.

[40]  Philipp W. Messer,et al.  The majority of recent short DNA insertions in the human genome are tandem duplications. , 2007, Molecular biology and evolution.

[41]  Charles Ofria,et al.  EFFECTS OF POPULATION SIZE AND MUTATION RATE ON THE EVOLUTION OF MUTATIONAL ROBUSTNESS , 2007, Evolution; international journal of organic evolution.

[42]  A. E. Escalante,et al.  Long‐distance colonization, isolation by distance, and historical demography in a relictual Mexican pinyon pine (Pinus nelsonii Shaw) as revealed by paternally inherited genetic markers (cpSSRs) , 2003, Molecular ecology.

[43]  P. Beier,et al.  Small isolated aspen stands enrich bird communities in southwestern ponderosa pine forests , 2003 .

[44]  A. DesRochers,et al.  Nitrogen fertilization of trembling aspen seedlings grown on soils of different pH , 2003 .

[45]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

[46]  Geneva W. Chong,et al.  Rapid assessment of butterfly diversity in a montane landscape , 2001, Biodiversity & Conservation.

[47]  K. Olsen,et al.  Gene genealogies and population variation in plants. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[48]  M. Nei,et al.  Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. , 1993, Molecular biology and evolution.

[49]  M T Clegg,et al.  Evolution of a noncoding region of the chloroplast genome. , 1993, Molecular phylogenetics and evolution.

[50]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[51]  R. Tanaka,et al.  Chlorophyll metabolism. , 2006, Current opinion in plant biology.

[52]  J. Shaw,et al.  The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. , 2005, American journal of botany.

[53]  M. Norell,et al.  Tree-based approaches to understanding history; comments on ranks, rules and the quality of the fossil record , 1993 .

[54]  J. Neigel,et al.  Intraspecific Phylogeography: The Mitochondrial DNA Bridge Between Population Genetics and Systematics , 1987 .

[55]  B. V. Barnes Phenotypic variation of trembling aspen in western North America , 1975 .

[56]  E. L. Little Atlas of United States trees. , 1971 .