Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch

Silver birch (Betula pendula) is a pioneer boreal tree that can be induced to flower within 1 year. Its rapid life cycle, small (440-Mb) genome, and advanced germplasm resources make birch an attractive model for forest biotechnology. We assembled and chromosomally anchored the nuclear genome of an inbred B. pendula individual. Gene duplicates from the paleohexaploid event were enriched for transcriptional regulation, whereas tandem duplicates were overrepresented by environmental responses. Population resequencing of 80 individuals showed effective population size crashes at major points of climatic upheaval. Selective sweeps were enriched among polyploid duplicates encoding key developmental and physiological triggering functions, suggesting that local adaptation has tuned the timing of and cross-talk between fundamental plant processes. Variation around the tightly-linked light response genes PHYC and FRS10 correlated with latitude and longitude and temperature, and with precipitation for PHYC. Similar associations characterized the growth-promoting cytokinin response regulator ARR1, and the wood development genes KAK and MED5A.

Petri Auvinen | Jarkko Salojärvi | Mikael Brosché | Jaakko Kangasjärvi | Juha Mikola | Péter Poczai | Ali Amiryousefi | Olli-Pekka Smolander | Andriy Kovalchuk | Ykä Helariutta | Juha Immanen | Kaisa Nieminen | Victor A Albert | Pasi Rastas | Elina Oksanen | Colin T Kelleher | Ari Pekka Mähönen | Chris Dardick | Ülo Niinemets | Suvi Sutela | Martin Lascoux | Paula Elomaa | Juhana I Kammonen | Tiina Blomster | Tianying Lan | Balamuralikrishna Jayaprakash | P. Auvinen | J. Salojärvi | Ü. Niinemets | P. Rastas | L. Paulin | Y. Helariutta | M. Lascoux | K. Nieminen | L. Kauppinen | J. Kangasjärvi | J. Vahala | Tiina Blomster | J. Immanen | A. P. Mähönen | A. Kärkönen | T. Teeri | Olli-Pekka Smolander | Hiroaki Fujii | P. Poczai | Courtney A. Hollender | C. Dardick | A. Schulman | J. Mikola | Timo P. Sipilä | M. Brosché | F. Asiegbu | V. Albert | Tuula Puhakainen | P. Heino | E. T. Palva | S. Kärenlampi | K. Mouhu | B. Jayaprakash | L. Pazouki | T. Lan | O. Blokhina | K. Fagerstedt | C. van der Schoot | A. Tervahauta | C. Kelleher | M. Rousi | J. Tanskanen | Suvi K. Broholm | P. Elomaa | Airi Lamminmäki | Ali Amiryousefi | Matti Rousi | Kristiina Himanen | A. Shapiguzov | A. Welling | S. Kontunen-Soppela | Aleksia Vaattovaara | Sitaram Rajaraman | O. Safronov | M. Wrzaczek | A. Gauthier | Sari Kontunen-Soppela | Andriy Kovalchuk | S. Sutela | Hiroaki Fujii | E Tapio Palva | Fred O Asiegbu | E. Oksanen | J. Barajas-López | Teemu H Teeri | Juhana I. Kammonen | Alan H Schulman | Raili Ruonala | Sitaram Rajaraman | Omid Safronov | Pezhman Safdari | Airi Lamminmäki | Jaakko Tanskanen | Risto Hagqvist | Gugan Eswaran | Viivi Helena Ahonen | Juan Alonso Serra | Juan de Dios Barajas-Lopez | Daniel Blande | Olga Blokhina | Suvi Broholm | Fuqiang Cui | Sanna E Ehonen | Sacha Escamez | Kurt V Fagerstedt | Adrien Gauthier | Peter J Gollan | Pauliina Halimaa | Pekka I Heino | Courtney Hollender | Saijaliisa Kangasjärvi | Leila Kauppinen | J Patrik Koskinen | Sirpa O Kärenlampi | Anna K Kärkönen | Kean-Jin Lim | Johanna Leppälä | Lee Macpherson | Katriina Mouhu | Kirk Overmyer | Leila Pazouki | Ville Pennanen | Tuula Puhakainen | Boy J H M Possen | Matleena Punkkinen | Moona M Rahikainen | Christiaan van der Schoot | Alexey Shapiguzov | Maija Sierla | Timo P Sipilä | Arja I Tervahauta | Aleksia Vaattovaara | Jorma Vahala | Lidia Vetchinnikova | Annikki Welling | Michael Wrzaczek | Enjun Xu | Lars G Paulin | Juan Antonio Alonso Serra | K. Overmyer | Matleena Punkkinen | Kean-Jin Lim | P. J. Gollan | B. Possen | V. Ahonen | Kristiina Himanen | E. Xu | Moona Rahikainen | Saijaliisa Kangasjärvi | C. Schoot | L. Macpherson | Maija Sierla | Daniel Blande | Fuqiang Cui | Raili Ruonala | J. Leppälä | Ville Pennanen | P. Halimaa | Sacha Escamez | Pezhman Safdari | R. Hagqvist | L. Vetchinnikova | S. Kontunen‐Soppela | Gugan Eswaran | Juan de Dios Barajas-López | Sanna Ehonen | J. Koskinen | Michael Wrzaczek | E. Palva | Juha Immanen | Pauliina Halimaa

[1]  C. Bettigole,et al.  Mapping tree density at a global scale , 2015, Nature.

[2]  P. Wareing,et al.  Early Induction of Flowering in Birch Seedlings , 1959, Nature.

[3]  E. T. Palva,et al.  Involvement of CBF Transcription Factors in Winter Hardiness in Birch1[W][OA] , 2008, Plant Physiology.

[4]  A. Tunnacliffe,et al.  LEA proteins prevent protein aggregation due to water stress. , 2005, The Biochemical journal.

[5]  Xiangzong Meng,et al.  Phosphorylation of a WRKY Transcription Factor by MAPKs Is Required for Pollen Development and Function in Arabidopsis , 2014, PLoS genetics.

[6]  M. Hülskamp,et al.  The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles , 2003, Molecular Genetics and Genomics.

[7]  C. Pál,et al.  Dosage sensitivity and the evolution of gene families in yeast , 2003, Nature.

[8]  P. B. Eidesen,et al.  Comparative analyses of plastid and AFLP data suggest different colonization history and asymmetric hybridization between Betula pubescens and B. nana , 2015, Molecular ecology.

[9]  Ari Pekka Mähönen,et al.  Cytokinin and Auxin Display Distinct but Interconnected Distribution and Signaling Profiles to Stimulate Cambial Activity , 2016, Current Biology.

[10]  Richard M. Clark,et al.  The PHYTOCHROME C photoreceptor gene mediates natural variation in flowering and growth responses of Arabidopsis thaliana , 2006, Nature Genetics.

[11]  C. Chapple,et al.  Can genetic engineering of lignin deposition be accomplished without an unacceptable yield penalty? , 2013, Current opinion in biotechnology.

[12]  Yeting Zhang,et al.  A genome triplication associated with early diversification of the core eudicots , 2012, Genome Biology.

[13]  J. Poulain,et al.  The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla , 2007, Nature.

[14]  M. Fortin,et al.  Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data , 2010, Molecular ecology resources.

[15]  Rongcheng Lin,et al.  Arabidopsis FHY3/FAR1 Gene Family and Distinct Roles of Its Members in Light Control of Arabidopsis Development1 , 2004, Plant Physiology.

[16]  P. Gibbard,et al.  Formal subdivision of the Quaternary System/Period: Past, present, and future , 2015 .

[17]  L. Herrera-Estrella,et al.  Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought , 2016, Proceedings of the National Academy of Sciences.

[18]  S. Mane,et al.  Contrasting patterns of evolution following whole genome versus tandem duplication events in Populus. , 2012, Genome research.

[19]  M. Hutchinson,et al.  Potential Impacts of Climate Change on the Distribution of North American Trees , 2007 .

[20]  A. Shvidenko,et al.  Boreal forest health and global change , 2015, Science.

[21]  A. Paleobotanical Interpretation of Tertiary Climates in the Northern Hemisphere : Data from fossil plants make it possible to reconstruct Tertiary climatic changes , which may be correlated with changes in the inclination of the earth ' s rotational axis , 2011 .

[22]  J. Alonso,et al.  Ethylene signaling: simple ligand, complex regulation. , 2013, Current opinion in plant biology.

[23]  Douglas G. Scofield,et al.  Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species , 2015, Genetics.

[24]  Michael Ladisch,et al.  Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant , 2014, Nature.

[25]  Takashi Aoyama,et al.  A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem , 2008, Science.

[26]  Swapan Mallick,et al.  Ancient Admixture in Human History , 2012, Genetics.

[27]  G. Sandberg,et al.  The Arabidopsis LRR-RLK, PXC1, is a regulator of secondary wall formation correlated with the TDIF-PXY/TDR-WOX4 signaling pathway , 2013, BMC Plant Biology.

[28]  N. Raikhel,et al.  An early secretory pathway mediated by GNOM-LIKE 1 and GNOM is essential for basal polarity establishment in Arabidopsis thaliana , 2015, Proceedings of the National Academy of Sciences.

[29]  Brian C. Thomas,et al.  Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. , 2006, Genome research.

[30]  E. Spalding,et al.  AtLAZY1 is a signaling component required for gravitropism of the Arabidopsis thaliana inflorescence. , 2013, The Plant journal : for cell and molecular biology.

[31]  A. Danon,et al.  The Arabidopsis sweetie mutant is affected in carbohydrate metabolism and defective in the control of growth, development and senescence. , 2008, The Plant journal : for cell and molecular biology.

[32]  J. Doonan,et al.  Endopolyploidy as a potential alternative adaptive strategy for Arabidopsis leaf size variation in response to UV-B , 2014, Journal of experimental botany.

[33]  Keith Roberts,et al.  "Big it up": endoreduplication and cell-size control in plants. , 2003, Current opinion in plant biology.

[34]  Chris Dardick,et al.  Molecular basis of angiosperm tree architecture. , 2015, The New phytologist.

[35]  Ykä Helariutta,et al.  A Mutually Inhibitory Interaction between Auxin and Cytokinin Specifies Vascular Pattern in Roots , 2011, Current Biology.

[36]  Le-Shin Wu,et al.  Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies , 2014, Genome Biology.

[37]  Yuriko Osakabe,et al.  RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis , 2010, Development.

[38]  Landscape and evolutionary dynamics of terminal repeat retrotransposons in miniature in plant genomes , 2016, Genome Biology.

[39]  D. Naquin,et al.  Suppression of Dwarf and irregular xylem Phenotypes Generates Low-Acetylated Biomass Lines in Arabidopsis1[OPEN] , 2015, Plant Physiology.

[40]  Diqiu Yu,et al.  Arabidopsis WRKY2 transcription factor mediates seed germination and postgermination arrest of development by abscisic acid , 2009, BMC Plant Biology.

[41]  Melissa D. Lehti-Shiu,et al.  Importance of Lineage-Specific Expansion of Plant Tandem Duplicates in the Adaptive Response to Environmental Stimuli1[W][OA] , 2008, Plant Physiology.

[42]  T. Schmülling,et al.  Gain-of-Function Mutants of the Cytokinin Receptors AHK2 and AHK3 Regulate Plant Organ Size, Flowering Time and Plant Longevity1 , 2017, Plant Physiology.

[43]  A. Millar,et al.  Low-temperature-specific effects of PHYTOCHROME C on the circadian clock in Arabidopsis suggest that PHYC underlies natural variation in biological timing , 2015, bioRxiv.

[44]  Anders Albrechtsen,et al.  ANGSD: Analysis of Next Generation Sequencing Data , 2014, BMC Bioinformatics.

[45]  Q. Qian,et al.  LAZY1 controls rice shoot gravitropism through regulating polar auxin transport , 2007, Cell Research.

[46]  C. Alonso-Blanco,et al.  Altitudinal and Climatic Adaptation Is Mediated by Flowering Traits and FRI, FLC, and PHYC Genes in Arabidopsis1[W] , 2011, Plant Physiology.

[47]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[48]  S. Berlin,et al.  Genetic and morphological evidence for introgression between three species of willows , 2015, BMC Evolutionary Biology.

[49]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[50]  Masayuki Higuchi,et al.  Cytokinin Signaling and Its Inhibitor AHP6 Regulate Cell Fate During Vascular Development , 2006, Science.

[51]  T. Kakimoto,et al.  Cytokinins are central regulators of cambial activity , 2008, Proceedings of the National Academy of Sciences.

[52]  O. M. Heide,et al.  Dormancy release and chilling requirement of buds of latitudinal ecotypes of Betula pendula and B. pubescens. , 1995, Tree physiology.

[53]  Douglas G. Scofield,et al.  The Norway spruce genome sequence and conifer genome evolution , 2013, Nature.

[54]  W. Jin,et al.  Pleiotropic effects of ZmLAZY1 on the auxin-mediated responses to gravity and light in maize shoot and inflorescences , 2013, Plant signaling & behavior.

[55]  Ying-Tang Lu,et al.  Low temperature inhibits root growth by reducing auxin accumulation via ARR1/12. , 2015, Plant & cell physiology.

[56]  Omer Gokcumen,et al.  Exploring the role of copy number variants in human adaptation. , 2012, Trends in genetics : TIG.

[57]  T. Araki,et al.  CRYPTIC PRECOCIOUS/MED12 is a Novel Flowering Regulator with Multiple Target Steps in Arabidopsis , 2012, Plant & cell physiology.

[58]  Yun-Xin Fu,et al.  Exploring Population Size Changes Using SNP Frequency Spectra , 2015, Nature Genetics.

[59]  Seung Y. Rhee,et al.  Genomic Signatures of Specialized Metabolism in Plants , 2014, Science.

[60]  M. Sofiev,et al.  Towards numerical forecasting of long-range air transport of birch pollen: theoretical considerations and a feasibility study , 2006, International journal of biometeorology.

[61]  M. Lascoux,et al.  Impact of Ice Ages on the genetic structure of trees and shrubs. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[62]  A. Paterson,et al.  Polyploidy-associated genome modifications during land plant evolution , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[63]  K. Shinozaki,et al.  Functional Analysis of an Arabidopsis Transcription Factor, DREB2A, Involved in Drought-Responsive Gene Expression[W][OA] , 2006, The Plant Cell Online.

[64]  Tong Wang,et al.  A receptor heteromer mediates the male perception of female attractants in plants , 2016, Nature.

[65]  H. McAllister,et al.  Molecular phylogeny and genome size evolution of the genus Betula (Betulaceae) , 2016, Annals of botany.

[66]  K. Anamthawat-jónsson,et al.  Natural hybridisation in birch: triploid hybrids between Betula nana and B. pubescens , 2003, Plant Cell, Tissue and Organ Culture.

[67]  M. Lynch Evolution of the mutation rate. , 2010, Trends in genetics : TIG.

[68]  Hai Wang,et al.  Phytochrome signaling: time to tighten up the loose ends. , 2015, Molecular plant.

[69]  T. Laux,et al.  Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. , 2011, Developmental cell.

[70]  Brody J Deyoung,et al.  The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. , 2006, The Plant journal : for cell and molecular biology.

[71]  Christophe Dessimoz,et al.  Gene Ontology: Pitfalls, Biases, and Remedies. , 2016, Methods in molecular biology.

[72]  Philipp W. Messer,et al.  Population genomics of rapid adaptation by soft selective sweeps. , 2013, Trends in ecology & evolution.

[73]  M. Schmid,et al.  MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor , 2010, Nature.

[74]  Lex E. Flagel,et al.  Gene duplication and evolutionary novelty in plants. , 2009, The New phytologist.

[75]  M. DePristo,et al.  A framework for variation discovery and genotyping using next-generation DNA sequencing data , 2011, Nature Genetics.

[76]  K. Heath,et al.  Discordant Longitudinal Clines in Flowering Time and Phytochrome C in Arabidopsis thaliana , 2008, Evolution; international journal of organic evolution.

[77]  T. Greb,et al.  MOL1 is required for cambium homeostasis in Arabidopsis , 2016, The Plant journal : for cell and molecular biology.