The chromosome-scale genome and population genomics reveal the adaptative evolution of Populus pruinosa to desertification environment

Jianhao Sun , Jindong Xu , Chen Qiu , Juntuan Zhai , Shanhe Zhang , Xiao Zhang , Zhihua Wu , Zhijun Li

Horticulture Research ›› 2024, Vol. 11 ›› Issue (3) : 034

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (3) :034 DOI: 10.1093/hr/uhae034
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The chromosome-scale genome and population genomics reveal the adaptative evolution of Populus pruinosa to desertification environment
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Abstract

The Populus pruinosa is a relic plant that has managed to survive in extremely harsh desert environments. Owing to intensifying global warming and desertification, research into ecological adaptation and speciation of P. pruinosa has attracted considerable interest, but the lack of a chromosome-scale genome has limited adaptive evolution research. Here, a 521.09 Mb chromosome-level reference genome of P. pruinosa was reported. Genome evolution and comparative genomic analysis revealed that tandemly duplicated genes and expanded gene families in P. pruinosa contributed to adaptability to extreme desert environments (especially high salinity and drought). The long terminal repeat retrotransposons (LTR-RTs) inserted genes in the gene body region might drive the adaptive evolution of P. pruinosa and species differentiation in saline-alkali desert environments. We recovered genetic differentiation in the populations of the northern Tianshan Mountain and southern Tianshan Mountain through whole-genome resequencing of 156 P. pruinosa individuals from 25 populations in China. Further analyses revealed that precipitation drove the local adaptation of P. pruinosa populations via some genetic sites, such as MAG2-interacting protein 2 (MIP2) and SET domain protein 25 (SDG25). This study will provide broad implications for adaptative evolution and population studies by integrating internal genetic and external environmental factors in P. pruinosa.

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Jianhao Sun, Jindong Xu, Chen Qiu, Juntuan Zhai, Shanhe Zhang, Xiao Zhang, Zhihua Wu, Zhijun Li. The chromosome-scale genome and population genomics reveal the adaptative evolution of Populus pruinosa to desertification environment. Horticulture Research, 2024, 11 (3) : 034 DOI:10.1093/hr/uhae034

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Acknowledgements

We would like to thank all authors for their valuable discussions. This work was financially supported by the Natural Science Foundation of China (32371838 and U1303101), the Bingtuan Science and Technology Program (2021BB010), and the Postgraduate Research and Innovation Project of Tarim University (TDBSCX202003).

Author contributions

J.H.S. performed investigation and writing-original draft. J.H.S. and J.D.X. performed formal analysis and visualization. C.Q., J.T.Z., S.H.Z., and X.Z. performed investigation. Z.H.W. performed project administration, acquisition of resources, and writing-review. Z.J.L. performed project administration, acquisition of resources, and funding acquisition. All authors revised and approved the final manuscript.

Data availability

The raw sequence reads (including short reads, long reads, and Hi-C reads) for the P. pruinosa genome, as well as the RNA-seq under salt and drought stress were submitted to NCBI (National Center for Biotechnology Information) with the BioProject accession number PRJNA863418. The assembly and annotation files were available from figshare (https://figshare.com/articles/online_resource/Pprgenome_fa/20705107/2). The whole-genome sequencing data for 156 P. pruinosa accessions also were uploaded to NCBI under the accession number PRJNA865525.

Conflict of interest statement

The authors declare no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Taylor G. Populus: arabidopsis for forestry. Do we need a model tree? Ann Bot. 2002; 90:681-9

[2]

Bradshaw HD, Ceulemans R, Davis J. et al. Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul. 2000; 19:306-13

[3]

Brunner AM, Busov VB, Strauss SH. Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci. 2004; 9:49-56

[4]

Dickmann DI, Kuzovkina J. In: Isebrands JG, Richardson J,eds. Poplars and Willows: Trees for Society and the Environment. Rome, Italy: CABI, 2014;15-6

[5]

Stettler RF, Bradshaw HD Jr, Heilman PE. et al. Biology of Populus and its Implications for Management and Conservation. Ottawa, Ontario, Canada: NRC Research Press, 1996;457-58

[6]

Zhang J, Feng J, Lu J. et al. Transcriptome differences between two sister desert poplar species under salt stress. BMC Genomics. 2014; 15:337

[7]

Wang J, Källman T, Liu J. et al. Speciation of two desert poplar species triggered by Pleistocene climatic oscillations. Heredity (Edinb). 2014; 112:156-64

[8]

Bruelheide H, Jandt U, Gries D. et al. Vegetation changes in a river oasis on the southern rim_of the Taklamakan Desert in China between 1956 and 2000. Phytocoenologia. 2003; 33:801-18

[9]

Li Y-H, Li D, Jiao YQ. et al. Identification of loci controlling adaptation in Chinese soya bean landraces via a combination of conventional and bioclimatic GWAS. Plant Biotechnol J. 2020; 18:389-401

[10]

Jiang X-L, Gardner EM, Meng H-H. et al. Land bridges in the Pleistocene contributed to flora assembly on the continental islands of South China: insights from the evolutionary history of Quercus championii. Mol Phylogenet Evol. 2019; 132:36-45

[11]

Yang W, Wang Y, Zhao Y. et al. The draft genome sequence of a desert tree Populus pruinosa. Gigascience. 2017; 6:1-7

[12]

Borthakur D, Busov V, Cao XH. et al. Current status and trends in forest genomics. Forestry Research. 2022; 2:11

[13]

Xue L, Wu H, Chen Y. et al. Evidences for a role of two Y-specific genes in sex determination in Populus deltoides. Nat Commun. 2020; 11:5893

[14]

Lin Y, Wang J, Delhomme N. et al. Functional and evolutionary genomic inferences in Populus through genome and population sequencing of American and European aspen. PNAS. 2018; 115:E10970-8

[15]

Ou S, Chen J, Jiang N. Assessing genome assembly quality using the LTR assembly index (LAI). Nucleic Acids Res. 2018; 46:e126

[16]

Murat F, Armero A, Pont C. et al. Reconstructing the genome of the most recent common ancestor of flowering plants. Nat Genet. 2017; 49:490-6

[17]

Wang X, Gao Y, Wu X. et al. High-quality evergreen azalea genome reveals tandem duplication-facilitated low-altitude adaptability and floral scent evolution. Plant Biotechnol J. 2021; 19:2544-60

[18]

Miao J, Feng Q, Li Y. et al. Chromosome-scale assembly and analysis of biomass crop Miscanthus lutarioriparius genome. Nat Commun. 2021; 12:2458

[19]

Park S-C, Lee JR, Shin SO. et al. Characterization of a heat-stable protein with antimicrobial activity from Arabidopsis thaliana. Biochem Biophys Res Commun. 2007; 362:562-7

[20]

Xu J, Zheng AQ, Xing XJ. et al. Transgenic Arabidopsis plants expressing grape glutathione S-transferase gene (VvGSTF13) show enhanced tolerance to abiotic stress. Biochemistry (Mosc). 2018; 83:755-65

[21]

Wagner U, Edwards R, Dixon DP. et al. Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol. 2002; 49:515-32

[22]

Mitsuya S, Taniguchi M, Miyake H. et al. Disruption of RCI2A leads to over-accumulation of Na+ and increased salt sensitivity in Arabidopsis thaliana plants. Planta. 2005; 222:1001-9

[23]

Medina J, Rodríguez-Franco M, Peñalosa A. et al. Arabidopsis mutants deregulated in RCI2A expression reveal new signaling pathways in abiotic stress responses. Plant J. 2005; 42:586-97

[24]

Rai AN, Tamirisa S, Rao KV. et al. Brassica RNA binding protein ERD4 is involved in conferring salt, drought tolerance and enhancing plant growth in Arabidopsis. Plant Mol Biol. 2016; 90:375-87

[25]

Ream TS, Woods DP, Schwartz CJ. et al. Interaction of photoperiod and vernalization determines flowering time of Brachypodium distachyon. Plant Physiol. 2014; 164:694-709

[26]

Sun X, Peng L, Guo J. et al. Formation of DEG5 and DEG8 complexes and their involvement in the degradation of photodamaged photosystem II reaction center D1 protein in Arabidopsis. Plant Cell. 2007; 19:1347-61

[27]

Xu Z-Y, Kim SY, Hyeon DY. et al. The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell. 2013; 25:4708-24

[28]

Zachos J, Pagani M, Sloan L. et al. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science. 2001; 292:686-93

[29]

Guo Z, Peng S, Hao Q. et al. Late Miocene-Pliocene development of Asian aridification as recorded in the Red-Earth Formation in northern China. Glob Planet Chang. 2004; 41:135-45

[30]

Santo SD, Stampfl H, Krasensky J. et al. Stress-induced GSK3 regulates the redox stress response by phosphorylating glucose-6-phosphate dehydrogenase in Arabidopsis. Plant Cell. 2012; 24:3380-92

[31]

Barroso C, Romero LC, Cejudo FJ. et al. Salt-specific regulation of the cytosolic O-acetylserine(thiol)lyase gene from Arabidopsis thaliana is dependent on abscisic acid. Plant Mol Biol. 1999; 40:729-36

[32]

Osakabe Y, Arinaga N, Umezawa T. et al. Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis. Plant Cell. 2013; 25:609-24

[33]

Yuenyong W, Sirikantaramas S, Qu L-J. et al. Isocitrate lyase plays important roles in plant salt tolerance. BMC Plant Biol. 2019; 19:472

[34]

Dubrovina AS, Aleynova OA, Manyakhin AY. et al. The role of calcium-dependent protein kinase genes CPK16, CPK25, CPK30, and CPK32 in stilbene biosynthesis and the stress resistance of grapevine Vitis amurensis Rupr. Appl Biochem Micro. 2018; 54:410-7

[35]

Patzke K, Prananingrum P, Klemens PAW. et al. The plastidic sugar transporter pSuT influences flowering and affects cold responses. Plant Physiol. 2019; 179:569-87

[36]

Pearson L, Pelling M.The UN Sendai framework for disaster risk reduction2015-2030: negotiation process and prospects for science and practice. J Extreme Events. 2015; 02:1571001

[37]

Weiland S, Hickmann T, Lederer M. et al. The 2030 agenda for sustainable development transformative change through the sustainable development goals. Pol Gov. 2021; 9:90-5

[38]

Zhao X, Guo X, Tang X. et al. Misregulation of ER-Golgi vesicle transport induces ER stress and affects seed vigor and stress response. Front Plant Sci. 2018; 9:658

[39]

Melgar J, Dunlop J, Albrigo L. et al. Winter drought stress can delay flowering and avoid immature fruit loss during late-season mechanical harvesting of ‘Valencia’ oranges. HortScience. 2010; 45:271-6

[40]

Earles JM, Stevens JT, Sperling O. et al. Extreme mid-winter drought weakens tree hydraulic-carbohydrate systems and slows growth. New Phytol. 2018; 219:89-97

[41]

Camarero JJ, Guada G, Sánchez-Salguero R. et al. Winter drought impairs xylem phenology, anatomy and growth in Mediterranean Scots pine forests. Tree Physiol. 2016; 36:1536-49

[42]

Wang J, Ding J. Molecular mechanisms of flowering phenology in trees. Forestry Research. 2023; 3:2

[43]

Berr A, Xu L, Gao J. et al. SET DOMAIN GROUP25 encodes a histone methyltransferase and is involved in FLOWERING LOCUS C activation and repression of flowering. Plant Physiol. 2009; 151:1476-85

[44]

Muellner-Riehl AN. Mountains as evolutionary arenas: patterns, emerging approaches, paradigm shifts, and their implications for plant phylogeographic research in the Tibeto-Himalayan region. Front Plant Sci. 2019; 10:195

[45]

Sang Y, Long Z, Dan X. et al. Genomic insights into local adaptation and future climate-induced vulnerability of a keystone forest tree in East Asia. Nat Commun. 2022; 13:6541

[46]

Müller NA, Kersten B, Leite Montalvão AP. et al. A single gene underlies the dynamic evolution of poplar sex determination. Nat Plants. 2020; 6:630-7

[47]

Belton J-M, McCord RP, Gibcus JH. et al. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods. 2012; 58:268-76

[48]

Liu B, Shi Y, Yuan J. et al. Estimation of genomic characteristics by analyzing k-mer frequency in de novo genome projects. Quant Biol. 2013; 35:62-7

[49]

Cheng H, Concepcion GT, Feng X. et al. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods. 2021; 18:170-5

[50]

Zhang X, Zhang S, Zhao Q. et al. Assembly of allele-aware, chromosomal-scale autopolyploid genomes based on hi-C data. Nat Plants. 2019; 5:833-45

[51]

Robinson JT, Turner D, Durand NC. et al. Juicebox.Js provides a cloud-based visualization system for hi-C data. Cell Syst. 2018; 6:256-258.e1

[52]

Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25:1754-60

[53]

Ou S, Jiang N. LTR_retriever: a highly accurate and sensitive program for identification of long terminal repeat retrotransposons. Plant Physiol. 2018; 176:1410-22

[54]

Xu Z, Wang H. LTR_FINDER: an efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Res. 2007; 35:W265-8

[55]

Simão FA, Waterhouse RM, Ioannidis P. et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31:3210-2

[56]

Rhie A, Walenz BP, Koren S. et al. Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies. Genome Biol. 2020; 21:245

[57]

Tarailo-Graovac M, Chen N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr Protoc Bioinformatics. 2009; 25:4.10.11-14.10.14

[58]

Beier S, Thiel T, Münch T. et al. MISA-web: a web server for microsatellite prediction. Bioinformatics. 2017; 33:2583-5

[59]

Zhou R, Macaya-Sanz D, Carlson CH. et al. A willow sex chromosome reveals convergent evolution of complex palindromic repeats. Genome Biol. 2020; 21:38

[60]

Wei S, Yang Y, Yin T. The chromosome-scale assembly of the willow genome provides insight into Salicaceae genome evolution. Hortic Res. 2020; 7:45

[61]

Tuskan GA, DiFazio S, Jansson S. et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006; 313:1596-604

[62]

Ma J, Wan D, Duan B. et al. Genome sequence and genetic transformation of a widely distributed and cultivated poplar. Plant Biotechnol J. 2019; 17:451-60

[63]

Camacho C, Coulouris G, Avagyan V. et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009; 10:421

[64]

Birney E, Clamp M, Durbin R. GeneWise and Genomewise. Genome Res. 2004; 14:988-95

[65]

Stanke M, Steinkamp R, Waack S. et al. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 2004; 32:W309-12

[66]

Alioto T, Blanco E, Parra G. et al. Using geneid to identify genes. Curr Protoc Bioinformatics. 2018; 64:e56

[67]

Burge C, Karlin S. Prediction of complete gene structures in human genomic DNA. J Mol Biol. 1997; 268:78-94

[68]

Majoros WH, Pertea M, Salzberg SL. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics. 2004; 20:2878-9

[69]

Korf I. Gene finding in novel genomes. BMC Bioinformatics. 2004; 5:59

[70]

Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015; 12:357-60

[71]

Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25:1105-11

[72]

Pertea M, Pertea GM, Antonescu CM. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015; 33:290-5

[73]

Trapnell C, Roberts A, Goff L. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and cufflinks. Nat Protoc. 2012; 7:562-78

[74]

Haas BJ, Salzberg SL, Zhu W. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol. 2008; 9:R7

[75]

Campbell MA, Haas BJ, Hamilton JP. et al. Comprehensive analysis of alternative splicing in rice and comparative analyses with Arabidopsis. BMC Genomics. 2006; 7:327

[76]

Marchler-Bauer A, Lu S, Anderson JB. et al. CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 2011; 39:D225-9

[77]

Boeckmann B, Bairoch A, Apweiler R. et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 2003; 31:365-70

[78]

Mount DW. Using the basic local alignment search tool (BLAST). CSH Protoc. 2007; 2007:pdb.top17

[79]

Finn RD, Mistry J, Schuster-Böckler B. et al. Pfam: clans, web tools and services. Nucleic Acids Res. 2006; 34:D247-51

[80]

Mistry J, Finn RD, Eddy SR. et al. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 2013; 41:e121

[81]

Griffiths-Jones S, Moxon S, Marshall M. et al. Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res. 2005; 33:D121-4

[82]

Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013; 29:2933-5

[83]

Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997; 25:955-64

[84]

Wang Y, Tang H, DeBarry JD. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40:e49

[85]

Ellinghaus D, Kurtz S, Willhoeft U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics. 2008; 9:18

[86]

Zhang S, Wu Z, Ma D. et al. Chromosome-scale assemblies of the male and female Populus euphratica genomes reveal the molecular basis of sex determination and sexual dimorphism. Commun Biol. 2022; 5:1186

[87]

Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24:1586-91

[88]

Yu G, Wang L-G, Han Y. et al. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS. 2012; 16:284-7

[89]

Kim D, Paggi JM, Park C. et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019; 37:907-15

[90]

Pertea M, Kim D, Pertea GM. et al. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016; 11:1650-67

[91]

Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015; 16:157

[92]

Nguyen L-T, Schmidt HA, Haeseler A. et al. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015; 32:268-74

[93]

Rannala B, Yang Z. Inferring speciation times under an episodic molecular clock. Syst Biol. 2007; 56:453-66

[94]

Manchester SR, Judd WS, Handley B. Foliage and fruits of early poplars (Salicaceae: Populus) from the Eocene of Utah, Colorado, and Wyoming. Int J Plant Sci. 2006; 167:897-908

[95]

Dai X, Hu Q, Cai Q. et al. The willow genome and divergent evolution from poplar after the common genome duplication. Cell Res. 2014; 24:1274-7

[96]

Zhang L, Xi Z, Wang M. et al. Plastome phylogeny and lineage diversification of Salicaceae with focus on poplars and willows. Ecol Evol. 2018; 8:7817-23

[97]

Han MV, Thomas GWC, Lugo-Martinez J. et al. Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. Mol Biol Evol. 2013; 30:1987-97

[98]

Chen S, Zhou Y, Chen Y. et al. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34:i884-90

[99]

Li H, Handsaker B, Wysoker A. et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25:2078-9

[100]

DePristo MA, Banks E, Poplin R. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011; 43:491-8

[101]

Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010; 38:e164

[102]

Manichaikul A, Mychaleckyj JC, Rich SS. et al. Robust relationship inference in genome-wide association studies. Bioinformatics. 2010; 26:2867-73

[103]

Raj A, Stephens M, Pritchard JK. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics. 2014; 197:573-89

[104]

Purcell S, Neale B, Todd-Brown K. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007; 81:559-75

[105]

Kumar S, Stecher G, Li M. et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018; 35:1547-9

[106]

Zhang C, Dong S-S, Xu J-Y. et al. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics. 2019; 35:1786-8

[107]

Terhorst J, Kamm JA, Song YS. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat Genet. 2017; 49:303-9

[108]

Frichot E, François O. LEA: an R package for landscape and ecological association studies. Methods Ecol Evol. 2015; 6:925-9

[109]

Forester BR, Lasky JR, Wagner HH. et al. Comparing methods for detecting multilocus adaptation with multivariate genotype-environment associations. Mol Ecol. 2018; 27:2215-33

[110]

Ellis N, Smith SJ, Pitcher CR. Gradient forests: calculating importance gradients on physical predictors. Ecology. 2012; 93:156-68

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