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Allelic variation in PtoPsbW associated with photosynthesis, growth, and wood properties in Populus tomentosa

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Abstract

Photosynthesis is one of the most important reactions on earth. PsbW, a nuclear-encoded subunit of photosystem II (PSII), stabilizes PSII structure and plays an important role in photosynthesis. Here, we used candidate gene-based linkage disequilibrium (LD) mapping to detect significant associations between allelic variations of PtoPsbW and traits related to photosynthesis, growth, and wood properties in Populus tomentosa. PtoPsbW showed the highest expression in leaves and it increased during the development of these leaves, suggesting that PtoPsbW may play an important role in plant growth and development. Analysis of nucleotide diversity and LD revealed that PtoPsbW has low single-nucleotide polymorphism (SNP) diversity (π tot = 0.0048 and θ w = 0.0050) and relatively low average value of LD (0.1500), indicating that PtoPsbW is conserved due to its indispensable function. Using single-SNP associations in an association population of 435 individuals, we identified five significant associations at the threshold of P ≤ 0.05, explaining 3.28–15.98 % of the phenotypic variation. Haplotype-based association analyses indicated that 13 haplotypes (P ≤ 0.05) from six blocks were associated with photosynthesis, growth, and wood properties. Our work shows that identifying allelic variation and LD can help to decipher the genetic basis of photosynthesis and could potentially be applied for molecular marker-assisted selection in Populus.

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References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barber J (2005) Engine of life and big bang of evolution: a personal perspective. In: Discoveries in photosynthesis. Springer, pp 283–301

  • Barber J (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34:619–632

    Article  CAS  PubMed  Google Scholar 

  • Beaulieu J, Doerksen T, Boyle B, Clément S, Deslauriers M, Beauseigle S, Blais S, Poulin P-L, Lenz P, Caron S (2011) Association genetics of wood physical traits in the conifer white spruce and relationships with gene expression. Genetics 188:197–214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop CL, Purton S, Nugent JH (2003) Molecular analysis of the Chlamydomonas nuclear gene encoding PsbW and demonstration that PsbW is a subunit of photosystem II, but not photosystem I. Plant Mol Biol 52:285–289

    Article  CAS  PubMed  Google Scholar 

  • Chang J, Zhang J, Mao X, Li A, Jia J, Jing R (2013) Polymorphism of TaSAP1-A1 and its association with agronomic traits in wheat. Planta 237:1495–1508

    Article  CAS  PubMed  Google Scholar 

  • Chu Y, Su X, Huang Q, Zhang X (2009) Patterns of DNA sequence variation at candidate gene loci in black poplar (Populus nigra L.) as revealed by single nucleotide polymorphisms. Genetica 137:141–150

    Article  CAS  PubMed  Google Scholar 

  • Chu Y, Huang Q, Zhang B, Ding C, Su X (2014) Expression and molecular evolution of two DREB1 genes in black poplar (Populus nigra). PLoS ONE 9:e98334

    Article  PubMed  PubMed Central  Google Scholar 

  • d’Alésio A, Garabédian M, Sabatier JP, Guaydier-Souquières G, Marcelli C, Lemaçon A, Walrant-Debray O, Jehan F (2005) Two single-nucleotide polymorphisms in the human vitamin D receptor promoter change protein–DNA complex formation and are associated with height and vitamin D status in adolescent girls. Hum Mol Genet 14:3539–3548

    Article  PubMed  Google Scholar 

  • Dillon SK, Nolan M, Li W, Bell C, Wu HX, Southerton SG (2010) Allelic variation in cell wall candidate genes affecting solid wood properties in natural populations and land races of Pinus radiata. Genetics 185:1477–1487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dillon SK, Brawner JT, Meder R, Lee DJ, Southerton SG (2012) Association genetics in Corymbia citriodora subsp. variegata identifies single nucleotide polymorphisms affecting wood growth and cellulosic pulp yield. New Phytol 195:596–608

    Article  CAS  PubMed  Google Scholar 

  • Du Q, Wang B, Wei Z, Zhang D, Li B (2012) Genetic diversity and population structure of Chinese white poplar (Populus tomentosa) revealed by SSR markers. J Heredity ess061

  • Du Q, Pan W, Xu B, Li B, Zhang D (2013a) Polymorphic simple sequence repeat (SSR) loci within cellulose synthase (PtoCesA) genes are associated with growth and wood properties in Populus tomentosa. New Phytol 197:763–776

    Article  CAS  PubMed  Google Scholar 

  • Du Q, Xu B, Pan W, Gong C, Wang Q, Tian J, Li B, Zhang D (2013b) Allelic variation in a cellulose synthase gene (PtoCesA4) associated with growth and wood properties in Populus tomentosa. G3: Genes| Genomes|. Genetics 3:2069–2084

    Google Scholar 

  • Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, Clair JBS, Neale DB (2009) Association genetics of coastal Douglas fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics 182:1289–1302

    CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Faivre-Rampant P, Zaina G, Jorge V, Giacomello S, Segura V, Scalabrin S, Guérin V, De Paoli E, Aluome C, Viger M (2016) New resources for genetic studies in Populus nigra: genome-wide SNP discovery and development of a 12 k Infinium array. Mol Ecol Resour

  • Fang X, Xu H, Zhang C, Zhang J, Lan X, Gu C, Hong C (2010) Polymorphisms in BMP-2 gene and their associations with growth traits in goats. Genes Genom 32:29–35

    Article  Google Scholar 

  • Funk C, Shi L, Schröder W (1995) Functional studies on the newly discovered 6.1 kDa protein from spinach thylakoids. Photosynth Light Biosphere 3:329–332

  • García-Cerdán JG, Kovács L, Tóth T, Kereïche S, Aseeva E, Boekema EJ, Mamedov F, Funk C, Schröder WP (2011) The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants. Plant J 65:368–381

    Article  PubMed  Google Scholar 

  • Guerra FP, Wegrzyn JL, Sykes R, Davis MF, Stanton BJ, Neale DB (2013) Association genetics of chemical wood properties in black poplar (Populus nigra). New Phytol 197:162–176

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hetherington SE, He J, Smillie RM (1989) Photoinhibition at low temperature in chilling-sensitive and-resistant plants. Plant Physiol 90:1609–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hill W, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231

    Article  CAS  PubMed  Google Scholar 

  • Ingvarsson PK (2005a) Molecular population genetics of herbivore-induced protease inhibitor genes in European aspen (Populus tremula L., Salicaceae). Mol Biol Evol

  • Ingvarsson PK (2005b) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irrgang K-D, Shi L-X, Funk C, Schröder WP (1995) A nuclear-encoded subunit of the photosystem II reaction center. J Biol Chem 270:17588–17593

    Article  CAS  PubMed  Google Scholar 

  • Jiang R, Tavaré S, Marjoram P (2009) Population genetic inference from resequencing data. Genetics 181:187–197

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim SJ, Robinson C, Mant A (1998) Sec/SRP-independent insertion of two thylakoid membrane proteins bearing cleavable signal peptides. FEBS Lett 424:105–108

    Article  CAS  PubMed  Google Scholar 

  • Li X, Wu HX, Dillon SK, Southerton SG (2009) Generation and analysis of expressed sequence tags from six developing xylem libraries in Pinus radiata D. Don. BMC Genom 10:41

    Article  CAS  Google Scholar 

  • Li Y, Xu B, Du Q, Zhang D (2015) Transcript abundance patterns of Populus C-repeat binding factor2 orthologs and genetic association of PsCBF2 allelic variation with physiological and biochemical traits in response to abiotic stress. Planta 242:295–312

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lorković Z, Schröder W, Pakrasi H, Irrgang K, Herrmann R, Oelmüller R (1995) Molecular characterization of PsbW, a nuclear-encoded component of the photosystem II reaction center complex in spinach. Proc Natl Acad Sci 92:8930–8934

    Article  PubMed  PubMed Central  Google Scholar 

  • Maestrini P, Cavallini A, Rizzo M, Giordani T, Bernardi R, Durante M, Natali L (2009) Isolation and expression analysis of low temperature-induced genes in white poplar (Populus alba). J Plant Physiol 166:1544–1556

    Article  CAS  PubMed  Google Scholar 

  • Makino A (2011) Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiol 155:125–129

    Article  CAS  PubMed  Google Scholar 

  • Marroni F, Pinosio S, Zaina G, Fogolari F, Felice N, Cattonaro F, Morgante M (2011) Nucleotide diversity and linkage disequilibrium in Populus nigra cinnamyl alcohol dehydrogenase (CAD4) gene. Tree Genet Genomes 7:1011–1023

    Article  Google Scholar 

  • McKown AD, Klápště J, Guy RD, Geraldes A, Porth I, Hannemann J, Friedmann M, Muchero W, Tuskan GA, Ehlting J (2014) Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa. New Phytol 203:535–553

    Article  CAS  PubMed  Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta (BBA)-Bioenerg 1767:414–421

  • Nasu S, Suzuki J, Ohta R, Hasegawa K, Yui R, Kitazawa N, Monna L, Minobe Y (2002) Search for and analysis of single nucleotide polymorphisms (SNPs) in rice (Oryza sativa, Oryza rufipogon) and establishment of SNP markers. DNA Res 9:163–171

    Article  CAS  PubMed  Google Scholar 

  • Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122

    Article  CAS  PubMed  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics Columbia University. New York, USA, New York

    Google Scholar 

  • Olson MS, Robertson AL, Takebayashi N, Silim S, Schroeder WR, Tiffin P (2010) Nucleotide diversity and linkage disequilibrium in balsam poplar (Populus balsamifera). New Phytol 186:526–536

    Article  PubMed  Google Scholar 

  • Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127:1513–1523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porth I, Klapšte J, Skyba O, Hannemann J, McKown AD, Guy RD, DiFazio SP, Muchero W, Ranjan P, Tuskan GA (2013) Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. New Phytol 200:710–726

    Article  CAS  PubMed  Google Scholar 

  • Ritland K (1996) Estimators for pairwise relatedness and individual inbreeding coefficients. Genet Res 67:175–185

    Article  Google Scholar 

  • Sharp RE, Boyer JS (1986) Photosynthesis at low water potentials in sunflower: lack of photoinhibitory effects. Plant Physiol 82:90–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi L-X, Lorković ZJ, Oelmüller R, Schröder WP (2000) The low molecular mass PsbW protein is involved in the stabilization of the dimeric photosystem II complex in Arabidopsis thaliana. J Biol Chem 275:37945–37950

    Article  CAS  PubMed  Google Scholar 

  • Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA (2012) Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 196:713–725

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Ci D, Tian M, Zhang D (2014) Comparison of the physiological effects and transcriptome responses of Populus simonii under different abiotic stresses. Plant Mol Biol 86:139–156

    Article  CAS  PubMed  Google Scholar 

  • Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247

    Article  CAS  Google Scholar 

  • Southerton S, MacMillan C, Bell J, Bhuiyan N, Dowries G, Ravenwood I, Joyce K, Williams D, Thumma B (2010) Association of allelic variation in xylem genes with wood properties in Eucalyptus nitens. Aust For 73:259–264

    Article  Google Scholar 

  • Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Human Genet 76:449–462

    Article  CAS  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci 100:9440–9445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thidholm E, Shi L-X, Schroder W (2001) The PsbW-protien. Its location and involvement in photoinhibition, Science Access, p 3

    Google Scholar 

  • Thidholm E, Lindström V, Tissier C, Robinson C, Schröder WP, Funk C (2002) Novel approach reveals localisation and assembly pathway of the PsbS and PsbW proteins into the photosystem II dimer. FEBS Lett 513:217–222

    Article  CAS  PubMed  Google Scholar 

  • Thompson SJ, Kim SJ, Robinson C (1998) Sec-independent insertion of thylakoid membrane proteins. Analysis of insertion forces and identification of a loop intermediate involving the signal peptide. J Biol Chem 273:18979–18983

    Article  CAS  PubMed  Google Scholar 

  • Thumma BR, Nolan MF, Evans R, Moran GF (2005) Polymorphisms in cinnamoyl CoA reductase (CCR) are associated with variation in microfibril angle in Eucalyptus spp. Genetics 171:1257–1265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thumma BR, Matheson BA, Zhang D, Meeske C, Meder R, Downes GM, Southerton SG (2009) Identification of a cis-acting regulatory polymorphism in a eucalypt COBRA-like gene affecting cellulose content. Genetics 183:1153–1164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian J, Chang M, Du Q, Xu B, Zhang D (2014) Single-nucleotide polymorphisms in PtoCesA7 and their association with growth and wood properties in Populus tomentosa. Mol Genet Genomics 289:439–455

    Article  CAS  PubMed  Google Scholar 

  • Tian J, Chen J, Li B, Zhang D (2016a) Association genetics in Populus reveals the interactions between Pto-miR160a and its target Pto-ARF16. Mol Genet Genomics 291:1069–1082

    Article  CAS  PubMed  Google Scholar 

  • Tian J, Song Y, Du Q, Yang X, Ci D, Chen J, Xie J, Li B, Zhang D (2016b) Population genomic analysis of gibberellin-responsive long non-coding RNAs in Populus. J Exp Bot erw057

  • Vanholme B, Cesarino I, Goeminne G, Kim H, Marroni F, Acker R, Vanholme R, Morreel K, Ivens B, Pinosio S (2013) Breeding with rare defective alleles (BRDA): a natural Populus nigra HCT mutant with modified lignin as a case study. New Phytol 198:765–776

    Article  CAS  PubMed  Google Scholar 

  • VanLiere JM, Rosenberg NA (2008) Mathematical properties of the r 2 measure of linkage disequilibrium. Theor Popul Biol 74:130–137

    Article  PubMed  PubMed Central  Google Scholar 

  • Watterson G (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276

    Article  CAS  PubMed  Google Scholar 

  • Wegrzyn JL, Eckert AJ, Choi M, Lee JM, Stanton BJ, Sykes R, Davis MF, Tsai CJ, Neale DB (2010) Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol 188:515–532

    Article  CAS  PubMed  Google Scholar 

  • Weickert C, Tiwari Y, Schofield P, Mowry B, Fullerton J (2012) Schizophrenia-associated HapICE haplotype is associated with increased NRG1 type III expression and high nucleotide diversity. Translat Psychiatr 2:e104

    Article  CAS  Google Scholar 

  • Xu N, Chen C, Shyu A-B (1997) Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol Cell Biol 17:4611–4621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu N, Loflin P, Chen C-YA, Shyu A-B (1998) A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy. Nucleic Acids Res 26:558–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  CAS  PubMed  Google Scholar 

  • Zaykin DV, Westfall PH, Young SS, Karnoub MA, Wagner MJ, Ehm MG (2002) Testing association of statistically inferred haplotypes with discrete and continuous traits in samples of unrelated individuals. Hum Hered 53:79–91

    Article  PubMed  Google Scholar 

  • Zhang D, Du Q, Xu B, Zhang Z, Li B (2010a) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genomics 284:105–119

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Yang X, Zhang Z, Li B (2010b) Expression and nucleotide diversity of the poplar COBL gene. Tree Genet Genomes 6:331–344

    Article  Google Scholar 

  • Zhang D, Xu B, Yang X, Zhang Z, Li B (2011) The sucrose synthase gene family in Populus: structure, expression, and evolution. Tree Genet Genomes 7:443–456

    Article  Google Scholar 

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Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China

    Longxin Wang, Bowen Wang, Qingzhang Du, Jinhui Chen, Jiaxing Tian, Xiaohui Yang & Deqiang Zhang

  2. Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China

    Longxin Wang, Bowen Wang, Qingzhang Du, Jinhui Chen, Jiaxing Tian, Xiaohui Yang & Deqiang Zhang

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  1. Longxin Wang
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  2. Bowen Wang
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  3. Qingzhang Du
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  4. Jinhui Chen
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  5. Jiaxing Tian
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  6. Xiaohui Yang
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Correspondence to Deqiang Zhang.

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This study was funded by the Fundamental Research Funds for Central Universities (No. 2015ZCQ-SW-01), and Shandong Province Agriculture Improved Variety Project (No. 2012213).

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Wang, L., Wang, B., Du, Q. et al. Allelic variation in PtoPsbW associated with photosynthesis, growth, and wood properties in Populus tomentosa . Mol Genet Genomics 292, 77–91 (2017). https://doi.org/10.1007/s00438-016-1257-1

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