Abstract
Key message
Measuring transcript levels for adaptive genes revealed polymorphisms having cis -effect upon gene expression levels related to phenotype variation in a black spruce natural population.
Abstract
Trees growing in temperate and boreal regions must acclimate to changes in climatic factors such as low winter temperatures to survive to seasonal variations. Common garden studies have shown that genetic variation in quantitative traits helps species to survive and adapt to environmental changes and local conditions. Twenty-four genes carrying SNPs were previously associated with genetic adaptation in black spruce (Picea mariana [Mill.] BSP). The objectives of this study were to investigate the potential role of these genes in regulation of winter acclimation and adaptation by studying their patterns of expression as a function of the physiological stage during the annual growth cycle, tissue type, and their SNP genotypic class. Considerable variability in gene expression was observed between different vegetative tissues or organs, and between physiological stages. The genes were expressed predominantly in tissues that could be linked more directly to winter acclimation and adaptation. The expression levels of several of the genes were significantly related to variation in tree height growth or budset timing and expression level variation related to SNP genotypic classes was observed in four of the genes. An interaction between genotypic classes and physiological stages was also observed for some genes, indicating genotypes with different reaction norms in terms of gene expression.
Similar content being viewed by others
References
Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326
Beaulieu J, Perron M, Bousquet J (2004) Multivariate patterns of adaptive genetic variation and seed source transfer in Picea mariana. Can J For Res 34:531–545
Bigras F, Colombo SJ (2001) Conifer cold hardiness. Kluwer Academic Publishers, Dordrecht
Boyle B, Dallaire N, MacKay J (2009) Evaluation of the impact of single nucleotide polymorphisms and primer mismatches on quantitative PCR. BMC Biotechnol 9:75
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116
Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160
Clutter ME (2013) Dormancy and developmental arrest: experimental analysis in plants and animals. Elsevier, London
Du F, Xu JN, Li D, Wang XY (2014) The identification of novel and differentially expressed apple-tree genes under low-temperature stress using high-throughput Illumina sequencing. Mol Biol Rep:1–12
Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, St Clair JBS, Neale DB (2009a) Asssociation genetics of coastal Douglas fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics 182:1289–1302
Eckert AJ, Wegrzyn JL, Pande B, Jermstad KD, Lee JM, Liechty JD, Tearse BR, Krutovsky KV, Neale DB (2009b) Multilocus patterns of nucleotide diversity and divergence reveal positive selection at candidate genes related to cold Hardiness in coastal Douglas Fir (Pseudotsuga menziesii var. menziesii). Genetics 183:289–298
Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95:14863–14868
El Kayal W, Allen CCG, Ju CJT, Adams E, King-Jones S, Zaharia LI, Abrams SR, Cooke JEK (2011) Molecular events of apical bud formation in white spruce, Picea glauca. Plant Cell Environ 34:480–500
Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM, Mohan J, Orwig DA, Rodenhouse NL, Sobczak WV, Stinson KA, Stone JK, Swan CM, Thompson J, Von Holle B, Webster JR (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486
Eveno E, Collada C, Guevara MA, Leger V, Soto A, Diaz L, Leger P, Gonzalez-Martinez SC, Cervera MT, Plomion C, Garnier-Gere PH (2008) Contrasting patterns of selection at Pinus pinaster Ait. Drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25:417–437
Farrar JL (1995) Trees in Canada. FIDES & Canadian Forest Service
Frewen BE, Chen THH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845
Gérardi S, Jaramillo-Correa JP, Beaulieu J, Bousquet J (2010) From glacial refugia to modern populations: new assemblages of organelle genomes generated by differential cytoplasmic gene flow in transcontinental black spruce. Mol Ecol 19:5265–5280
Groh B, Hübner C, Lendzian KJ (2002) Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels. Planta 215:794–801
Groover A, Robischon M (2006) Developmental mechanisms regulating secondary growth in woody plants. Curr Opin Plant Biol 9:55–58
Hall D, Luquez V, Garcia VM, St Onge KR, Jansson S, Ingvarsson PK (2007) Adaptive population differentiation in phenology across a latitudinal gradient in European aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes and phenotypic traits. Evolution 61:2849–2860
Holliday JA, Ralph SG, White R, Bohlmann J, Aitken SN (2008) Global monitoring of autumn gene expression within and among phenotypically divergent populations of Sitka spruce (Picea sitchensis). New Phytol 178:103–122
Holliday JA, Ritland K, Aitken SN (2010) Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis). New Phytol 188:501–514
Howe G, Saruul P, Davis J, Chen T (2000) Quantitative genetics of bud phenology, frost damage, and winter survival in an F2 family of hybrid poplars. Theor Appl Genet 101:632–642
Huang J, Wang JF, Wang QH, Zhang HS (2005) Identification of a rice zinc finger protein whose expression is transiently induced by drought, cold but not by salinity and abscisic acid. Mitochondrial DNA 16:130–136
Hurme P, Repo T, Savolainen O, Paakkonen T (1997) Climatic adaptation of bud set and frost hardiness in Scots pine (Pinus sylvestris). Can J For Res 27:716–723
Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S (2008) Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics 178:2217–2226
Iuchi S (2001) Three classes of C2H2 zinc finger proteins. Cell Mol Life Sci CMLS 58:625–635
Jaramillo-Correa JP, Beaulieu J, Bousquet J (2001) Contrasting evolutionary forces driving population structure at expressed sequence tag polymorphisms, allozymes and quantitative traits in white spruce. Mol Ecol 10:2729–2740
Jaramillo-Correa JP, Prunier J, Vázquez-Lobo A, Keller SR, Moreno-Letelier A (2015) Molecular signatures of adaptation and selection in forest trees. Advances in Botanical Research
Kim WY, Kim JY, Jung HJ, Oh SH, Han YS, Kang H (2010) Comparative analysis of Arabidopsis zinc finger-containing glycine-rich RNA-binding proteins during cold adaptation. Plant Physiol Biochem 48:866–872
Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189
Lang GA, Early JD, Martin GC, Darnell RL (1987) Endodormancy, paradormancy, and ecodormancy—physiological terminology and classification for dormancy research. HortScience 22:371–377
Lemos B, Araripe LO, Fontanillas P, Hartl DL (2008) Dominance and the evolutionary accumulation of cis-and trans-effects on gene expression. Proc Natl Acad Sci 105:14471–14476
Li P, Beaulieu J, Corriveau A, Bousquet J (1993) Genetic-variation in juvenile growth and phenology in a white spruce provenance progeny test. Silvae Genet 42:52–60
Li P, Beaulieu J, Bousquet J (1997) Genetic structure and patterns of genetic variation among populations in eastern white spruce (Picea glauca). Can J For Res 27:189–198
Machado A, Pereira H, Teixeira RT (2013) Anatomy and development of the endodermis and phellem of quercus suber L. roots. Microsc Microanal 19:525–534
Martin L, Leblanc-Fournier N, Azri W, Lenne C, Henry C, Coutand C, Julien J-L (2009) Characterization and expression analysis under bending and other abiotic factors of PtaZFP2, a poplar gene encoding a Cys2/His2 zinc finger protein. Tree Physiol 29:125–136
Morgenstern EK (1969) Genetic variation in seedlings of picea mariana (Mill.) BSP: I. Correlation with ecological factors. Silvae Genet 18:151–167
Namroud MC, Beaulieu J, Juge N, Laroche J, Bousquet J (2008) Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Mol Ecol 17:3599–3613
Pavy N, Boyle B, Nelson C, Paule C, Giguère I, Caron S, Parsons LS, Dallaire N, Bedon F, Bérubé H (2008) Identification of conserved core xylem gene sets: conifer cDNA microarray development, transcript profiling and computational analyses. New Phytol 180:766–786
Pelgas B, Bousquet J, Meirmans PG, Ritland K, Isabel N (2011) QTL mapping in white spruce: gene maps and genomic regions underlying adaptive traits across pedigrees, years and environments. BMC Genom 12:145
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Prunier J, Laroche J, Beaulieu J, Bousquet J (2011) Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Mol Ecol 20:1702–1716
Prunier J, Gerardi S, Laroche J, Beaulieu J, Bousquet J (2012) Parallel and lineage-specific molecular adaptation to climate in boreal black spruce. Mol Ecol 21:4270–4286
Prunier J, Pelgas B, Gagnon F, Desponts M, Isabel N, Beaulieu J, Bousquet J (2013) The genomic architecture and association genetics of adaptive characters using a candidate SNP approach in boreal black spruce. BMC Genom 14:368
Prunier J, Verta JP, MacKay JJ (2015) Conifer genomics and adaptation: at the crossroads of genetic diversity and genome function. New Phytol
Reitz MU, Bissue JK, Zocher K, Attard A, Hückelhoven R, Becker K, Imani J, Eichmann R, Schäfer P (2012) The subcellular localization of Tubby-like proteins and participation in stress signaling and root colonization by the mutualist Piriformospora indica. Plant Physiol 160:349–364
Rigault P, Boyle B, Lepage P, Cooke JEK, Bousquet J, MacKay J (2011) A white spruce gene catalog for conifer genome analyses. Plant Physiol 157:14–28
Rinne P, Welling A, Kaikuranta P (1998) Onset of freezing tolerance in birch (Betula pubescens Ehrh.) involves LEA proteins and osmoregulation and is impaired in an ABA-deficient genotype. Plant Cell Environ 21:601–611
Ripley B, Hornik K, Gebhardt A, Firth D (2012) Functions and datasets to support Venables and Ripley, ‘Modern Applied Statistics with S’ (2002): package “MASS”. http://cranr-project.org
Rodriguez Milla MA, Townsend J, Chang F, Cushman JC (2006) The Arabidopsis AtDi19 gene family encodes a novel type of Cys2/His2 zinc-finger protein implicated in ABA-independent dehydration, high-salinity stress and light signaling pathways. Plant Mol Biol 61:13–30
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223
Rohde A, Ruttink T, Hostyn V, Sterck L, Van Driessche K, Boerjan W (2007) Gene expression during the induction, maintenance, and release of dormancy in apical buds of poplar. J Exp Bot 58:4047–4060
Rutledge RG, Stewart D (2008) Critical evaluation of methods used to determine amplification efficiency refutes the exponential character of real-time PCR. BMC Mol Biol 9:96
Ruttink T, Arend M, Morreel K, Storme V, Rombauts S, Fromm J, Bhalerao RP, Boerjan W, Rohde A (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell Online 19:2370–2390
Saeed A, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374
Sakai A, Larcher W (1987) Frost survival of plants. Responses and adaptation to freezing stress. Springer, Berlin
Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746
Schrader J, Moyle R, Bhalerao R, Hertzberg M, Lundeberg J, Nilsson P, Bhalerao RP (2004) Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome. Plant J 40:173–187
Schreiber L, Hartmann K, Skrabs M, Zeier J (1999) Apoplastic barriers in roots: chemical composition of endodermal and hypodermal cell walls. J Exp Bot 50:1267–1280
Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell Online 13:61–72
Shukla RK, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol 142:113–123
Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688
Torii KU (2004) Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol 234:1–46
Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3
Viereck L, Johnston W (1990) Picea mariana (Mill.) BSP, Black spruce. In: Silvics of North America. USDA, pp 227–237
Welling A, Palva ET (2006) Molecular control of cold acclimation in trees. Physiol Plant 127:167–181
Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell Online 14:S165–S183
Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot:2541–2556
Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6:486–503
Acknowledgments
We thank Brian Boyle, Isabelle Giguère, and Sébastien Caron for assistance with lab work, as well as Claude Bomal for fruitful discussion during the study design. We also thank Martin Perron and Armand Seguin for comments on the first manuscript. This work was supported by a Grant from the Fonds de Recherche du Québec—Nature et Technologies (FRQNT) attributed to Jean Bousquet and John MacKay. We also thank two anonymous reviewers for their insightful comments upon the first version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by M. C. Jordan.
J. Prunier and G. Tessier contributed equally to the work as co-first authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Prunier, J., Tessier, G., Bousquet, J. et al. From genotypes to phenotypes: expression levels of genes encompassing adaptive SNPs in black spruce. Plant Cell Rep 34, 2111–2125 (2015). https://doi.org/10.1007/s00299-015-1855-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-015-1855-0