Abstract
The ecologically dominant and economically important genus Populus, with its available full genome sequence, has become an ideal woody species for genomic study. Rapid growth is one of the primary advantageous features of Populus, and extensive physiological research has been carried out on the growth of Populus throughout the growing period among different clones. However, the molecular information related to the mechanisms of rapid growth is rather limited. In this study, an Affymetrix poplar genome array was employed to analyze the transcriptomic changes from the pre-growth to the fast-growth phase in two poplar clones (P.deltoides × P.nigra, DN2, and P.nigra × (P.deltoides × P. nigra), NE19) with different growth rates. A total of 1,695 differently expressed genes were identified between two time points in NE19 and DN2 (two-way ANOVA, P < 0.01 and fold change ≥2). Except for genes changing in common for both clones, many transcripts were regulated specifically in one genotype. After functional analysis of the differentially expressed genes, distinct biological strategies seemed to be utilized by the two genotypes to accommodate their fast-growth phase. The faster-growing clone NE19, which has a higher photosynthetic rate and larger total leaf area, emphasized growth-related primary metabolism. However, the slower-growing DN2 tended to have more up-regulated genes involved in defense-related secondary metabolism and stress response. Emphasis of such divergent biological processes in two clones may explain their significant growth differences during the fast-growth phase.
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Abbreviations
- ABA:
-
Abscisic acid
- ANOVA:
-
Analysis of variance
- BR:
-
Brassinolide
- CTK:
-
Cytokinin
- DPTF:
-
The database of poplar transcription factor
- ETH:
-
Ethylene
- GA:
-
Gibberellin
- IAA:
-
Indole-3-acetic acid
- JA:
-
Jasmonic acid
- JGI:
-
Joint Genome Institute
- PS I:
-
Photosystem I
- PS II:
-
Photosystem II
- PlnTFDB:
-
Plant transcription factor database
- qRT-PCR:
-
Real-time quantitative reverse transcription PCR
- SA:
-
Salicylic acid
- TAIR:
-
The Arabidopsis information resource
References
Anderson GH, Veit B, Hanson MR (2005) The Arabidopsis AtRaptor genes are essential for post-embryonic plant growth. BMC Biol 3:12. doi:10.1186/1741-7007-3-12
Ashburner M, Ball CA, Blake JA et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25(1):25–29
Autran D, Jonak C, Belcram K, Beemster GT, Kronenberger J, Grandjean O, Inzé D, Traas J (2002) Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21(22):6036–6049. doi:10.1093/emboj/cdf614
Bao Y, Dharmawardhana P, Mockler TC, Strauss SH (2009) Genome scale transcriptome analysis of shoot organogenesis in Populus. BMC Plant Biol 9:132. doi:10.1186/1471-2229-9-132
Barigah TS, Saugierb B, Mousseaub M, Guittetb J, Ceulemansc R (1994) Photosynthesis, leaf area and productivity of 5 poplar clones during their establishment year. Ann For Sci 51:613–625. doi:10.1051/forest:19940607
Behnke K, Kaiser A, Zimmer I et al (2010) RNAi-mediated suppression of isoprene emission in poplar transiently impacts phenolic metabolism under high temperature and high light intensities: a transcriptomic and metabolomic analysis. Plant Mol Biol 74(1–2):61–75. doi:10.1007/s11103-010-9654-z
Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Björkbacka H, Birve SJ, Karlsson J, Gardeström P, Gustafsson P, Lundeberg J, Jansson S (2003) Gene expression in autumn leaves. Plant Physiol 131(2):430–442
Bieker JJ, Martin PL, Roeder RG (1985) Formation of a ratelimiting intermediate in 5S RNA gene transcription. Cell 40(1):119–127. doi:10.1016/0092-8674(85)90315-0
Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218(5):683–692. doi:10.1007/s00425-004-1203-z
Bradshaw HD, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313
Chang SJ, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11(2):113–116. doi:10.1007/BF02670468
Chen M, Han G, Dietrich CR, Dunn TM, Cahoon EB (2006) The essential nature of sphingolipids in plants as revealed by the functional identification and characterization of the Arabidopsis LCB1 subunit of serine palmitoyltransferase. Plant Cell 18(12):3576–3593. doi:10.1105/tpc.105.040774
Chen Z, Zheng Z, Huang J, Lai Z, Fan B (2009) Biosynthesis of salicylic acid in plants. Plant Signal Behav 4(6):493–496
Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM (2004) A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37(6):853–863. doi:10.1111/j.1365-313X.2003.02012.x
Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230(4728):895–899. doi:10.1126/science.230.4728.895
Coutinho PM, Stam M, Blanc E, Henrissat B (2003) Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci 8(12):563–565. doi:10.1016/j.tplants.2003.10.002
Cseke LJ, Tsai CJ, Rogers A, Nelsen MP, White HL, Karnosky DF, Podila GK (2009) Transcriptomic comparison in the leaves of two aspen genotypes having similar carbon assimilation rates but different partitioning patterns under elevated [CO2]. New Phytol 182:891–911. doi:10.1111/j.1469-8137.2009.02812.x
Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18(2):215–222. doi:10.1046/j.1365-313X.1999.00444.x
Devine WD, Harrington CA, DeBell DS (2010) Intra-annual growth and mortality of four Populus clones in pure and mixed plantings. New Forest 39:287–299. doi:10.1007/s11056-009-9171-6
Dharmawardhana P, Brunner AM, Strauss SH (2010) Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC Genomics 11:150
Dickmann DI, Stuart KW (1983) The culture of poplars in eastern North America. Michigan State University, East Lansing
Ding M, Hou P, Shen X, Wang M, Deng S, Sun J ,Xiao F, Wang R, Zhou X, Lu C, Zhang D, Zheng X, Hu Z, Chen S (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol 73(3):251–269. doi:10.1007/s11103-010-9612-9
Donaldson JR, Kruger EL, Lindroth RL (2006) Competition- and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytol 169(3):561–570. doi:10.1111/j.1469-8137.2005.01613.x
Ehlting J, Sauveplane V, Olry A, Ginglinger JF, Provart NJ, Werck-Reichhart D (2008) An extensive (co-)expression analysis tool for the cytochrome P450 superfamily in Arabidopsis thaliana. BMC Plant Biol 8:47. doi:10.1186/1471-2229-8-47
Favery B, Lecomte P, Gil N, Bechtold N, Bouchez D, Dalmasso A, Abad P (1998) RPE, a plant gene involved in early developmental steps of nematode feeding cells. EMBO J 17(23):6799–6811. doi:10.1093/emboj/17.23.6799
Ferrer JL, Austin MB, Stewart C Jr, Noel JP (2008) Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiol Biochem 46:356–370. doi:10.1016/j.plaphy.2007.12.009
Geisler-Lee J, Geisler M, Coutinho PM et al (2006) Poplar carbohydrate-active enzymes. Gene identification and expression analyses. Plant Physiol 140(3):946–962. doi:10.1104/pp.105.072652
Glynn C, Herms DA, Orians CM, Hansen RC, Larsson S (2007) Testing the growth—differentiation balance hypothesis: dynamic responses of willows to nutrient availability. New Phytol 176(3):623–634. doi:10.1111/j.1469-8137.2007.02203.x
Gray-Mitsumune M, Blomquist K, McQueen-Mason S, Teeri TT, Sundberg B, Mellerowicz EJ (2008) Ectopic expression of a wood-abundant expansin PttEXPA1 promotes cell expansion in primary and secondary tissues in aspen. Plant Biotechnol J 6(1):62–72. doi:10.1111/j.1467-7652.2007.00295.x
Grisel N, Zoller S, Künzli-Gontarczyk M, Lampart T, Münsterkötter M, Brunner I, Bovet L, Métraux JP, Sperisen C (2010) Transcriptome responses to aluminum stress in roots of aspen (Populus tremula). BMC Plant Biol 10:185. doi:10.1186/1471-2229-10-185
Hamberger B, Ellis M, Friedmann M, de Azevedo Sousa C, Barbazuk B, Douglas C (2007) Genome-wide analyses of phenylpropanoid-related genes in Populus trichocarpa, Arabidopsis thaliana, and Oryza sativa: the Populus lignin toolbox and conservation and diversification of angiosperm gene families. Can J Bot 85(12):1182–1201. doi:10.1139/B07-098
Harding SA, Jarvie MM, Lindroth RL, Tsai CJ (2009) A comparative analysis of phenylpropanoid metabolism, N utilization, and carbon partitioning in fast- and slow-growing Populus hybrid clones. J Exp Bot (12):3443–3452. doi:10.1093/jxb/erp180
Harris MA, Clark J, Ireland A et al (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32(Database issue):D258–D261. doi:10.1093/nar/gkh036
Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335
Hu WJ, Kawaoka A, Tsai CJ, Lung J, Osakabe K, Ebinuma H, Chiang VL (1998) Compartmentalized expression of two structurally and functionally distinct 4-coumarate:CoA ligase genes in aspen (Populus tremuloides). Proc Natl Acad Sci 95(9):5407–5412
Huang J, Gu M, Lai Z, Fan B, Shi K, Zhou YH, Yu JQ, Chen Z (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153(4):1526–1538. doi:10.1104/pp.110.157370
Janz D, Behnke K, Schnitzler JP, Kanawati B, Schmitt-Kopplin P, Polle A (2010) Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biol 10:150
Jonsson TH, Óskarsson Ú (2007) Shoot growth strategy of 29 black cottonwood (Populus trichocarpa) clones. Icel Agric Sci. 20:25–36
Kao YY, Harding SA, Tsai CJ (2002) Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol 130(2):796–807. doi:10.1104/pp.006262
Kim M, Christopher DA, Mullet JE (1993) Direct evidence for selective modulation of psbA, rpoA, rbcL and 16S RNA stability during barley chloroplast development. Plant Mol Biol 22(3):447–463. doi:10.1007/BF00015975
Klaff P, Gruissem W (1991) Changes in chloroplast mRNA stability during leaf development. Plant Cell 3(5):517–529
Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009) PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21(12):3839–3849. doi:10.1105/tpc.109.071639
Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49(1):79–90. doi:10.1111/j.1365-313X.2006.02947.x
Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1, 7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiol 138(1):451–460. doi:10.1104/pp.104.055046
Levée V, Major I, Levasseur C, Tremblay L, MacKay J, Séguin A (2009) Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytol 184(1):48–70. doi:10.1111/j.1469-8137.2009.02955.x
Liu S, Jia J, Gao Y, Zhang B, Han Y (2010) The AtTudor2, a protein with SN-Tudor domains, is involved in control of seed germination in Arabidopsis. Planta 232(1):197–207. doi:10.1007/s00425-010-1167-0
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15(1):31–39. doi:10.1016/j.tplants.2009.11.003
McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15(5):1120–1130. doi:10.1105/tpc.010827
Müller D, Schmitz G, Theres K (2006) Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18(3):586–597. doi:10.1105/tpc.105.038745
Park S, Keathley DE, Han KH (2008) Transcriptional profiles of the annual growth cycle in Populus deltoides. Tree Physiol 28(3):321–329
Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LG, Rensing SA, Kersten B, Mueller-Roeber B (2009) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38(Database issue):D822–D827. doi:10.1093/nar/gkp805
Phillips LP, Huttly AK (1994) Cloning of two gibberellin-regulated cDNAs from Arabidopsis thaliana by subtractive hybridization: expression of the tonoplast water channel, gamma-TIP, is increased by GA3. Plant Mol Biol 24(4):603–615
Rennenberg H, Wildhagen H, Ehlting B (2010) Nitrogen nutrition of poplar trees. Plant Biol (Stuttg) 12(2):275–291. doi:10.1111/j.1438-8677.2009.00309.x
Ridge CR, Hinckley TM, Stettler RF, Van Volkenburgh E (1986) Leaf growth characteristics of fast-growing poplar hybrids Populus trichocarpa × P. deltoides. Tree Physiol 1(2):209–216
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(15–16):4047–4060. doi:10.1093/jxb/erm261
Ruuhola T, Julkunen-Titto R (2003) Trade-off between synthesis of salicylates and growth of micropropagated Salix pentandra. J Chem Ecol 29(7):1565–1588. doi:10.1023/A:1024266612585
Schliep M, Ebert B, Simon-Rosin U, Zoeller D, Fisahn J (2010) Quantitative expression analysis of selected transcription factors in pavement, basal and trichome cells of mature leaves from Arabidopsis thaliana. Protoplasma 241(1–4):29–36. doi:10.1007/s00709-009-0099-7
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37(5):501–506. doi:10.1038/ng1543
Schrader J, Nilsson J, Mellerowicz E et al (2004) A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem cell identity. Plant Cell 16:2278–2292
Shevell DE, Leu WM, Gillmor CS, Xia G, Feldmann KA, Chua NH (1994) EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77(7):1051–1062. doi:10.1016/0092-8674(94)90444-8
Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) Functional characterization of the Arabidopsis AtSUC2 Sucrose/H + symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol 148(1):200–211. doi:10.1104/pp.108.124776
Stitt M, Müller C, Matt P, Gibon Y, Carillo P, Morcuende R, Scheible W-R, Krapp A (2002) Steps towards an integrated view of nitrogen metabolism. J Exp Bot 53(370):959–970. doi:10.1093/jexbot/53.370.959
Street NR, Skogström O, Sjödin A, Tucker J, Rodríguez-Acosta M, Nilsson P, Jansson S, Taylor G (2006) The genetics and genomics of the drought response in Populus. Plant J 48(3):321–324. doi:10.1111/j.1365-313X.2006.02864.x
Taylor G (2002) Populus: Arabidopsis for forestry. do we need a model tree? Ann Bot 90:681–689. doi:10.1093/aob/mcf255
Tuskan GA, DiFazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Unneberg P, Strömberg M, Lundeberg J, Jansson S, Sterky F (2005) Analysis of 70,000 EST sequences to study divergence between two closely related Populus species. Tree Genet Genomes 1:109–115. doi:10.1007/s11295-005-0014-0
Walters RG, Ibrahim DG, Horton P, Kruger NJ (2004) A mutant of Arabidopsis lacking the triose-phosphate/phosphate translocator reveals metabolic regulation of starch breakdown in the light. Plant Physiol 135(2):891–906. doi:10.1104/pp.104.040469
Werck-Reichhart D (1995) Cytochromes P450 in phenylpropanoid metabolism. Drug Metabol Drug Interact 12(3–4):221–243
Wilkins O, Waldron L, Nahal H, Provart NJ, Campbell MM (2009) Genotype and time of day shape the Populus drought response. Plant J 60(4):703–715. doi:10.1111/j.1365-313X.2009.03993.x
Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE (2006) Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18(12):3476–3490. doi:10.1105/tpc.106.047290
Würschum T, Gross-Hardt R, Laux T (2006) APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18(2):295–307. doi:10.1105/tpc.105.038398
Yaeno T, Iba K (2008) BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiol 148(2):1032–1041. doi:10.1104/pp.108.124529
Zhu QH, Guo AY, Gao G, Zhong YF, Xu M, Huang M, Luo J (2007) DPTF: a database of poplar transcription factors. Bioinformatics 23(10):1307–1308. doi:10.1093/bioinformatics/btm113
Acknowledgments
This work was supported by the National Basic Research Program of China (2009CB119101), National Natural Science Foundation of China (30730077, 30972339, 31070597), Program for New Century Excellent Talents in University of China (NCET-07-0083), National R&D Key Project of China (2011BAD38B01). We thank Prof. Dr. Hongwei Guo (College of Life Sciences, Peking University, Beijing, China) for helpful suggestions.
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Hao, S., Zhao, T., Xia, X. et al. Genome-wide comparison of two poplar genotypes with different growth rates. Plant Mol Biol 76, 575–591 (2011). https://doi.org/10.1007/s11103-011-9790-0
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DOI: https://doi.org/10.1007/s11103-011-9790-0