Abstract
Polyploidy has played an important role in Populus breeding because allopolyploid trees generally display characteristics of increased height growth over diploids, and tree growth is determined by cell division and expansion in the apical region. However, the transcriptome characteristics of the shoot apical meristem involved in stem segment elongation and plant height growth remain unclear. In this study, apical buds were sampled from high and low growth vigor plants from a single full-sib cross between the parental clones, and their gene expression profiles were compared using high-throughput sequencing. In total, 4,870 genes were identified with differential expression between the high growth vigor allotriploid and its parents, and 821 genes were nonadditively expressed in the high growth vigor allotriploid. The differences in gene expression between the allotriploid and the male parent were more significant than those between it and its female parent. Many of the differentially expressed genes related to cell proliferation, meristem initiation, transcription factors, DNA and RNA methylation. Our results indicated that Populus allotriploids can generate extensive transcriptomic diversity compared with their parents. In addition, we found that the DEGs between high and low growth vigor Populus allotriploids are involved in important biological processes. Major changes in gene expression probably provide a driving force for phenotypic variation and adaptation in allopolyploids. The DEGs selected in this study provide important insight to obtain a better understanding of height growth heterosis in Populus allotriploids.
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References
Bastiaanssen HJM, Van den Berg PMMM, Lindhout P, Jacobsen E, Ramanna MS (1998) Postmeiotic restitution in 2n egg formation of diploid potato. Heredity 81:20–27
Boer DR, Freire-Rios A, van den Berg WA, Saaki T, Manfield IW, Kepinski S, López-Vidrieo I, Franco-Zorrilla JM, de Vries SC, Solano R, Weijers D, Coll M (2014) Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156(3):577–589
Carputo D, Frusciante L, Peloquin SJ (2003) The role of 2n gametes and endosperm balance number in the origin and evolution of polyploids in the tuber-bearing Solanums. Genetics 163(1):287–294
Chelaifa H, Monnier A, Ainouche M (2010) Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina x townsendii and Spartina anglica (Poaceae). New Phytol 186(1):161–174
Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15(2):57–71
Dong CB, Suo YJ, Kang XY (2014) Assessment of the genetic composition of triploid hybrid Populus using SSR markers with low recombination frequencies. Can J For Res 44(7):692–699
Donoghue MT, Fort A, Clifton R, Zhang X, McKeown PC, Voigt-Zielinksi ML, Borevitz JO, Spillane C (2014) C(m)CGG methylation-independent parent-of-origin effects on genome-wide transcript levels in isogenic reciprocal F1 triploid plants. DNA Res 21(2):141–151
Einspahr DW (1984) Production and utilization of triploid hybrid aspen. Iowa State J Res 58(4):401–409
Friml J, Benková E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K (2002a) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108(5):661–673
Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002b) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415(6873):806–809
Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426(6963):147–153
Fu Y, Dominissini D, Rechavi G, He C (2014) Gene expression regulation mediated through reversible m6A RNA methylation. Nat Rev Genet 15(5):293–306
Grover CE, Gallagher JP, Szadkowski EP, Yoo MJ, Flagel LE, Wendel JF (2012) Homoeolog expression bias and expression level dominance in allopolyploids. New Phytol 196:966–971
Hermsen JG (1984) Mechanisms and genetic implications of 2n gamete formation. Iowa State J Res 58:421–434
Jin Z, Xu W, Liu A (2014) Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.). Planta 239(2):299–312
Kaya H, Shibahara KI, Taoka KI, Iwabuchi M, Stillman B, Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell 104(1):131–142
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25
Li SW, Zhang ZY, Luo JM, He CZ, Pu YS, An XM (2005) Progress and strategies in cross breeding of poplars in china. Forestry Studies in China 7(3):54–60
Li YH, Kang XY, Wang SD, Zhang ZH, Chen HW (2008) Triploid induction in Populus alba × P. glandulosa by chromosome doubling of female gametes. Silvae Genet 57:37–40
Li A, Liu D, Wu J, Zhao X, Hao M, Geng S, Yan J, Jiang X, Zhang L, Wu J, Yin L, Zhang R, Wu L, Zheng Y, Mao L (2014) mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. Plant Cell 26(5):1870–1900
Lim K, Shen T, Barba-Gonzalez R, Ramanna MS, Van Tuyl JM (2004) Occurrence of SDR 2n-gamete in Lilium hybrids. Breed Sci 54:13–18
Liu N, Wu S, Van Houten J, Wang Y, Ding B, Fei Z, Clarke TH, Reed JW, van der Knaap E (2014) Down-regulation of AUXIN RESPONSE FACTORS 6 and 8 by microRNA 167 leads to floral development defects and female sterility in tomato. J Exp Bot 65(9):2507–2520
Lu M, Zhang P, Kang X (2013) Induction of 2n female gametes in Populus adenopoda Maxim by high temperature exposure during female gametophyte development. Breed Sci 63:96–103
Madlung A, Wendel JF (2013) Genetic and epigenetic aspects of polyploid evolution in plants. Cytogenet Genome Res 140(2–4):270–285
Matsumoto T, Morishige H, Tanaka T, Kanamori H, Komatsuda T, Sato K, Itoh T, Wu JD, Nakamura S (2014) Transcriptome analysis of barley identifies heat shock and HD-Zip I transcription factors up-regulated in response to multiple abiotic stresses. Mol Breeding 34(2):761–768
Miller M, Zhang C, Chen ZJ (2012) Ploidy and hybridity effects on growth vigor and gene expression in Arabidopsis thaliana hybrids and their parents. G3 2(4):505–513
Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4(6):533–539
Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17(23):6903–6911
Müntzing A (1936) The chromosomes of a giant Populus tremula. Hereditas 21:383–393
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432
Ng DW, Zhang C, Miller M, Shen Z, Briggs SP, Chen ZJ (2012) Proteomic divergence in Arabidopsis autopolyploids and allopolyploids and their progenitors. Heredity 108(4):419–430
Ni DA, Sozzani R, Blanchet S, Domenichini S, Reuzeau C, Cella R, Bergounioux C, Raynaud C (2009) The Arabidopsis MCM2 gene is essential to embryo development and its over-expression alters root meristem function. New Phytol 184(2):311–322
Nilsson-Ehle H (1936) Note regarding the gigas form of Populus tremula found in nature. Hereditas 21:372–382
Peloquin SJ, Boiteux LS, Simon PW, Jansky SH (2008) A chromosome-specific estimate of transmission of heterozygosity by 2n gametes in potato. J Hered 99(2):177–181
Qi B, Huang W, Zhu B, Zhong X, Guo J, Zhao N, Xu C, Zhang H, Pang J, Han F, Liu B (2012) Global transgenerational gene expression dynamics in two newly synthesized allohexaploid wheat (Triticum aestivum) lines. BMC Biol 10:3
Rapp RA, Udall JA, Wendel JF (2009) Genomic expression dominance in allopolyploids. BMC Biol 7:18
Romberger JA (1963) Meristems, growth and development in woody plants. USDA For Serv Tech Bull No. 1293
Rook F, Gerrits N, Kortstee A, van Kampen M, Borrias M, Weisbeek P, Smeekens S (1998) Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J 15(2):253–263
Sugimoto-Shirasu K, Roberts K (2003) ‘Big it up’: endoreduplication and cell-size control in plants. Curr Opin Plant Biol 6(6):544–553
Sui Y, Li B, Shi J, Chen M (2014) Genomic, regulatory and epigenetic mechanisms underlying duplicated gene evolution in the natural allotetraploid Oryza minuta. BMC Genom 15:11
Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25(9):1105–1111
Trupiano D, Yordanov Y, Regan S, Meilan R, Tschaplinski T, Scippa GS, Busov V (2013) Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus. Planta 238(2):271–282
Van Buijtenen JP, Joranson PN, Einspahr DW (1958) Diploid versus triploid aspen as pulpwood sources with reference to growth, chemical, physical and pulping differences. TAPPI 41:170–175
Van Minnebruggen A, Neyt P, De Groeve S, Coussens G, Ponce MR, Micol JL, Van Lijsebettens M (2010) The ang3 mutation identified the ribosomal protein gene RPL5B with a role in cell expansion during organ growth. Physiol Plant 138(1):91–101
Wang J, Kang XY, Li DL, Chen HW, Zhang PD (2010) Induction of diploid eggs with colchicine during embryo sac development in Populus. Silvae Genet 59:40–48
Wang J, Li DL, Kang XY (2012) Induction of unreduced megaspores with high temperature during megasporogenesis in Populus. Ann For Sci 15:1–9
Weisgerber H, Rau HM, Gartner EJ, Baumeister G, Kohnert H, Karner L (1980) 25 years of forest tree breeding in Hessen. Allg For 26:665–712
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95(5):707–735
Xiao J, Song C, Liu S, Tao M, Hu J, Wang J, Liu W, Zeng M, Liu Y (2013) DNA methylation analysis of allotetraploid hybrids of red crucian carp (Carassius auratus red var.) and common carp (Cyprinus carpio L.). PLoS One 8(2):e56409
Xie S, Lam E (1994) Abundance of nuclear DNA topoisomerase II is correlated with proliferation in Arabidopsis thaliana. Nucleic Acids Res 22(25):5729–5736
Yang XY, Li XG, Li BL, Zhang DQ (2014) Identification of genes differentially expressed in shoot apical meristems and in mature xylem of Populus tomentosa. Plant Mol Biol Rep 32:452–464
Zhao Q, Zou J, Meng J, Mei S, Wang J (2013) Tracing the transcriptomic changes in synthetic trigenomic allohexaploids of Brassica using an RNA-Seq approach. PLoS One 8(7):e68883
Zhu ZT, Kang XY, Zhang ZY (1998) Studies on selection of natural triploids of Populus tomentosa. Sci Silave Sin 34:22–31
Zhu Y, Dong A, Meyer D, Pichon O, Renou JP, Cao K, Shen WH (2006) Arabidopsis NRP1 and NRP2 encode histone chaperones and are required for maintaining postembryonic root growth. Plant Cell 18(11):2879–2892
Acknowledgments
This work was supported in part by Special Fund for Forest Scientific Research in the Public Welfare (201404113), a Foundation for the Author of National Excellent Doctoral Dissertation of P. R. China (Grant No. 201267), and 111 Project (B13007). The authors would like to thank Dr. Guanjing Hu in Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames IA, for her critical reading of the manuscript. The authors also wish to thank Drs. Dai Chen and Bo Zhang (Novel Bioinformatics Ltd., Co, Shanghai, China) for their technical assistance in bioinformatics analysis.
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Cheng, S., Huang, Z., Suo, Y. et al. Gene expression differences associated with growth vigor in Populus full-sib allotriploid progeny following manipulated first division restitution of the diploid maternal parent. Euphytica 203, 683–700 (2015). https://doi.org/10.1007/s10681-014-1316-9
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DOI: https://doi.org/10.1007/s10681-014-1316-9