Abstract
Whole genome duplication (WGD) is a common phenomenon in plants, inducing species diversity, promoting speciation, and playing an important role in providing new genetic material in plant evolution. So far, numerous new gene functions such as pseudogenization, neofunctionalization, and subfunctionalization have evolved through WGD. WGD has occurred several times during the evolution of angiosperms over the past 200 million years. Poaceae, one of the largest plant families in the angiosperms, is considered one of the most economically important and ecologically successful plants, with approximately 600 genera and 10,000 species. Many genetic studies have been conducted on these plants. However, study of the most active phylogeny in the Poaceae family study has not yet been completed. Through comparative studies of major Poaceae groups, this review focuses on the effects of genome duplication in the Poaceae family on its evolutionary history and the changes in chromosome numbers.
Similar content being viewed by others
References
Alix K, Gérard PR, Schwarzacher T, Heslop-Harrison J (2017) Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Ann Bot 120:183–194
Balakirev ES, Ayala FJ (2003) Pseudogenes: are they “junk” or functional DNA? Annu Rev Genet 37:123–151
Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, van der Bank M et al (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Mol Phylogenet Evol 47:488–505
Bouchenak-Khelladi Y, Verboom GA, Savolainen V, Hodkinson TR (2010) Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Bot J Linn Soc 162:543–557
Brockington SF, Yang Y, Gandia-Herrero F, Covshoff S, Hibberd JM et al (2015) Lineage-specific gene radiations underlie the evolution of novel betalain pigmentation in Caryophyllales. New Phytol 207:1170–1180
Burke SV, Wysocki WP, Zuloaga FO, Craine JM, Pires JC et al (2016) Evolutionary relationships in Panicoid grasses based on plastome phylogenomics (Panicoideae; Poaceae). BMC Plant Biol 16:140
Chalhoub B, Denoeud F, Liu S, Parkin IA, Tang H et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953
Changsoo K, Haibao T, Paterson AH (2009) Duplication and divergence of grass genomes: integrating the chloridoids. Trop Plant Biol 2:51–62
Chantret N, Salse J, Sabot F, Rahman S, Bellec A et al (2005) Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:1033–1045
Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406
Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15:57–71
Chen ZJ, Ni ZF (2006) Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. BioEssays 28:240–252
Christin PA, Besnard G (2009) Two independent C4 origins in Aristidoideae (Poaceae) revealed by the recruitment of distinct phosphoenolpyruvate carboxylase genes. Am J Bot 96:2234–2239
Christin P-A, Osborne CP (2013) The recurrent assembly of C 4 photosynthesis, an evolutionary tale. Photosynth Res 117:163–175
Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR et al (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Curr Biol 18:37–43
Christin PA, Osborne CP, Chatelet DS, Columbus JT, Besnard G et al (2013) Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc Natl Acad Sci UA 110:1381–1386
Christin P-A, Spriggs E, Osborne CP, Strömberg CA, Salamin N, Edwards EJ (2014) Molecular dating, evolutionary rates, and the age of the grasses. Syst Biol 63:153–165
Clark JW, Donoghue PCJ (2017) Constraining the timing of whole genome duplication in plant evolutionary history. Proc R Soc B Biol Sci 284:20170912
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846
Conant GC, Birchler JA, Pires JC (2014) Dosage, duplication, and diploidization: clarifying the interplay of multiple models for duplicate gene evolution over time. Curr Opin Plant Biol 19:91–98
Conrad B, Antonarakis SE (2007) Gene duplication: a drive for phenotypic diversity and cause of human disease. Annu Rev Genom Hum Genet 8:17–35
Cotton JL, Wysocki WP, Clark LG, Kelchner SA, Pires JC et al (2015) Resolving deep relationships of PACMAD grasses: a phylogenomic approach. BMC Plant Biol 15:178
D'Antonio M, Ciccarelli FD (2011) Modification of gene duplicability during the evolution of protein interaction network. PLoS Comput Biol 7:e1002029
Davidson RM, Gowda M, Moghe G, Lin HN, Vaillancourt B et al (2012) Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution. Plant J 71:492–502
De Smet R, Van de Peer Y (2012) Redundancy and rewiring of genetic networks following genome-wide duplication events. Curr Opin Plant Biol 15:168–176
Devos KM (2005) Updating the ‘crop circle’. Curr Opin Plant Biol 8:155–162
Dodsworth S, Chase MW, Leitch AR (2016) Is post-polyploidization diploidization the key to the evolutionary success of angiosperms? Bot J Linn Soc 180:1–5
Eckardt NA (2008) Grass genome evolution. Am Soc Plant Biol
Edwards EJ, Osborne CP, Strömberg CA, Smith SA (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328:587–591
Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Zool 19:99–113
Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545
Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16:805–814
Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28
Hughes TE, Langdale JA, Kelly S (2014) The impact of widespread regulatory neofunctionalization on homeolog gene evolution following whole-genome duplication in maize. Genome Res 24:1348–1355
Humphreys AM, Linder HP (2013) Evidence for recent evolution of cold tolerance in grasses suggests current distribution is not limited by (low) temperature. New Phytol 198:1261–1273
Innan H (2009) Population genetic models of duplicated genes. Genetica 137:19–37
Jackson S, Chen ZJ (2010a) Genomic and expression plasticity of polyploidy. Curr Opin Plant Biol 13:153–159
Katju V, Lynch M (2006) On the formation of novel genes by duplication in the Caenorhabditis elegans genome. Mol Biol Evol 23:1056–1067
Kejnovsky E, Leitch IJ, Leitch AR (2009) Contrasting evolutionary dynamics between angiosperm and mammalian genomes. Trends Ecol Evol 24:572–582
Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205
Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921
Li L, Briskine R, Schaefer R, Schnable PS, Myers CL et al (2016) Co-expression network analysis of duplicate genes in maize (Zea mays L.) reveals no subgenome bias. BMC Genom 17:875
Linder HP, Rudall PJ (2005) Evolutionary history of Poales. Annu Rev Ecol Evol Syst 36:107–124
Liu H, Liu H, Zhou L, Zhang Z, Zhang X et al (2015) Parallel domestication of the heading date 1 gene in cereals. Mol Biol Evol 32:2726–2737
Lynch M (2002) Genomics. Gene duplication and evolution. Science 297:945–947
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473
Mable BK (2003) Breaking down taxonomic barriers in polyploidy research. Trends Plant Sci 8:582–590
MacKintosh C, Ferrier DEK (2017) Recent advances in understanding the roles of whole genome duplications in evolution. F1000Res 6:1623
Madlung A (2013) Polyploidy and its effect on evolutionary success: old questions revisited with new tools. Heredity 110:99–104
Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. J Genet 92:155–161
Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T (2015) A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol 207:437–453
Mannion PD, Upchurch P, Benson RB, Goswami A (2014) The latitudinal biodiversity gradient through deep time. Trends Ecol Evol 29:42–50
Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS et al (2011) Recently formed polyploid plants diversify at lower rates. Science 333:1257–1257
Mayrose I, Zhan SH, Rothfels CJ, Arrigo N, Barker MS et al (2015) Methods for studying polyploid diversification and the dead end hypothesis: a reply to Soltis et al. (2014). New Phytol 206:27–35
Moore G, Devos K, Wang Z, Gale M (1995) Cereal genome evolution: grasses, line up and form a circle. Curr Biol 5:737–739
Moriyama Y, Koshiba-Takeuchi K (2018) Significance of whole-genome duplications on the emergence of evolutionary novelties. Briefings Funct Genom 17:329–338
Mudelsee M, Bickert T, Lear CH, Lohmann G (2014) Cenozoic climate changes: a review based on time series analysis of marine benthic delta O-18 records. Rev Geophys 52:333–374
Murat F, Van de Peer Y, Salse J (2012) Decoding plant and animal genome plasticity from differential paleo-evolutionary patterns and processes. Genome Biol Evol 4:917–928
Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York
Olsen KM, Wendel JF (2013) A bountiful harvest: genomic insights into crop domestication phenotypes. Annu Rev Plant Biol 64:47–70
Panchy N, Lehti-Shiu M, Shiu S-H (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316
Parisod C, Holderegger R, Brochmann C (2010) Evolutionary consequences of autopolyploidy. New Phytol 186:5–17
Parrish DJ, Casler MD, Monti A (2012) The evolution of switchgrass as an energy crop. In “Switchgrass”. Springer, New York, pp 1–28
Paterson A, Bowers J, Chapman B (2004a) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci 101:9903–9908
Paterson AH, Bowers JE, Chapman BA (2004b) Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA 101:9903–9908
Paun O, Bateman RM, Fay MF, Luna JA, Moat J et al (2011) Altered gene expression and ecological divergence in sibling allopolyploids of Dactylorhiza (Orchidaceae). Bmc Evol Biol 11:113
Peter Linder H, Antonelli A, Humphreys AM, Pirie MD, Wüest RO (2013) What determines biogeographical ranges? Historical wanderings and ecological constraints in the danthonioid grasses. J Biogeogr 40:821–834
Prasad V, Strömberg C, Leaché A, Samant B, Patnaik R et al (2011) Late Cretaceous origin of the rice tribe provides evidence for early diversification in Poaceae. Nat Commun 2:480
Preston JC, Sandve SR (2013) Adaptation to seasonality and the winter freeze. Front Plant Sci 4:167
Puttick MN (2015) Size is not everything: rates of genome size evolution, not C-value, correlate with speciation in angiosperms. Proc R Society B Biol Sci 282(1820):20152289
Rasmussen DA, Kramer EM, Zimmer EA (2009) One size fits all? Molecular evidence for a commonly inherited petal identity program in Ranunculales. Am J Bot 96:96–109
Rastogi S, Liberles DA (2005) Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evol Biol 5:28
Ren R, Wang H, Guo C, Zhang N, Zeng L et al (2018) Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Mol Plant 11:414–428
Renny-Byfield S, Wendel JF (2014a) Doubling down on genomes: polyploidy and crop plants. Am J Bot 101:1711–1725
Rieseberg LH, Widmer A, Arntz AM, Burke JM (2002) Directional selection is the primary cause of phenotypic diversification. Proc Natl Acad Sci USA 99:12242–12245
Rijpkema AS, Royaert S, Zethof J, van der Weerden G, Gerats T, Vandenbussche M (2006) Analysis of the Petunia TM6 MADS box gene reveals functional divergence within the DEF/AP3 lineage. Plant Cell 18:1819–1832
Rouquier S, Blancher A, Giorgi D (2000) The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc Natl Acad Sci USA 97:2870–2874
Ruiz-Sanchez E (2011) Biogeography and divergence time estimates of woody bamboos: insights in the evolution of Neotropical bamboos. Bot Sci 88:67–75
Sakai H, Koyanagi KO, Imanishi T, Itoh T, Gojobori T (2007) Frequent emergence and functional resurrection of processed pseudogenes in the human and mouse genomes. Gene 389:196–203
Salman-Minkov A, Sabath N, Mayrose I (2016) Whole-genome duplication as a key factor in crop domestication. Nat Plants 2:1–4
Salse J, Bolot S, Throude M, Jouffe V, Piegu B et al (2008) Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20:11–24
Sandra A, Hester LB, Guillaume B, Pascal‐Antoine C, Travis C, Melvin RD, Erika JE, Liliana G, Kristen HL, Khidir WH, Trevor RH, Amanda LI, Elizabeth AK, Saeideh M, Osvaldo M, Colin PO, Nicolas S, Hanno S, Elizabeth S, Stephen AS, Fernando Z (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312
Sánchen-Ken JG, Clark LG, Kellogg EA, Kay EE (2007) Reinstatement and emendation of subfamily Micrairoideae (Poaceae). Syst Bot 32:1
Sandve SR, Rudi H, Asp T, Rognli OA (2008) Tracking the evolution of a cold stress associated gene family in cold tolerant grasses. BMC Evol Biol 8:245
Sandye S, Fjellheim S (2010) Did gene family expansions during the Eocene–Oligocene boundary climate cooling play a role in Pooideae adaptation to cool climates? Mol Ecol 19:2075–2088
Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178
Schranz ME, Mohammadin S, Edger PP (2012) Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. Curr Opin Plant Biol 15:147–153
Semon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17:505–512
Shantz H (1954) The place of grasslands in the Earth’s cover. Ecology 35:143–145
Shchapova A (2012) Evolution of the basic chromosome number in Poaceae Barnh. Russ J Genet Appl Res 2:252–259
Simonin KA, Roddy AB (2018) Genome downsizing, physiological novelty, and the global dominance of flowering plants. Plos Biol 2018:16
Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588
Soltis DE, Visger CJ, Soltis PS (2014) The polyploidy revolution then and now: Stebbins revisited. Am J Bot 101:1057–1078
Soreng RJ, Peterson PM, Romaschenko K, Davidse G, Zuloaga FO et al (2015) A worldwide phylogenetic classification of the Poaceae (Gramineae). J Syst Evol 53:117–137
Soreng RJ, Peterson PM, Romaschenko K, Davidse G, Teisher JK et al (2017) A worldwide phylogenetic classification of the Poaceae (Gramineae) II: an update and a comparison of two 2015 classifications. J Syst Evol 55:259–290
Spriggs EL, Christin P-A, Edwards EJ (2014) C4 photosynthesis promoted species diversification during the Miocene grassland expansion. PLoS ONE 9:e97722
Stoltzfus A (1999) On the possibility of constructive neutral evolution. J Mol Evol 49:169–181
Sungkaew S, Stapleton CM, Salamin N, Hodkinson TR (2009) Non-monophyly of the woody bamboos (Bambuseae; Poaceae): a multi-gene region phylogenetic analysis of Bambusoideae ss. J Plant Res 122:95
Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE et al (2015a) Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol 207:454–467
Taylor SH, Ripley BS, Martin T, De-Wet LA, Woodward FI, Osborne CP (2014) Physiological advantages of C4 grasses in the field: a comparative experiment demonstrating the importance of drought. Glob Change Biol 20:1992–2003
Teisher JK (2016) Systematics and evolution of the Arundinoideae and Micrairoideae (Poaceae).
Teisher J, McKain M, Schaal B, Kellogg E (2017) Polyphyly of Arundinoideae (Poaceae) and evolution of the twisted geniculate lemma awn. Ann Bot 120:725–738
Thibaud-Nissen F, Ouyang S, Buell CR (2009) Identification and characterization of pseudogenes in the rice gene complement. BMC Genom 10:317
Thomas BC, Pedersen B, Freeling M (2006) Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res 16:934–946
Tsukaya H (2013) Does ploidy level directly control cell size? Counterevidence from Arabidopsis Genetics. PLoS ONE 2013:8
Van de Peer Y, Maere S, Meyer A (2009) The evolutionary significance of ancient genome duplications. Nat Rev Genet 10:725–732
Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nat Rev Genet 18:411–424
Vigeland MD, Spannagl M, Asp T, Paina C, Rudi H et al (2013) Evidence for adaptive evolution of low-temperature stress response genes in a Pooideae grass ancestor. New Phytol 199:1060–1068
Vorontsova MS, Haevermans T, Haevermans A, Razanatsoa J, Lundgren MR, Besnard G (2015) The genus Sartidia (Poaceae: Aristidoideae) in Madagascar. Syst Bot 40:448–453
Wang E, Wang J, Zhu X, Hao W, Wang L et al (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370
Wang E, Xu X, Zhang L, Zhang H, Lin L et al (2010) Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication. BMC Evol Biol 10:108
Wei F, Coe WN, Bharti AK, Engler F, Butler HK et al (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 2007:3
Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249
Yang Y, Li Y, Chen Q, Sun Y, Lu Z (2019) WGDdetector: a pipeline for detecting whole genome duplication events using the genome or transcriptome annotations. BMC Bioinform 20(1):75
Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693
Zeng X, Yuan Z, Tong X, Li Q, Gao W et al (2012) Phylogenetic study of Oryzoideae species and related taxa of the Poaceae based on atpB-rbcL and ndhF DNA sequences. Mol Biol Rep 39:5737–5744
Zeven AC, Zhukovsky PM (1975) Dictionary of cultivated plants and their centres of diversity: excluding ornamentals, forest trees and lower plants. Pudoc.
Zhang J (2003) Evolution by gene duplication: an update. TRENDS Ecol Evol 18(6):292
Zhang Z, Belcram H, Gornicki P, Charles M, Just J et al (2011) Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proc Natl Acad Sci 108:18737–18742
Zhao L, Zhang N, Ma P-F, Liu Q, Li D-Z, Guo Z-H (2013) Phylogenomic analyses of nuclear genes reveal the evolutionary relationships within the BEP clade and the evidence of positive selection in Poaceae. PLoS ONE 8:e64642
Zou C, Lehti-Shiu MD, Thibaud-Nissen F, Prakash T, Buell CR, Shiu SH (2009) Evolutionary and expression signatures of pseudogenes in Arabidopsis and rice. Plant Physiol 151:3–15
Acknowledgements
This work was supported by the “Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01315902)”, Rural Development Administration, Republic of Korea.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Lee, S., Choi, S., Jeon, D. et al. Evolutionary impact of whole genome duplication in Poaceae family. J. Crop Sci. Biotechnol. 23, 413–425 (2020). https://doi.org/10.1007/s12892-020-00049-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12892-020-00049-2