Comparative Genomics in Perennial Ryegrass (Lolium perenne L.): Identification and Characterisation of an Orthologue for the Rice Plant Architecture-Controlling Gene OsABCG5
Perennial ryegrass is an important pasture grass in temperate regions. As a forage biomass-generating species, plant architecture-related characters provide key objectives for breeding improvement. In silico comparative genomics analysis predicted colocation between a previously identified QTL for plant type (erect versus prostrate growth) and the ortholocus of the rice OsABCG5 gene (LpABCG5), as well as related QTLs in other Poaceae species. Sequencing of an LpABCG5-containing BAC clone identified presence of a paralogue (LpABCG6) in the vicinity of the LpABCG5 locus, in addition to three other gene-like sequences. Comparative genomics involving five other 5 grass species (rice, Brachypodium, sorghum, maize, and foxtail millet) revealed conserved microsynteny in the ABCG5 ortholocus-flanking region. Gene expression profiling and phylogenetic analysis suggested that the two paralogues are functionally distinct. Fourteen additional ABCG5 gene family members, which may interact with the LpABCG5 gene, were identified through sequencing of transcriptomes from perennial ryegrass leaf, anther, and pistils. A larger-scale phylogenetic analysis of the ABCG gene family suggested conservation between major branches of the Poaceae family. This study identified the LpABCG5 gene as a candidate for the plant type determinant, suggesting that manipulation of gene expression may provide valuable phenotypes for perennial ryegrass breeding. 1. Introduction Perennial ryegrass is an economically important temperate pasture grass species and a diploid ( ) member of the Poaceae family which includes other major cereal crops such as rice (Oryza sativa L.), wheat (Triticum aestivum L.), barley (Hordeum vulgare L.), sorghum (Sorghum bicolor L.), and maize (Zea mays L.) [1, 2]. Due to superior herbage digestibility and grazing tolerance, perennial ryegrass has been a primary target for molecular breeding among forage and turf crops [3]. Following establishment of a whole-genome genetic map consisting of 7 linkage groups (LGs) [4, 5], a number of quantitative trait loci (QTLs) related to variation for herbage yield and quality have been identified [6–9]. Plant morphological traits contribute to such variation in pasture grass species and are largely controlled by genetic factors [6, 10]. For example, evaluation of a one-way pseudotestcross genetic mapping population obtained a broad sense heritability ( ) value of 0.73 for the herbage fresh weight character, and significant correlations were observed between this and other traits such as plant height and tiller number [6].
References
[1]
P. W. Wilkins, “Breeding perennial ryegrass for agriculture,” Euphytica, vol. 52, no. 3, pp. 201–214, 1991.
[2]
K. M. Devos and M. D. Gale, “Comparative genetics in the grasses,” Plant Molecular Biology, vol. 35, no. 1-2, pp. 3–15, 1997.
[3]
J. W. Forster, N. O. I. Cogan, M. P. Dobrowolski, M. G. Francki, G. C. Spangenberg, and K. F. Smith, “Functionally-associated molecular genetic markers for temperate pasture plant improvement,” in Plant Genotyping II: SNP Technology, R. J. Henry, Ed., pp. 154–187, CABI Press, Wallingford, Oxford, UK, 2008.
[4]
E. S. Jones, N. L. Mahoney, M. D. Hayward et al., “An enhanced molecular marker based genetic map of perennial ryegrass (Lolium perenne) reveals comparative relationships with other Poaceae genomes,” Genome, vol. 45, no. 2, pp. 282–295, 2002.
[5]
E. S. Jones, M. P. Dupal, J. L. Dumsday, L. J. Hughes, and J. W. Forster, “An SSR-based genetic linkage map for perennial ryegrass (Lolium perenne L.),” Theoretical and Applied Genetics, vol. 105, no. 4, pp. 577–584, 2002.
[6]
T. Yamada, E. S. Jones, N. O. I. Cogan et al., “QTL analysis of morphological, developmental, and winter hardiness-associated traits in perennial ryegrass,” Crop Science, vol. 44, no. 3, pp. 925–935, 2004.
[7]
N. O. I. Cogan, K. F. Smith, T. Yamada et al., “QTL analysis and comparative genomics of herbage quality traits in perennial ryegrass (Lolium perenne L.),” Theoretical and Applied Genetics, vol. 110, no. 2, pp. 364–380, 2005.
[8]
S. Sim, K. Diesburg, M. Casler, and G. Jung, “Mapping and comparative analysis of QTL for crown rust resistance in an Italian x perennial ryegrass population,” Phytopathology, vol. 97, no. 6, pp. 767–776, 2007.
[9]
A. Pearson, N. O.I. Cogan, R. C. Baillie et al., “Identification of QTLs for morphological traits influencing waterlogging tolerance in perennial ryegrass (Lolium perenne L.),” Theoretical and Applied Genetics, vol. 122, no. 3, pp. 609–622, 2011.
[10]
M. Inoue, Z. Gao, and H. Cai, “QTL analysis of lodging resistance and related traits in Italian ryegrass (Lolium multiflorum Lam.),” Theoretical and Applied Genetics, vol. 109, no. 8, pp. 1576–1585, 2004.
[11]
A. J. Windsor and T. Mitchell-Olds, “Comparative genomics as a tool for gene discovery,” Current Opinion in Biotechnology, vol. 17, no. 2, pp. 161–167, 2006.
[12]
J. P. Vogel, D. F. Garvin, T. C. Mockler et al., “Genome sequencing and analysis of the model grass Brachypodium distachyon,” Nature, vol. 463, no. 7282, pp. 763–768, 2010.
[13]
P. S. Schnable, D. Ware, R. S. Fulton et al., “The B73 maize genome: complexity, diversity, and dynamics,” Science, vol. 326, no. 5956, pp. 1112–1115, 2009.
[14]
Q. J. Jia, J. J. Zhang, S. Westcott et al., “GA-20 oxidase as a candidate for the semidwarf gene sdw1/denso in barley,” Functional and Integrative Genomics, vol. 9, no. 2, pp. 255–262, 2009.
[15]
G. T. H. Vu, T. Wicker, J. P. Buchmann et al., “Fine mapping and syntenic integration of the semi-dwarfing gene sdw3 of barley,” Functional and Integrative Genomics, vol. 10, no. 4, pp. 509–521, 2010.
[16]
I. P. Armstead, L. B. Turner, A. H. Marshall, M. O. Humphreys, I. P. King, and D. Thorogood, “Identifying genetic components controlling fertility in the outcrossing grass species perennial ryegrass (Lolium perenne) by quantitative trait loci analysis and comparative genetics,” New Phytologist, vol. 178, no. 3, pp. 559–571, 2008.
[17]
H. Shinozuka, H. Hisano, R. C. Ponting et al., “Molecular cloning and genetic mapping of perennial ryegrass casein protein kinase 2 α-subunit genes,” Theoretical and Applied Genetics, vol. 112, no. 1, pp. 167–177, 2005.
[18]
H. Shinozuka, N. O. I. Cogan, K. F. Smith, G. C. Spangenberg, and J. W. Forster, “Fine-scale comparative genetic and physical mapping supports map-based cloning strategies for the self-incompatibility loci of perennial ryegrass (Lolium perenne L.),” Plant Molecular Biology, vol. 72, no. 3, pp. 343–355, 2010.
[19]
N. Yasuno, I. Takamure, S. I. Kidou et al., “Rice shoot branching requires an ATP-binding cassette subfamily G protein,” New Phytologist, vol. 182, no. 1, pp. 91–101, 2009.
[20]
P. J. Verrier, D. Bird, B. Burla, et al., “Plant ABC proteins—a unified nomenclature and updated inventory,” Trends in Plant Science, vol. 13, no. 4, pp. 151–159, 2008.
[21]
N. Yasuno, Y. Yasui, I. Takamure, and K. Kato, “Genetic interaction between 2 tillering genes, reduced culm number 1 (rcn1) and tillering dwarf gene d3, in rice,” Journal of Heredity, vol. 98, no. 2, pp. 169–172, 2007.
[22]
S. Velamakanni, S. L. Wei, T. Janvilisri, and H. W. van Veen, “ABCG transporters: structure, substrate specificities and physiological roles—a brief overview,” Journal of Bioenergetics and Biomembranes, vol. 39, no. 5-6, pp. 465–471, 2007.
[23]
H. E. Mcfarlane, J. J. H. Shin, D. A. Bird, and A. L. Samuels, “Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations,” Plant Cell, vol. 22, no. 9, pp. 3066–3075, 2010.
[24]
S. Marguerat and J. B？hler, “RNA-seq: from technology to biology,” Cellular and Molecular Life Sciences, vol. 67, no. 4, pp. 569–579, 2010.
[25]
F. Ozsolak and P. M. Milos, “RNA sequencing: advances, challenges and opportunities,” Nature Reviews Genetics, vol. 12, no. 2, pp. 87–98, 2011.
[26]
S. Zeng, G. Xiao, J. Guo et al., “Development of a EST dataset and characterization of EST-SSRs in a traditional Chinese medicinal plant, Epimedium sagittatum (Sieb. Et Zucc.) Maxim,” BMC Genomics, vol. 11, no. 1, article 94, 2010.
[27]
S. L. Byrne, K. Durandeau, I. Nagy, and S. Barth, “Identification of ABC transporters from Lolium perenne L. that are regulated by toxic levels of selenium,” Planta, vol. 231, no. 4, pp. 901–911, 2010.
[28]
B. Korber, “HIV signature and sequence variation analysis,” in Computational and Evolutionary Analysis of HIV Molecular Sequences, A. G. Rodrigo and G. H. Learn, Eds., pp. 55–72, Kluwer Academic Publishers, Dordrecht, The Netherlands, 2000.
[29]
M. Nei, Molecular Evolutionary Genetics, Columbia University Press, New York, NY, USA, 1987.
[30]
C. Kim, H. Tang, and A. H. Paterson, “Duplication and divergence of grass genomes: integrating the chloridoids,” Tropical Plant Biology, vol. 2, no. 1, pp. 51–62, 2009.
[31]
E. Ritter, C. Gebhardt, and F. Salamini, “Estimation of recombination frequencies and construction of RFLP linkage maps in plants from crosses between heterozygous parents,” Genetics, vol. 125, no. 3, pp. 645–654, 1990.
[32]
J. W. van Ooijen and R. E. Voorrips, JoinMap？ 3.0, Software for the Calculation of Genetic Linkage Maps, Plant Research International, Wageningen, The Netherlands, 2001.
[33]
G. C. Spangenberg, J. W. Forster, D. Edwards, et al., “Future directions in the molecular breeding of forage and turf,” in Molecular Breeding for the Genetic Improvement of Forage Crops and Turf, M. O. Humphreys, Ed., pp. 83–97, Wageningen Academic Publishers, Wageningen, The Netherlands, 2005.
[34]
F. B. Dean, S. Hosono, L. Fang et al., “Comprehensive human genome amplification using multiple displacement amplification,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 8, pp. 5261–5266, 2002.
[35]
M. J. Faville, A. C. Vecchies, M. Schreiber et al., “Functionally associated molecular genetic marker map construction in perennial ryegrass (Lolium perenne L.),” Theoretical and Applied Genetics, vol. 110, no. 1, pp. 12–32, 2004.
[36]
Y. Tu, S. Rochfort, Z. Liu et al., “Functional analyses of caffeic acid O-methyltransferase and Cinnamoyl-CoA-reductase genes from perennial ryegrass (Lolium perenne),” Plant Cell, vol. 22, no. 10, pp. 3357–3373, 2010.
[37]
E. Meyer, G. V. Aglyamova, S. Wang et al., “Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx,” BMC Genomics, vol. 10, article 219, 2009.
[38]
S. A. Flint-Garcia, J. M. Thornsberry, and S. B. Edward, “Structure of linkage disequilibrium in plants,” Annual Review of Plant Biology, vol. 54, pp. 357–374, 2003.
[39]
M. von Korff, H. Wang, J. Léon, and K. Pillen, “AB-QTL analysis in spring barley: II. Detection of favourable exotic alleles for agronomic traits introgressed from wild barley (H. vulgare ssp. spontaneum),” Theoretical and Applied Genetics, vol. 112, no. 7, pp. 1221–1231, 2006.
[40]
M. von Korff, S. Grando, A. Del Greco, D. This, M. Baum, and S. Ceccarelli, “Quantitative trait loci associated with adaptation to Mediterranean dryland conditions in barley,” Theoretical and Applied Genetics, vol. 117, no. 5, pp. 653–669, 2008.
[41]
P. Hedden, “The genes of the green revolution,” Trends in Genetics, vol. 19, no. 1, pp. 5–9, 2003.
[42]
T. Sakamoto and M. Matsuoka, “Identifying and exploiting grain yield genes in rice,” Current Opinion in Plant Biology, vol. 11, no. 2, pp. 209–214, 2008.
[43]
M. G. Salas Fernandez, P. W. Becraft, Y. Yin, and T. Lübberstedt, “From dwarves to giants? Plant height manipulation for biomass yield,” Trends in Plant Science, vol. 14, no. 8, pp. 454–461, 2009.
