Abstract
Chromosomal segments from wild rice species Oryza rufipogon, introgressed into an elite indica rice restorer line (KMR3) using molecular markers, resulted in significant increase in yield. Here we report the transcriptome analysis of flag leaves and fully emerged young panicles of one of the high yielding introgression lines IL50-7 in comparison to KMR3. A 66-fold upregulated gene Os11Gsk, which showed no transcript in KMR3 was highly expressed in O. rufipogon and IL50-7. A 5-kb genomic region including Os11Gsk and its flanking regions could be PCR amplified only from IL50-7, O. rufipogon, japonica varieties of rice-Nipponbare and Kitaake but not from the indica varieties, KMR3 and Taichung Native-1. Three sister lines of IL50-7 yielding higher than KMR3 showed presence of Os11Gsk, whereas the gene was absent in three other ILs from the same cross having lower yield than KMR3, indicating an association of the presence of Os11Gsk with high yield. Southern analysis showed additional bands in the genomic DNA of O. rufipogon and IL50-7 with Os11Gsk probe. Genomic sequence analysis of ten highly co-expressed differentially regulated genes revealed that two upregulated genes in IL50-7 were derived from O. rufipogon and most of the downregulated genes were either from KMR3 or common to KMR3, IL50-7, and O. rufipogon. Thus, we show that Os11Gsk is a wild rice-derived gene introduced in KMR3 background and increases yield either by regulating expression of functional genes sharing homology with it or by causing epigenetic modifications in the introgression line.
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Alexa A, Rahnenf uhrer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22(13):1600–1607
Ali ML, Sanchez PL, Yu SB, Lorieux M, Eizenga GC (2010) Chromosome segment substitution lines: a powerful tool for the introgression of valuable genes from Oryza wild species into cultivated rice (O. sativa). Rice 3:218–234
Ashikari M, Sakakibara H, Lin S, Yamamoto T, Takashi T, Nishimura A, Enrique R, Qian Q, Hidemi K, Makoto M (2005) Cytokinin oxidase regulates rice grain production. Science 309:741–745
Babu AP, Ramesha MS, Sudhakar T, Reddy CS, Swamy BPM, Viraktamath BC Sarla N (2009) Marker assisted introgression of QTL yld2.1 or sub QTL regions from O. rufipogon increases yield of KMR3 and derived hybrids. Proceedings of the 7th International Symposium on Rice Functional Genomics, November 16-19, 2009, International Rice Research Institute, pp: 44
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300
Bentsink L, Hanson J, Hanhart CJ, Vries HB, Coltrane C, Keizer P, El-Lithy M, Blanco CA, Andrés MT, Reymond M, Eeuwijk F, Smeekens S, Koornneef M (2010) Natural variation for seed dormancy in Arabidopsis is regulated by additive genetic and molecular pathways. PNAS 107(9):4264–4269
Boutrot F, Chantret N, Gautier MF (2008) Genome-wide analysis of the rice and arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics 9:86
Brar DS, Khush GS (1997) Alien introgression in rice. Plant Mol Biol 35:35–47
Buhot N, Douliez JP, Jacquemard A, Marion D, Tran V, Maume B, Milat ML, Ponchet M, Mikes V, Kader JC, Blein JP (2001) A lipid transfer protein binds to a receptor involved in the control of plant defence responses. FEBS Lett 509(1):27–30
Cho S, Garvin DF, Muehlbauer GJ (2006) Transcriptome analysis and physical mapping of barley genes in wheat–barley chromosome addition lines. Genetics 172:1277–1285
Chung Y, Maharjan PM, Lee O, Fujioka S, Jang S, Kim B, Takatsuto S, Tsujimoto M, Kim H, Cho S, Park T, Cho H, Hwang I, Choe S (2011) Auxin stimulates DWARF4 expression and brassinosteroid biosynthesis in Arabidopsis. The Plant J 66:564–578
Clouse SD (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. The Plant Cell 23:1219–1230
d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Simon M, Jenczewski E, Mercier R (2008) Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains. PLoS Genet 4(e1000274)
De Paepe A, Vuylsteke M, Van Hummelen P, Zabeau M, Van Der Straeten D (2004) Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J 39:537–59, Erratum in: 2008. Plant J. 56:180
Deng QY, Chen LY, Deng HB, Zhuang W, Xiong YD (2006) Yield-increasing effect of yield-enhancing QTL from Oryza rufipogon after being transferred into late-season rice restorer line. Mol Plant Breeding 4:59–64
Divi UK, Krishna P (2009) Brassinosteroid: a biotechnological target for enhancing crop yield and stress tolerance. New Biotechnol 26:131–136
Dornelas MC, van Lammeren AAM, Kreis M (2000) Arabidopsis thaliana SHAGGY-related protein kinases (AtSK11 and 12) function in perianth and gynoecium development. Plant J 21:419–429
Edqvist J, Farbos I (2002) Characterization of germination-specific lipid transfer proteins from Euphorbia lagascae. Planta 215:41–50
Endo M, Tsuchiya T, Saito H, Matsubara H, Hakozaki H, Masuko H et al (2004) Identification and molecular characterization of novel anther-specific genes in japonica rice, Oryza sativa L. by using cDNA microarray. Genes Genet Syst 79:213–226
Fu Q, Zhang P, Tan L, Zhu Z, Ma D, Fu Y, Zhan X, Cai H, Sun C (2010) Analysis of QTLs for yield-related traits in Yuanjiang common wild rice (Oryza rufipogon Griff.). J Gen Genomics 37:147–1
Gur A, Semel Y, Osorio S, Friedmann M, Seekh S, Ghareeb B, Mohammad A, Pleban T, Gera G, Fernie AR, Zamir D (2011) Yield quantitative trait loci from wild tomato are predominately expressed by the shoot. Theor Appl Genet 122:405–420
Han FP, Liu ZL, Tan M, Hao S, Fedak G, Liu B (2004) Mobilized retrotransposon Tos17 of rice by alien DNA introgression transposes into genes and causes structural and methylation alterations of a flanking genomic region. Hereditas 141:243–251
He GM, Luo X, Tian F, Li K, Zhu Z, Su W (2006) Haplotype variation in structure and expression of a gene cluster associated with a quantitative trait locus for improved yield in rice. Genome Res 16:618–626
Huang YI, Zhang L, Zhang J, Yuan D, Xu C, Li X, Zhou D, Wang S, Zhang Q (2006) Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs. Plant Mol Biol 62:579–591
Jansen RC, Nap JP (2001) Genetical genomics: the added value from segregation. Trends Genet 17:388–391
Jeon JS, Jung KH, Kim HB, Suh JP, Khush GS (2011) Genetic and molecular insights into the enhancement of rice yield potential. J Plant Biol 54:1–9
Jung KH, Dardick C, Bartley LE, Cao P, Phetsom J, Canlas P, Seo YS, Shultz M, Ouyang S, Yuan Q et al (2008) Refinement of light-responsive transcript lists using rice Oligonucleotide arrays: evaluation of gene-redundancy. PLoS One 3(10):e3337
Kamenetzky L, Asıs R, Bassi S, de Godoy F, Bermu dez L, Fernie AR, Van Sluys MA, Julia Vrebalov J, Giovannoni JJ, Rossi M, Carrari F (2010) Genomic analysis of wild tomato introgressions. Determining metabolism and yield-associated traits. Plant Physiol 152:1772–1786
Katsumi M (1985) Interaction of a brassinosteroid with IAA and GA3 in the elongation of cucumber hypocotyl sections. Plant Cell Physiol 26:615–625
Kim TW, Shenheng Guan S, Sun Y, Deng Z, Tang W, Shang JX, Ying Sun Y, Burlingame AL, Wang ZY (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nature Cell Biol 11:1254–1260
Koh S, Lee SC, Kim MK, Koh JH, Lee S, An G, Choe S, Kim SE (2007) T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsisi BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol Biol 65:453–466
Kondou H, Ooka H, Yamada H, Satoh K, Kikuchi S, Takahara Y, Yamamoto K (2006) Microarray analysis of gene expression at initial stages of rice seed development. Breeding Sci 56(3):235–242
Laitinen RAE, Immanen J, Auvinen P (2005) Analysis of the floral transcriptome uncovers new regulators of organ determination and gene families related to flower organ differentiation in Gerbera hybrida (Asteraceae). Genome Res 15:475–486
Lee T-H, Kim Y-K, Pham TTM, Song SI, Kim J-K, Kang KY, An G, Jung K-H, Galbraith DW, Kim M, Yoon U-H, Nahm BH (2009) RiceArrayNet: a database for correlating gene expression from transcriptome profiling, and its application to the analysis of coexpressed genes in rice. Plany Physiol 151:16–33
Lee I, Seob Y-S, Coltraneb D, Hwanga S, Oha T, Marcottec EM, Ronald PC (2011) Genetic dissection of the biotic stress response using a genome-scale gene network for rice. PNAS 108:18548–18553
Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16:596–615
Liang F, Deng Q, Wang Y, Xiong Y, Jin D, Li J, Wang B (2004) Molecular marker-assisted selection for yield-enhancing genes in the progeny of “9311 × O. rufipogon” using SSR. Euphytica 139:159–165
Lin M, Hu B, Chen L, Sun P, Fan Y, Wu P, Chen X (2009) Computational identification of potential molecular interactions in Arabidopsis. Plant Physiol 151(1):34–46
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCt method. Methods 25:402–408
Luo X, Wu S, Tian F, Xin X, Zha X, Dong X, Fu Y, Wang X, Yang J, Sun C (2011) Identification of heterotic loci associated with yield-related traits in Chinese common wild rice (Oryza rufipogon Griff). Plant Science 181:14–22
Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A predicted lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419:399–403
Marathe R, Guan Z, Anandalakshmi R, Zhao H, Dinesh-Kumar SP (2004) Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Mol Biol 55:501–520
Marri PR, Sarla N, Reddy LV, Siddiq EA (2005) Identification and mapping of yield and yield related QTLs from an Indian accession of Oryza rufipogon. BMC Genet 6:33
Moncada P, Martinez CP, Borrero J, Chatel M, Gauch HJ, Guimaraes E, Tohme J, McCouch SR (2001) Quantitative trait loci for yield and yield components in an Oryza sativa × Oryza rufipogon BC2F2 population evaluated in an upland environment. Theor Appl Genet 102:41–52
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Mussig C, Fischer S, Altmann T (2002) Brassinosteroid-regulated gene expression. Plant Physiol 129:1241–1251
Pandit A, Rai V, Bal S, Sinha S, Kumar V, Chauhan M, Gautam RK, Singh R, Sharma PC, Singh AK, Gaikwad K, Sharma TR, Mohapatra T, Singh NK (2010) Combining QTL mapping and transcriptome profiling of bulked RILs for identification of functional polymorphism for salt tolerance genes in rice (Oryza sativa L.). Mol Genet Genomics 284:121–136
Peng Z-Y, Zhang TL, Dzikiewicz KM, Li S, Wang X, Hu G, Zhu Z, Wei X (2009) Characterization of the genome expression trends in the heading-stage panicle of six rice lineages. Genomics 93:169–178
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Shinozaki KY (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767
Sarla N, Mallikarjuna Swamy BP, Sudhakar T, Prasad Babu A, Kaladhar K, Surendhar Reddy C, Ashok Reddy G, Ramesha MS, Shobha Rani N and Viraktamath (2009) High yielding rice lines from elite × wild crosses. 2009. Directorate of Rice Research, News letter, Vol.7 No.2
Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Shinozaki KY, Carninci P, Kawai J, Hayashizaki Y, Kazuo Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. The Plant J 31:279–292
Swamy BPM, Sarla N (2008) Yield-enhancing quantitative trait loci (QTLs) from wild species. Biotechnol Adv 26:106–120
Swamy BPM, Sarla N (2011) Meta-analysis of yield QTLs derived from inter-specific crosses of rice reveals consensus regions and candidate genes. Plant Mol Biol Rep 29:663–680
Swamy BPM, Kaladhar K, Ramesha MS, Viraktamath BC, Sarla N (2011) Molecular mapping of QTLs for yield and yield-related traits in Oryza sativa cv Swarna×O. nivara (IRGC81848) backcross population. Rice Science 18:178–186
Swanson-Wagner R, Eichten SR, Kumari S (2010) Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor. Genome Res. doi:10.1101/gr.109165.110
Takabayashi A, Ishikawa N, Obayashi T, Ishida S, Obokata J, Endo T, Sato F (2009) Three novel subunits of Arabidopsis chloroplastic NAD(P)H dehydrogenase identified by bioinformatic and reverse genetic approaches. The Plant J 57:207–219
Tanksley SD, Mc Couch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277:1063–1066
Thomson MJ, Tai TH, McClung AM, Lai XH, Hinga ME, Lobos KB, Xu Y, Martinez CP, McCouch SR (2003) Mapping quantitative trait loci for yield, yield components and morphological traits in an advanced backcross population between Oryza rufipogon and the Oryza sativa cultivar Jefferson. Theor Appl Genet 107:479–493
Tian F, Li DJ, Fu Q, Zhu ZF, Fu YC, Wang XK (2006) Construction of introgression lines carrying wild rice (Oryza rufipogon Griff.) segments in cultivated rice (Oryza sativa L.) background and characterization of introgressed segments associated with yield related traits. Theor Appl Genet 112:570–80
Tichtinsky G, Tavares R, Takvorian A, Schwebel Dugue N, Twell D, Kreis M (1998) An evolutionary conserved group of plant GSK-3/shaggy-like protein kinase genes preferentially expressed in developing pollen. Biochim Biophys Acta 1442:261–273
Walia H, Wilson C, Zeng L, Ismail AM, Condamine P, Close TJ (2007) Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant Mol Biol 63:609–623
Wang YM, Dong ZY, Zhang ZJ, Lin XY, Shen Y, Zhou D, Liu B (2005) Extensive denovo variation in rice induced by introgression from wild rice (Zizania latifolia ). Genetics 170:1945–1956
Wang N, Wang H et al (2010) Transpositional reactivation of the Dart transposon family in rice lines derived from introgressive hybridization with Zizania latifolia. BMC Plant Biol 10:190
Wei G, Tao Y, Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, Li X, Song G et al (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. PNAS 106:7695–7701
Woeste KE, Vogel JP, Kieber JJ (1999) Factors regulating ethylene biosynthesis in etiolated Arabidopsis thaliana seedlings. Physiol Plant 105:478–484
Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. The Plant Cell 4:759–771
Wu X (2009) Prospects of developing hybrid rice with super high yield. Agron J 101(3688)
Xiao J, Grandillo S, Ahn SN, Mc Couch SR, Tanksley SD, Li J, Yuan L (1996) Genes from wild rice improve yield. Nature 384:223–224
Xiao J, Li J, Grandillo S, Ahn SN, Yuan L, Tanksley SD, Mc Couch SR (1998) Identification of trait improving quantitative trait loci alleles from a wild rice relative Oryza rufipogon. Genetics 150:899–909
Yamakawa H, Hirose T, Kuroda M, Yamaguchi T (2007) Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiol 144:258–277
Yang GX, Jan A, Shen SH, Yazaki J, Ishikawa M, Shimatani Z, Kishimoto N, Kikuchi S, Matsumoto H, Komatsu S (2004) Microarray analysis of brassinosteroids and gibberellin regulated gene expression in rice seedlings. Mol Gen Genomics 271:468–478
Zalewski W, Galuszka P, Gasparis S, Orczyk W, Nadolska Orczyk A (2010) Silencing of the HvCKX1 gene decreases the cytokinin oxidase/dehydrogenase level in barley and leads to higher plant productivity. J Exp Bot 61:1839–1851
Zhang Q, Lin SC, Zho BY, Wang CL, Yang WC, Zhou YL, Li DY, Chen CB, Zhu LH (1998) Identification and tagging a new gene for resistance to bacterial blight (Xanthomonas orzyae pv. oryzae) from O. rufipogon. Rice Genet Newsl 15:138–142
Zhang HY, He H, Chen LB, Li L, Liang MZ, Wang XF, Liu XG, He GM, Chen RS, Ma LG, Deng XW (2008) A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol Plant 1:720–731
Zhong G, Burns JK (2003) Profiling ethylene-regulated gene expression in Arabidopsis thaliana by microarray analysis. Plant Mol Biol 53:117–131
Acknowledgments
This work and ST were supported by a DBT grant to NS [DBT No.BT/AD/FG-2(PH-II)2009]. AKB was funded by Indian Council for Agricultural Research project 3019 (NPTC/FG/05/2672/33). We acknowledge the contributions of A Prasad Babu, C Surendhar Reddy, and BP Mallikarjuna Swamy in earlier work on developing and evaluating introgression lines and marker aided selection. We thank Project Director, DRR for the encouragement. We thank G. Haritha and N. Naga Deepthi for help in identifying polymorphic markers. The authors are thankful to the Sequencing laboratory CCMB, India for providing the sequencing facility used for this study.
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The microarray data have been submitted to the GEO repository and assigned GEO accession number. GSE30487. It was released on the 31st of December 2011.
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Thalapati, S., Batchu, A.K., Neelamraju, S. et al. Os11Gsk gene from a wild rice, Oryza rufipogon improves yield in rice. Funct Integr Genomics 12, 277–289 (2012). https://doi.org/10.1007/s10142-012-0265-4
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DOI: https://doi.org/10.1007/s10142-012-0265-4