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Plant Molecular Biology

, Volume 92, Issue 1–2, pp 71–88 | Cite as

Genome-wide identification and analysis of rice genes preferentially expressed in pollen at an early developmental stage

  • Tien Dung Nguyen
  • Sunok Moon
  • Van Ngoc Tuyet Nguyen
  • Yunsil Gho
  • Anil Kumar Nalini Chandran
  • Moon-Soo Soh
  • Jong Tae Song
  • Gynheung An
  • Sung Aeong Oh
  • Soon Ki ParkEmail author
  • Ki-Hong JungEmail author
Article

Abstract

Microspore production using endogenous developmental programs has not been well studied. The main limitation is the difficulty in identifying genes preferentially expressed in pollen grains at early stages. To overcome this limitation, we collected transcriptome data from anthers and microspore/pollen and performed meta-expression analysis. Subsequently, we identified 410 genes showing preferential expression patterns in early developing pollen samples of both japonica and indica cultivars. The expression patterns of these genes are distinguishable from genes showing pollen mother cell or tapetum-preferred expression patterns. Gene Ontology enrichment and MapMan analyses indicated that microspores in rice are closely linked with protein degradation, nucleotide metabolism, and DNA biosynthesis and regulation, while the pollen mother cell or tapetum are strongly associated with cell wall metabolism, lipid metabolism, secondary metabolism, and RNA biosynthesis and regulation. We also generated transgenic lines under the control of the promoters of eight microspore-preferred genes and confirmed the preferred expression patterns in plants using the GUS reporting system. Furthermore, cis-regulatory element analysis revealed that pollen specific elements such as POLLEN1LELAT52, and 5659BOXLELAT5659 were commonly identified in the promoter regions of eight rice genes with more frequency than estimation. Our study will provide new sights on early pollen development in rice, a model crop plant.

Keywords

GUS reporter system Microspore-preferred genes Rice cis-Regulatory element 

Notes

Acknowledgments

We appreciate the support of Dr. Pamela Ronald and Dr. Peijian Cao in developing the meta-expression profiling database for rice. This work was supported by the Next-Generation BioGreen21 Program of the Rural Development Administration in the Republic of Korea (PJ01100401 to KHJ and PJ01194201 to SKP), and by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology (NRF-2013R1A1A2006040 to KHJ).

Author contributions

T.D.N., S.M., S.K.P., G.A., M.S.S., J.T.S., and K.H.J. designed the research. T.D.N., S.M., A.K.N.C., V.N.T.N., Y.S.G., and S.A.O. performed experiments. T.D.N. and S.M. analyzed data. T.D.N., S.M., S.A.O., S.K.P., and K.H.J. wrote the manuscript.

Supplementary material

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Supplementary material 1 (PDF 3667 KB)
11103_2016_496_MOESM2_ESM.xlsx (181 kb)
Supplementary material 2 (XLSX 181 KB)
11103_2016_496_MOESM3_ESM.docx (12 kb)
Supplementary material 3 (DOCX 11 KB)

References

  1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alandete-Saez M, Ron M, McCormick S (2008) GEX3, expressed in the male gametophyte and in the egg cell of Arabidopsis thaliana, is essential for micropylar pollen tube guidance and plays a role during early embryogenesis. Mol Plant 1:586–598CrossRefPubMedGoogle Scholar
  3. Alandete-Saez M, Ron M, Leiboff S, McCormick S (2011) Arabidopsis thaliana GEX1 has dual functions in gametophyte development and early embryogenesis. Plant J 68:620–632CrossRefPubMedGoogle Scholar
  4. Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21:1453–1472CrossRefPubMedPubMedCentralGoogle Scholar
  5. Aya K, Suzuki G, Suwabe K, Hobo T, Takahashi H, Shiono K, Yano K, Tsutsumi N, Nakazono M, Nagamura Y, Matsuoka M, Watanabe M (2011) Comprehensive network analysis of anther-expressed genes in rice by the combination of 33 laser microdissection and 143 spatiotemporal microarrays. PLoS One 6:e26162CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bae HK, Kang HG, Kim GJ, Eu HJ, Oh SA, Song JT, Chung IK, Eun MY, Park SK (2010) Transgenic rice plants carrying RNA interference constructs of AOS (allene oxide synthase) genes show severe male sterility. Plant Breed 129:647–651CrossRefGoogle Scholar
  7. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Edgar R (2009) NCBI GEO: archive for high-throughput functional genomic data. Nucleic Acids Res 37:D885–D890 (database issue)CrossRefPubMedGoogle Scholar
  8. Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37:859–869CrossRefPubMedGoogle Scholar
  9. Becker JD, Boavida LC, Carneiro J, Haury M, Feijó JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4:879–887CrossRefPubMedPubMedCentralGoogle Scholar
  11. Binarova P, Straatman K, Hause B, Hause G, van Lammeren AAM (1993) Nuclear DNA synthesis during the induction of embryogenesis in cultured microspores and pollen of Brassica napus L. Theor Appl Genet 87:9–16CrossRefPubMedGoogle Scholar
  12. Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148:1168–1181CrossRefPubMedPubMedCentralGoogle Scholar
  13. Brownfield L, Hafidh S, Durbarry A, Khatab H, Sidorova A, Doerner P, Twell D (2009) Arabidopsis DUO POLLEN3 is a key regulator of male germline development and embryogenesis. Plant Cell 21:1940–1956CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cao P, Jung KH, Choi D, Hwang D, Zhu J, Ronald PC (2012) The rice oligonucleotide array database: an atlas of rice gene expression. Rice 5:17CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chandran AKN, Jung KH (2014) Resources for systems biology in rice. J Plant Biol 57:80–92CrossRefGoogle Scholar
  16. Chen G, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu YG, Sameri M, Li X, Zhao X, Liu Y, Li C, Ma X, Wang A, Nair S, Wang N, Miyao A, Sakuma S, Yamaji N, Zheng X, Nevo E (2011) An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad Sci USA 108:12354–12359CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cui R, Han J, Zhao S, Su K, Wu F, Du X, Xu Q, Chong K, Theissen G, Meng Z (2010) Functional conservation and diversification of class E floral homeotic genes in rice (Oryza sativa). Plant J 61:767–781CrossRefPubMedGoogle Scholar
  18. Deveshwar P, Bovill WD, Sharma R, Able JA, Kapoor S (2011) Analysis of anther transcriptomes to identify genes contributing to meiosis and male gametophyte development in rice. BMC Plant Biol 11:78CrossRefPubMedPubMedCentralGoogle Scholar
  19. Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 138:2124–2133CrossRefPubMedPubMedCentralGoogle Scholar
  20. Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J 18:4689–4699. doi: 10.1093/emboj/18.17.4689 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fehlberg V, Vieweg MF, Dohmann EM, Hohnjec N, Puhler A, Perlick AM, Kuster H (2005) The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. J Exp Bot 56:799–806CrossRefPubMedGoogle Scholar
  22. Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, Yamaki S, Tsuda K, Nagata T, Niihama M, Kato H, Kikuchi S, Hamada K, Mochizuki T, Ishimizu T, Iwai H, Tsutsumi N, Kurata N (2010) Rice expression atlas in reproductive development. Plant Cell Physiol 51:2060–2081CrossRefPubMedGoogle Scholar
  23. Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16:1077–1090CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gupta V, Khurana R, Tyagi AK (2007) Promoters of two anther-specific genes confer organ-specific gene expression in a stage-specific manner in transgenic systems. Plant Cell Rep 26:1919–1931CrossRefPubMedGoogle Scholar
  25. Han MJ, Jung KH, Yi G, Lee DY, An G (2006) Rice Immature Pollen 1 (RIP1) is a regulator of late pollen development. Plant Cell Physiol 47:1457–1472. doi: 10.1093/pcp/pcl013 CrossRefPubMedGoogle Scholar
  26. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucl Aacids Res 27:297–300CrossRefGoogle Scholar
  27. Hobo T, Suwabe K, Aya K, Suzuki G, Yano K, Ishimizu T, Fujita M, Kikuchi S, Hamada K, Miyano M, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Takahashi H, Shiono K, Nakazono M, Tsutsumi N, Nagamura Y, Kurata N, Watanabe M, Matsuoka M (2008) Various spatiotemporal expression profiles of anther-expressed genes in rice. Plant Cell Physiol 49:1417–1428CrossRefPubMedPubMedCentralGoogle Scholar
  28. Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652CrossRefPubMedPubMedCentralGoogle Scholar
  29. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hrubá P, Honys D, Twell D, Capková V, Tupý J (2005) Expression of beta-galactosidase and beta-xylosidase genes during microspore and pollen development. Planta 220:931–940CrossRefPubMedGoogle Scholar
  31. Jeon JS, Chung YY, Lee S, Yi GH, Oh BG, An G (1999) Isolation and characterization of an anther-specific gene, RA8, from rice (Oryza sativa L.) Plant Mol Biol 39:35–44CrossRefPubMedGoogle Scholar
  32. Jeong HJ, Jung KH (2015) Rice tissue-specific promoters and condition-dependent promoters for effective translational application. J Integr Plant Biol 57:913–924CrossRefPubMedGoogle Scholar
  33. Jung KH, An G (2012) Application of MapMan and RiceNet drives systematic analyses of the early heat stress transcriptome in rice seedlings. J Plant Biol 55:436–449CrossRefGoogle Scholar
  34. Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice undeveloped tapetum 1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kang HG, Jeon JS, Lee S ,An G (1998) Identification of class B and class C floral organ identity genes from rice plants. Plant Mol Biol 38:1021–1029CrossRefPubMedGoogle Scholar
  36. Khurana R, Kapoor S, Tyagi AK (2013) Spatial and temporal activity of upstream regulatory regions of rice anther-specific genes in transgenic rice and Arabidopsis. Transgenic Res 22:31–46CrossRefPubMedGoogle Scholar
  37. Kim DW, Lee SH, Choi SB, Won SK, Heo YK, Cho M, Park YI, Cho HT (2006) Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. Plant Cell 18:2958–2970CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ko SS, Li MJ, Sun-Ben Ku M, Ho YC, Lin YJ, Chuang MH, Hsing HX, Lien YC, Yang HT, Chang HC, Chan MT (2014) The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26:2486–2504CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kobayashi K, Maekawa M, Miyao A, Hirochika H, Kyozuka J (2010) PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice. Plant Cell Physiol 51:47–57CrossRefPubMedGoogle Scholar
  40. Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yoshida H, Nagamura Y, Kyozuka (2012) Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 24:1848–1859CrossRefPubMedPubMedCentralGoogle Scholar
  41. Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M, Kurata N, Nonomura K (2014) Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78:385–397CrossRefPubMedGoogle Scholar
  42. Lee S, Jung KH, An G, Chung YY (2004) Isolation and characterization of a rice cysteine protease gene, OsCP1, using T-DNA gene-trap system. Plant Mol Biol 54:755–765CrossRefPubMedGoogle Scholar
  43. Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhan DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014CrossRefPubMedPubMedCentralGoogle Scholar
  44. Li X, Yang Y, Yao J, Chen G, Li X, Zhang Q, Wu C (2009) FLEXIBLE CULM 1 encoding a cinnamyl-alcohol dehydrogenase controls culm mechanical strength in rice. Plant Mol Biol 69:685–689CrossRefPubMedGoogle Scholar
  45. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, Liang W, Zhang D (2010) Cytochrome P450 family member CYP704B2 catalyzes the Ñ -hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22:173–190CrossRefPubMedPubMedCentralGoogle Scholar
  46. Li H, Liang W, Hu Y, Zhu L, Yin C, Xu J, Dreni L, Kater MM, Zhang D (2011a) Rice MADS6 interacts with the floral homeotic genes SUPERWOMAN1, MADS3, MADS58, MADS13, and DROOPING LEAF in specifying floral organ identities and meristem fate. Plant Cell 23:2536–2552CrossRefPubMedPubMedCentralGoogle Scholar
  47. Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011b) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630CrossRefPubMedPubMedCentralGoogle Scholar
  48. Li J, Yuan J, Li M (2014) Characterization of putative cis-regulatory elements in genes preferentially expressed in Arabidopsis male meiocytes. BioMed Res Int 708364Google Scholar
  49. Liu X, Shangguan Y, Zhu J, Lu Y, Han B (2013) The rice OsLTP6 gene promoter directs anther-specific expression by a combination of positive and negative regulatory elements. Planta 238:845–857CrossRefPubMedGoogle Scholar
  50. Luo H, Lee JY, Hu Q, Nelson-Vasilchik K, Eitas TK, Lickwar C, Kausch AP, Chandlee JM, Hodges TK (2006) RTS, a rice anther-specific gene is required for male fertility and its promoter sequence directs tissue-specific gene expression in different plant species. Plant Mol Biol 62:397–408CrossRefPubMedGoogle Scholar
  51. Mehrotra R, Sethi S, Zutshi I, Bhalothia P, Mehrotra S (2013) Patterns and evolution of ACGT repeat cis-element landscape across four plant genomes. BMC Genomics 14:203CrossRefPubMedPubMedCentralGoogle Scholar
  52. Nguyen TD, Oo MM, Moon S, Bae HK, Oh SA, Soh MS, Song JT, Kim JH, Jung KH, Park SK (2015) Expression analysis of two rice pollen-specific promoters using homologous and heterologous systems. Plant Biotechnol Rep 9:297–306CrossRefGoogle Scholar
  53. Niu N, Liang W, Yang X, Jin W, Wilson ZA, Hu J, Zhang D (2013) EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat Commun 4:1445CrossRefPubMedGoogle Scholar
  54. Oldenhof MT, de Groot PFM, Visser JH, Schrauwen JAM, Wullems GJ (1996) Isolation and characterization of a microspore-specific gene from tobacco. Plant Mol Biol 31:213–225CrossRefPubMedGoogle Scholar
  55. Oo MM, Bae HK, Nguyen TD, Moon S, Oh SA, Kim JH, Soh MS, Song JT, Jung KH, Park SK (2014) Evaluation of rice promoters conferring pollen-specific expression in a heterologous system, Arabidopsis. Plant Reprod 27:47–58CrossRefPubMedGoogle Scholar
  56. Park JI, Hakozaki H, Endo M, Takada Y, Ito H, Uchida M, Okabe T, Watanabe M (2006) Molecular characterization of mature pollen-specific genes encoding novel small cysteine-rich proteins in rice (Oryza sativa L.). Plant Cell Rep 25:466–474CrossRefPubMedGoogle Scholar
  57. Pretova A, De Ruijter NCA, Van Lammeren AAM, Schel JHN (1993) Structural observations during androgenic microspore culture of the 4 cl genotype of Zea mays L. Euphytica 65:61–69CrossRefGoogle Scholar
  58. Qiu D, Xiao J, Xie W, Liu H, Li X, Xiong L, Wang S (2008) Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant 1:538–551PubMedGoogle Scholar
  59. Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134:1718–1732CrossRefPubMedPubMedCentralGoogle Scholar
  60. Rogers HJ, Bate N, Combe J, Sullivan J, Sweetman J, Swan C, Lonsdale DM, Twell D (2001) Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 45:577–585CrossRefPubMedGoogle Scholar
  61. Russell SD, Gou X, Wong CE, Wang X, Yuan T, Wei X, Bhalla PL, Singh MB (2012) Genomic profiling of rice sperm cell transcripts reveals conserved and distinct elements in the flowering plant male germ lineage. New Phytol 195(3):560–573CrossRefPubMedGoogle Scholar
  62. Sakai H, Aoyama T, Oka A (2000) Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J 24:703–711CrossRefPubMedGoogle Scholar
  63. Schunmann PH, Richardson AE, Vickers CE, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiol 136:4205–4214CrossRefPubMedPubMedCentralGoogle Scholar
  64. Secco D, Baumann A, Poirier Y (2010) Characterization of the rice PHO1 gene family reveals a key role for OsPHO1;2 in phosphate homeostasis and the evolution of a distinct clade in dicotyledons. Plant Physiol 152:1693–1704CrossRefPubMedPubMedCentralGoogle Scholar
  65. Shen Y, Tang D, Wang K, Wang M, Huang J, Luo W, Luo Q, Hong L, Li M, Cheng Z (2012). ZIP4 in homologous chromosome synapsis and crossover formation in rice meiosis. J Cell Sci 125:2581–91CrossRefPubMedGoogle Scholar
  66. Shi J, Tan H, Yu XH, Liu Y, Liang W, Ranathunge K, Franke RB, Schreiber L, Wang Y, Kai G, Shanklin J, Ma H, Zhang D (2011) Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23:2225–2246CrossRefPubMedPubMedCentralGoogle Scholar
  67. Shirsat A, Wilford N, Croy R, Boulter D (1989) Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco. Mol Gen Genet 215:326–331CrossRefPubMedGoogle Scholar
  68. Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270CrossRefPubMedGoogle Scholar
  69. Sobkowiak L, Bielewicz D, Malecka EM, Jakobsen I, Albrechtsen M, Szweykowska-Kulinska Z, Pacak A (2012) The role of the P1BS element containing promoter-driven genes in Pi transport and homeostasis in plants. Front. Plant Sci 3:58Google Scholar
  70. Song X, Li P, Zhai J, Zhou M, Ma L, Liu B, Jeong DH, Nakano M, Cao S, Liu C, Chu C, Wang XJ, Green PJ, Meyers BC, Cao X (2012) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69:462–474CrossRefPubMedGoogle Scholar
  71. Suwabe K, Suzuki G, Takahashi H, Shiono K, Endo M, Yano K, Fujita M, Masuko H, Saito H, Fujioka T, Kaneko F, Kazama T, Mizuta Y, Kawagishi-Kobayashi M, Tsutsumi N, Kurata N, Nakazono M, Watanabe M (2008) Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray. Plant Cell Physiol 49:1407–1416CrossRefPubMedPubMedCentralGoogle Scholar
  72. Swapna L, Khurana R, Kumar SV, Tyagi AK, Rao KV (2011) Pollen-specific expression of Oryza sativa indica pollen allergen gene (OSIPA) promoter in rice and Arabidopsis transgenic systems. Mol Biotechnol 48:49–59CrossRefPubMedGoogle Scholar
  73. Takehisa H, Sato Y, Igarashi M, Abiko T, Antonio BA, Kamatsuki K, Minami H, Namiki N, Inukai Y, Nakazono M, Nagamura Y (2012) Genome-wide transcriptome dissection of the rice root system: implications for developmental and physiological functions. Plant J 69:126–140CrossRefPubMedGoogle Scholar
  74. Tan H, Liang W, Hu J, Zhang D (2012) MTR1 encodes a secretory fasciclin glycoprotein required for male reproductive development in rice. Dev Cell 22:1127–1137CrossRefPubMedGoogle Scholar
  75. Thangasamy S, Chen PW, Lai MH, Chen J, Jauh GY (2012) Rice LGD1 containing RNA binding activity affects growth and development through alternative promoters. Plant J 71:288–302CrossRefPubMedGoogle Scholar
  76. Thilmony R, Guttman M, Thomson JG, Blechl AE (2009) The LP2 leucine-rich repeat receptor kinase gene promoter directs organ-specific, light-responsive expression in transgenic rice. Plant Biotechnol J 7:867–882CrossRefPubMedGoogle Scholar
  77. Tseng IC, Hong CY, Yu SM, Ho TH (2013) Abscisic acid- and stress-induced highly proline-rich glycoproteins regulate root growth in rice. Plant Physiol 163:118–134CrossRefPubMedPubMedCentralGoogle Scholar
  78. Tsuchiya T, Toriyama K, Nasrallah ME, Ejiri S (1992) Isolation of genes abundantly expressed in rice anthers at the microspore stage. Plant Mol Biol 20:1189–1193CrossRefGoogle Scholar
  79. Twell D, Yamaguchi J, Wing RA, Ushiba J, McCormick S (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev 5:496–507CrossRefPubMedGoogle Scholar
  80. Wang E, Wang J, Zhu X, Hao W, Wang L, Li Q, Zhang L, He W, Lu B, Lin H, Ma H, Zhang G, He Z (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370–1374CrossRefPubMedGoogle Scholar
  81. Wang S, Zhang G, Song Q, Zhang Y, Li Z, Guo J et al (2015) Abnormal development of tapetum and microspores induced by chemical hybridization agent SQ-1 in wheat. PLoS ONE 10:e0119557CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wei LQ, Xu WY, Deng ZY, Su Z, Xue Y, Wang T (2010) Genome-scale analysis and comparison of gene expression profiles in developing and germinated pollen in Oryza sativa. BMC Genomics 11:338CrossRefPubMedCentralGoogle Scholar
  83. Welchen E, Gonzalez DH (2005) Differential expression of the Arabidopsis cytochrome c genes Cytc-1 and Cytc-2. Evidence for the involvement of TCP-domain protein-binding elements in anther- and meristem-specific expression of the Cytc-1 gene. Plant Physiol 139:88–100CrossRefPubMedPubMedCentralGoogle Scholar
  84. Yamamoto E, Yonemaru J-I, Yamamoto T, Yano M (2012) OGRO: the overview of functionally characterized genes in rice online database. Rice 5:1–10CrossRefGoogle Scholar
  85. Yanagisawa S (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 21:281–288CrossRefPubMedGoogle Scholar
  86. Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391CrossRefPubMedGoogle Scholar
  87. Yanagisawa S, Schmidt RJ (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J 17:209–214CrossRefPubMedGoogle Scholar
  88. Yang J, Zhao X, Cheng K, Du H, Ouyang Y, Chen J, Qiu S, Huang J, Jiang Y, Jiang L, Ding J, Wang J, Xu C, Li X, Zhang Q (2012) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336–1340CrossRefPubMedGoogle Scholar
  89. Yi J, Moon S, Lee YS, Zhu L, Liang W, Zhang D, Jung KH, An G (2016) Defective tapetum cell death 1 (DTC1) regulates ROS levels by binding to metallothionein during tapetum Degeneration. Plant Physiol 170:1611–1623PubMedGoogle Scholar
  90. Yokoi S, Tsuchiya T, Toriyama K, Hinata K (1997) Tapetum-specific expression of the Osg6B promoter-β-glucuronidase gene in transgenic rice. Plant Cell Rep 16:363–367Google Scholar
  91. Zhang H, Liang W, Yang X, Luo X, Jiang N, Ma H, Zhang D (2010a) Carbon starved anther encodes a MYB domain protein that regulates sugar partitioning required for rice pollen development. Plant Cell 22:672–689CrossRefPubMedPubMedCentralGoogle Scholar
  92. Zhang J, Nallamilli BR, Mujahid H, Peng Z (2010b) OsMADS6 plays an essential role in endosperm nutrient accumulation and is subject to epigenetic regulation in rice (Oryza sativa). Plant J 64:604–617CrossRefPubMedGoogle Scholar
  93. Zhu L, Shi J, Zhao G, Zhang D, Liang W (2013) Post-meiotic Deficient Anther1 (PDA1) encodes an ABC transporter required for the development of anther cuticle and pollen exine in rice. J Plant Biol 56:59–68CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Tien Dung Nguyen
    • 1
  • Sunok Moon
    • 2
  • Van Ngoc Tuyet Nguyen
    • 2
  • Yunsil Gho
    • 2
  • Anil Kumar Nalini Chandran
    • 2
  • Moon-Soo Soh
    • 3
  • Jong Tae Song
    • 1
  • Gynheung An
    • 2
  • Sung Aeong Oh
    • 1
  • Soon Ki Park
    • 1
    Email author
  • Ki-Hong Jung
    • 2
    Email author
  1. 1.School of Applied BiosciencesKyungpook National UniversityDaeguRepublic of Korea
  2. 2.Graduate School of Biotechnology and Crop Biotech InstituteKyung Hee UniversityYonginRepublic of Korea
  3. 3.Department of Molecular BiologySejong UniversitySeoulRepublic of Korea

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