Comparative analysis of anther transcriptome profiles of two different rice male sterile lines genotypes under cold stress

International Journal of Molecular Sciences

Volumn 16, Issue 5, 2015, Pages 11398-11416

  Bai, Bin ^a,b   Wu, Jun ^a,b   Sheng, Wen Tao ^a,b   Zhou, B ^c   Zhou, Li Jie ^a,b   Zhuang, Wen ^b   Yao, Dong Ping ^b,d   Deng, Qi Yun ^a,b,d  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b Hunan Hybrid Rice Research Center   (China)

^c INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

^d HUNAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Anther; Cold stress; PTGMS rice; RNA seq; Transcriptome

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALMODULIN; TRANSCRIPTOME; ZINC FINGER PROTEIN; PLANT RNA;

ANALYSIS OF VARIANCE; ANTHER; ARTICLE; BIOINFORMATICS; CELL LINE; COLD STRESS; CONTROLLED STUDY; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ANALYSIS; GENOTYPE; HUMIDITY; KYOTO ENCYCLOPEDIA OF GENE AND GENOME ANALYSIS; METABOLISM; NONHUMAN; PHOTO THERMO SENSITIVE GENIC MALE STERILE LINE RICE; PLANT GROWTH; PLANT REPRODUCTION; POLLEN; QUALITY CONTROL; QUANTITATIVE TRAIT LOCUS; REAL TIME POLYMERASE CHAIN REACTION; RICE; RNA ISOLATION; RNA SEQUENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; CLUSTER ANALYSIS; COLD; GENETICS; ISOLATION AND PURIFICATION; ORYZA; PLANT GENE; SEQUENCE ANALYSIS;

ORYZA;

CLUSTER ANALYSIS; COLD TEMPERATURE; GENES, PLANT; GENOTYPE; ORYZA; QUANTITATIVE TRAIT LOCI; REAL-TIME POLYMERASE CHAIN REACTION; RNA, PLANT; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84930666553     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160511398     Document Type: Article

References (67)

1. Imin, N.K.T.; Weinman, J.J.; Rolfe, B.G. Low temperature treatment at the young microspore stage induces protein changes in rice anthers. Mol. Cell. Proteomics 2006, 5, 274–292.
2. Chinnusamy, V.; Zhu, J.; Zhu, J.K. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007, 12, 444–451.
3. Ito, Y.; Katsura, K.; Maruyama, K.; Taji, T.; Kobayashi, M.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol. 2006, 47, 141–153.
4. Maruyama, K.; Todaka, D.; Mizoi, J.; Yoshida, T.; Kidokoro, S.; Matsukura, S.; Takasaki, H.; Sakurai, T.; Yamamoto, Y.Y.; Yoshiwara, K.; et al. Identification of cis-acting promoter elements in cold- and dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res. 2012, 19, 37–49.
5. Rabbani, M.A.; Maruyama, K.; Abe, H.; Khan, M.A.; Katsura, K.; Ito, Y.; Yoshiwara, K.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. 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. 2003, 133, 1755–1767.
6. Cheng, C.; Yun, K.Y.; Ressom, H.W.; Mohanty, B.; Bajic, V.B.; Jia, Y.; Yun, S.J.; de los Reyes, B.G. An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genomics 2007, 8, 175.
7. Yun, K.; Park, M.R.; Mohanty, B.; Herath, V.; Xu, F.Y.; Mauleon, R.; Wijaya, E.; Bajic, V.B.; Bruskiewich, R.; Reyes, B.G. Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol. 2010, 10, 16.
8. Takasaki, H.; Maruyama, K.; Kidokoro, S.; Ito, Y.; Fujita, Y.; Shinozaki, K.; Yamaguchi-Shinozaki, K.; Nakashima, K. The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol. Genet. Genomics 2010, 284, 173–183.
9. Zhang, T.; Zhao, X.; Wang, W.; Pan, Y.; Huang, L.; Liu, X.; Zong, Y.; Zhu, L.; Yang, D.; Fu, B. Comparative transcriptome profiling of chilling stress responsiveness in two contrasting rice genotypes. PLoS ONE 2012, 7, e43274.
10. Okoniewski, M.J.; Miller, C.J. Hybridization interactions between probesets in short oligo microarrays lead to spurious correlations. BMC Bioinform. 2006, 7, 276.
11. Royce, T.E.; Rozowsky, J.S.; Gerstein, M.B. Toward a universal microarray: Prediction of gene expression through nearest-neighbor probe sequence identification. Nucleic Acids Res. 2007, 35, e99.
12. Wang, Z.; Gerstein, M.; Snyder, M. RNA-Seq: A revolutionary tool for transcriptomics. Nat. Rev. Genet. 2009, 10, 57–63.
13. He, G.; Zhu, X.; Elling, A.A.; Chen, L.; Wang, X.; Guo, L.; Liang, M.; He, H.; Zhang, H.; Chen, F.; et al. Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 2010, 22, 17–33.
14. Lu, T.; Lu, G.; Fan, D.; Zhu, C.; Li, W.; Zhao, Q.; Feng, Q.; Zhao, Y.; Guo, Y.; Huang, X.; et al. Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res. 2010, 20, 1238–1249.
15. Mizuno, H.; Kawahara, Y.; Sakai, H.; Kanamori, H.; Wakimoto, H.; Yamagata, H.; Oono, Y.; Wu, J.; Ikawa, H.; Itoh, T.; et al. Massive parallel sequencing of mRNA in identification of unannotated salinity stress-inducible transcripts in rice (Oryza sativa L.). BMC Genomics 2010, 11, 683.
16. Zhang, G.; Guo, G.; Hu, X.; Zhang, Y.; Li, Q.; Li, R.; Zhuang, R.; Lu, Z.; He, Z.; Fang, X.; et al. Deep RNA sequencing at single base-pair resolution reveals high complexity of the rice transcriptome. Genome Res. 2010, 20, 646–654.
17. Oono, Y.; Kawahara, Y.; Kanamori, H.; Mizuno, H.; Yamagata, H.; Yamamoto, M.; Hosokawa, S.; Ikawa, H.; Akahane, I.; Zhu, Z.; et al. mRNA-Seq reveals a comprehensive transcriptome profile of rice under phosphate stress. Rice 2011, 4, 50–65.
18. Ji, H.; Gheysen, G.; Denil, S.; Lindsey, K.; Topping, J.F.; Nahar, K.; Haegeman, A.; de Vos, W.H.; Trooskens, G.; van Criekinge, W.; et al. Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots. J. Exp. Bot. 2013, 64, 3885–3898.
19. Venu, R.C.; Sreerekha, M.V.; Sheshu Madhav, M.; Nobuta, K.; Mohan, K.M.; Chen, S.; Jia, Y.; Meyers, B.C.; Wang, G.-L. Deep transcriptome sequencing reveals the expression of key functional and regulatory genes involved in the abiotic stress signaling pathways in rice. J. Plant Biol. 2013, 56, 216–231.
20. Si, H.M.; Liu, W.Z.; Fu, Y.P.; Song, Z.X.; Hu, G.C. Current situation and suggestions for development of two-line hybrid rice in China. Chin. J. Rice Sci. 2011, 25, 544–552.
21. Deng, Q.Y.; Yuan, L.P. Fertility stability of P(T)GMS lines in rice and its identification techniques. Chin. J. Rice Sci. 1998, 12, 200–206.
22. Thakur, P.; Kumar, S.; Malik, J.A.; Berger, J.D.; Nayyar, H. Cold stress effects on reproductive development in grain crops: An overview. Environ. Exp. Bot. 2010, 67, 429–443.
23. Miura, K.; Furumoto, T. Cold signaling and cold response in plants. Int. J. Mol. Sci 2013, 14, 5312–5337.
24. Zhou, L.; Zeng, Y.; Zheng, W.; Tang, B.; Yang, S.; Zhang, H.; Li, J.; Li, Z. Fine mapping a QTL qCTB7 for cold tolerance at the booting stage on rice chromosome 7 using a near-isogenic line. Theor. Appl. Genet. 2010, 121, 895–905.
25. Shirasawa, S.; Endo, T.; Nakagomi, K.; Yamaguchi, M.; Nishio, T. Delimitation of a QTL region controlling cold tolerance at booting stage of a cultivar, “lijiangxintuanheigu”, in rice, Oryza sativa L. Theor. Appl. Genet. 2012, 124, 937–946.
26. Deng, Q.Y. Breeding of the ptgms line Y58S with wide adaptability in rice. Hybrid Rice 2005, 20, 15–18.
27. Vinocur, B.; Altman, A. Recent advances in engineering plant tolerance to abiotic stress: Achievements and limitations. Curr. Opin. Biotechnol. 2005, 16, 123–132.
28. Sanghera, G.S.; Wani, S.H.; Hussain, W.; Singh, N.B. Engineering cold stress tolerance in crop plants. Curr. Genomics 2011, 12, 30–43.
29. Cushman, J.C.; Bohnert, H.J. Genomic approaches to plant stress tolerance. Curr. Opin. Biotechnol. 2000, 3, 117–124.
30. Fowler, S. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 2002, 14, 1675–1690.
31. Chinnusamy, V.; Ohta, M.; Kanrar, S.; Lee, B.H.; Hong, X.; Agarwal, M.; Zhu, J.K. ICE1: A regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev. 2003, 17, 1043–1054.
32. Niu, N.; Liang, W.; Yang, X.; Jin, W.; Wilson, Z.A.; Hu, J.; Zhang, D. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat. Commun. 2013, 4, 1445.
33. Badawi, M.; Reddy, Y.V.; Agharbaoui, Z.; Tominaga, Y.; Danyluk, J.; Sarhan, F.; Houde, M. Structure and functional analysis of wheat ice (inducer of CBF expression) genes. Plant Cell Physiol. 2008, 49, 1237–1249.
34. Ma, Q.; Dai, X.; Xu, Y.; Guo, J.; Liu, Y.; Chen, N.; Xiao, J.; Zhang, D.; Xu, Z.; Zhang, X.; et al. Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol. 2009, 150, 244–256.
35. Su, C.F.; Wang, Y.C.; Hsieh, T.H.; Lu, C.A.; Tseng, T.H.; Yu, S.M. A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol. 2010, 153, 145–158.
36. Hossain, M.A.; Cho, J.I.; Han, M.; Ahn, C.H.; Jeon, J.S.; An, G.; Park, P.B. The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J. Plant Physiol. 2010, 167, 1512–1520.
37. Liu, C.; Wu, Y.; Wang, X. bZIP transcription factor OsbZIP52/RISBZ5: A potential negative regulator of cold and drought stress response in rice. Planta 2012, 235, 1157–1169.
38. Rushton, P.J.; Somssich, I.E.; Ringler, P.; Shen, Q.J. WRKY transcription factors. Trends Plant Sci. 2010, 15, 247–258.
39. Ramamoorthy, R.; Jiang, S.Y.; Kumar, N.; Venkatesh, P.N.; Ramachandran, S. A comprehensive transcriptional profiling of the wrky gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol. 2008, 49, 865–879.
40. Kanneganti, V.; Gupta, A. Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol. Biol. 2008, 66, 445–462.
41. Kong, Z.; Li, M.; Yang, W.; Xu, W.; Xue, Y. A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol. 2006, 141, 1376–1388.
42. Jan, A.; Maruyama, K.; Todaka, D.; Kidokoro, S.; Abo, M.; Yoshimura, E.; Shinozaki, K.; Nakashima, K.; Yamaguchi-Shinozaki, K. OsTZF1, a CCCH-tandem zinc finger protein, confers delayed senescence and stress tolerance in rice by regulating stress-related genes. Plant Physiol. 2013, 161, 1202–1216.
43. Gong, Z.; Dong, C.H.; Lee, H.; Zhu, J.; Xiong, L.; Gong, D.; Stevenson, B.; Zhu, J.K. A dead box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 2005, 17, 256–267.
44. Townley, H.E.; Knight, M.R. Calmodulin as a potential negative regulator of ArabidopsisCOR gene expression. Plant Physiol. 2002, 128, 1169–1172.
45. Komatsu, S.; Yang, G.; Khan, M.; Onodera, H.; Toki, S.; Yamaguchi, M. Over-expression of calcium-dependent protein kinase 13 and calreticulin interacting protein 1 confers cold tolerance on rice plants. Mol. Genet. Genomics 2007, 277, 713–723.
46. Kobayashi, Y.; Yamamoto, S.; Minami, H.; Kagaya, Y.; Hattori, T. Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 2004, 16, 1163–1177.
47. Shibasaki, K.; Uemura, M.; Tsurumi, S.; Rahman, A. Auxin response in Arabidopsis under cold stress: Underlying molecular mechanisms. Plant Cell 2009, 21, 3823–3838.
48. Miura, K.; Lee, J.; Gong, Q.; Ma, S.; Jin, J.B.; Yoo, C.Y.; Miura, T.; Sato, A.; Bohnert, H.J.; Hasegawa, P.M. SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol. 2011, 155, 1000–1012.
49. Yang, X.; Yang, Y.N.; Xue, L.J.; Zou, M.J.; Liu, J.Y.; Chen, F.; Xue, H.W. Rice ABI5-like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes. Plant Physiol. 2011, 156, 1397–1409.
50. Ivanov, A.G.; Rosso, D.; Savitch, L.V.; Stachula, P.; Rosembert, M.; Oquist, G.; Hurry, V.; Huner, N.P. Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth. Res. 2012, 113, 191–206.
51. Jain, M.; Nijhawan, A.; Arora, R.; Agarwal, P.; Ray, S.; Sharma, P.; Kapoor, S.; Tyagi, A.K.; Khurana, J.P. F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol. 2007, 143, 1467–1483.
52. Hannah, M.A.; Heyer, A.G.; Hincha, D.K. A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet. 2005, 1, e26.
53. Heidarvand, L.; Maali Amiri, R. What happens in plant molecular responses to cold stress? Acta Physiol. Plant 2010, 32, 419–431.
54. Dang, H.; Tran, N.; Gill, S.; Tuteja, R.; Tuteja, N. A single subunit MCM6 from pea promotes salinity stress tolerance without affecting yield. Plant Mol. Biol. 2011, 76, 19–34.
55. Vashisht, A.A.; Pradhan, A.; Tuteja, R.; Tuteja, N. Cold- and salinity stress-induced bipolar pea DNA helicase 47 is involved in protein synthesis and stimulated by phosphorylation with protein kinase C. Plant J. 2005, 44, 76–87.
56. Marwedel, T.; Ishibashi, T.; Lorbiecke, R.; Jacob, S.; Sakaguchi, K.; Sauter, M. Plant-specific regulation of replication protein A2 (OsRPA2) from rice during the cell cycle and in response to ultraviolet light exposure. Planta 2003, 217, 457–465.
57. Byrne, M.E. A role for the ribosome in development. Trends Plant Sci. 2009, 14, 512–519.
58. Bae, M.S.; Cho, E.J.; Choi, E.; Park, O.K. Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J. 2003, 36, 652–663.
59. Wang, J.; Lan, P.; Gao, H.; Zheng, L.; Li, W.; Schmidt, W. Expression changes of ribosomal proteins in phosphate- and iron-deficient arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics 2013, 14, 1–14.
60. S1 processes UbL40 mRNAs and controls thermosensitive genic male sterility in rice. Nat. Commun. 2014, 5, 4884.
61. Zhang, D.; Wilson, Z.A. Stamen specification and anther development in rice. Chin. Sci. Bull. 2009, 54, 2342–2353.
62. Kuroki, M.; Saito, K.; Matsuba, S.; Yokogami, N.; Shimizu, H.; Ando, I.; Sato, Y. A quantitative trait locus for cold tolerance at the booting stage on rice chromosome 8. Theor. Appl. Genet. 2007, 115, 593–600.
63. Trapnell, C.; Roberts, A.; Goff, L.; Pertea, G.; Kim, D.; Kelley, D.R.; Pimentel, H.; Salzberg, S.L.; Rinn, J.L.; Pachter, L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 2012, 7, 562–578.
64. Mortazavi, A.; Williams, B.A.; McCue, K.; Schaeffer, L.; Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat. Methods 2008, 5, 621–628.
65. Anders, S.; Huber, W. Differential expression analysis for sequence count data. Genome Biol. 2010, 11, R106.
66. Young, M.D.; Wakefield, M.J.; Smyth, G.K.; Oshlack, A. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biol. 2010, 11, R14.
67. Mao, X.; Cai, T.; Olyarchuk, J.G.; Wei, L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005, 21, 3787–3793.