Identification of wild soybean miRNAs and their target genes responsive to aluminum stress

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Zeng, Qiao Ying ^a   Yang, Cun Yi ^a   Ma, Qi Bin ^a   Li, Xiu Ping ^a   Dong, Wen Wen ^a   Nian, Hai ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Aluminum stress; High throughput sequencing; miRNA; Wild soybean

Indexed keywords

GLYCINE MAX; GLYCINE SOJA;

ALUMINUM; MESSENGER RNA; MICRORNA;

ARTICLE; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; RNA STABILITY; SOYBEAN;

ALUMINUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICRORNAS; MOLECULAR SEQUENCE ANNOTATION; RNA STABILITY; RNA, MESSENGER; SOYBEANS; STRESS, PHYSIOLOGICAL;

EID: 84870823419     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-182     Document Type: Article

References (92)

1. Hymowitz T. On the domestication of the soybean. Economic Botany 1970, 24:408-421.
2. Ge Y, Zhu Y, Lv D, Dong T, Wang W, Tan S, Liu C, Zou P. Research on responses of wild soybean to alkaline stress. Pratacultural Science 2009, 26:47-52.
3. Ge Y, Li Y, Zhu Y, Bai X, Lv D, Guo D, Ji W, Cai H. Global transcriptome profiling of wild soybean roots under NaHCO3 treatment. BMC Plant Biol 2010, 10:153.
4. Aladdin H, Xu D. Conserved salt tolerance quantitative trait locus (QTL) in wild and cultivated soybeans. Breeding Science 2008, 58:355-359.
5. Tuyen D, Lal S, Xu D. Identification of a major QTL allele from wild soybean (Glycihe soja Sieb. & Zucc.) for increasing alkaline salt tolerance in soybean. Theor Appl Genet 2010, 121:229-236.
6. Hyten D, Song Q, Zhu Y, Choi I, Nelson R, Costa J, Specht J, Shoemaker R, Cregan P. Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci USA 2006, 103:16666-16671.
7. Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL, Li MW, He W, Qin N, Wang B, et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 2010, 42(12):1053-1059.
8. Kim MY, Lee S, Van K, Kim TH, Jeong SC, Choi IY, Kim DS, Lee YS, Park D, Ma J, et al. Whole-genome sequencing and intensive analysis of the undomesticated soybean (Glycine soja Sieb. and Zucc.) genome. Proc Natl Acad Sci USA 2010, 107(51):22032-22037.
9. Kochian LV, Hoekenga OA, Pineros MA. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 2004, 55:459-493.
10. Ma JF. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. International Review of Cytolog 2007, 264:225-252.
11. Kochian L, Piñeros M, Hoekenga O. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 2005, 274(1):175.
12. Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H. Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA 2004, 101(42):15249-15254.
13. Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 2009, 21(2):655-667.
14. Liu J, Magalhaes JV, Shaff J, Kochian LV. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 2009, 57(3):389-399.
15. Huang CF, Yamaji N, Chen Z, Ma JF. A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J 2012, 69(5):857-867.
16. Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn S, Ryan P, Delhaize E. E MH: A wheat gene encoding an aluminum-activated malate transporter. Plant J 2004, 37:645-653.
17. Iuchi S, Koyama H, Iuchi A, Kobayashi Y, Kitabayashi S, Kobayashi Y, Ikka T, Hirayama T, Shinozaki K, Kobayashi M. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA 2007, 104(23):9900-9905.
18. Yamaji N, Huang CF, Nagao S, Yano M, Sato Y, Nagamura Y, Ma JF. A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell 2009, 21(10):3339-3349.
19. Bianchi-Hall CM, Thomas E, Carter J, Bailey M, Al E. Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Science 2000, 40:538-545.
20. Nian H, Yang Z, Huang H, Yan X, Matsumoto H. Citrate secretion induced by aluminum stress may not be a key mechanism responsible for differential aluminum tolerance of some soybean genotypes. Journal of Plant Nutrition 2004, 27:2047-2066.
21. Ermolayev V, Weschke W, Manteuffel R. Comparison of Al-induced gene expression in sensitive and tolerant soybean cultivars. J Exp Bot 2003, 54:2745-2756.
22. Ragland M, Soliman K. Two genes induced by Al in soybean roots. Plant Physiol 1997, 114:395.
23. Duressa D, Soliman K, Chen D. Identification of aluminum responsive genes in Al-tolerant soybean line PI 416937. International Journal of Plant Genomics 2010, 2010:1-13.
24. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. Widespread translational inhibition by plant miRNAs and siRNAs. Science 2008, 320:1185-1190.
25. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
26. Jones-Rhoades MW, Bartel DP, Bartel B. MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 2006, 57:19-53.
27. Mallory AC, Vaucheret H. Functions of microRNAs and related small RNAs in plants. Nat Genet 2006, 38:S31-S36.
28. Ruiz-Ferrer V, Voinnet O. Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 2009, 60:485-510.
29. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, et al. High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2007, 2(2):e219.
30. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu J. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 2008, 8:25.
31. Zhao CZ, Xia H, Frazier TP, Yao YY, Bi YP, Li AQ, Li MJ, Li CS, Zhang BH, Wang XJ. Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 2010, 10:3.
32. Chi X, Yang Q, Chen X, Wang J, Pan L, Chen M, Yang Z, He Y, Liang X, Yu S. Identification and characterization of microRNAs from peanut (Arachis hypogaea L.) by high-throughput sequencing. PLoS One 2011, 6(11):e27530.
33. Li Y, Zhang Q, Zhang J, Wu L, Qi Y, Zhou JM. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 2010, 152(4):2222-2231.
34. Chen L, Zhang Y, Ren Y, Xu J, Zhang Z, Wang Y. Genome-wide identification of cold-responsive and new microRNAs in Populus tomentosa by high-throughput sequencing. Biochemical and Biophysical Research Communication 2011, 417:897-896.
35. Wang T, Chen L, Zhao M, Tian Q, Zhang W. Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 2011, 12:367.
36. Zhou ZS, Zeng HQ, Liu ZP, Yang ZM. Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 2012, 35(1):86-99.
37. Li H, Dong Y, Yin H, Wang N, Yang J, Liu X, Wang Y, Wu J, Li X. Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 2011, 11:170.
38. Song QX, Liu YF, Hu XY, Zhang WK, Ma B, Chen SY, Zhang JS. Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol 2011, 11:5.
39. Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu JK, Yu O. Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 2008, 9:160.
40. Wang Y, Li P, Cao X, Wang X, Zhang A, Li X. Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochemical and Biophysical Research Communication 2009, 378(4):799-803.
41. Wong CE, Zhao YT, Wang XJ, Croft L, Wang ZH, Haerizadeh F, Mattick JS, Singh MB, Carroll BJ, Bhalla PL. MicroRNAs in the shoot apical meristem of soybean. Journal of Experimental Botony 2011, 62(8):2495-2506.
42. Yong-xin L, Wei C, Ying-peng H, Quan Z, Mao-zu G, Wen-bin L. In silico detection of novel MicroRNAs genes in soybean genome. Agricultural Sciences in China 2011, 10:1336-1345.
43. Zhang B, Pan X, Stellwag EJ. Identification of soybean microRNAs and their targets. Planta 2008, 229(1):161-182.
44. Jing W, Chun-yan L, Li-wei Z, Jia-lin W, Guo-hua H, Jun-jie D, Qing-shan C. MicroRNAs Involved in the Pathogenesis of Phytophthora Root Rot of Soybean (Glycine max). Agricultural Sciences in China 2011, 10:1159-1167.
45. Kulcheski FR, de Oliveira LF, Molina LG, Almerao MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimaraes FC, et al. Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 2011, 12:307.
46. Chen R, Hu Z, Zhang H. Identification of microRNAs in wild soybean (Glycine soja). J Integr Plant Biol 2009, 51(12):1071-1079.
47. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 2008, 18(10):758-762.
48. German MA, Pillay M, Jeong DH, Hetawal A, Luo SJ, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, Paoli ED, Lu C, Schroth G, Meyers BC, Green PJ. Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 2008, 26:941-946.
49. Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R. Transcriptome-wide identification of microRNA targets in rice. Plant J 2010, 62(5):742-759.
50. Chen L, Wang T, Zhao M, Tian Q, Zhang WH. Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 2012, 235(2):375-386.
51. Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J. Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 2010, 62(6):960-976.
52. Martinez G, Forment J, Llave C, Pallas V, Gomez G. High-throughput sequencing, characterization and detection of new and conserved cucumber miRNAs. PLoS One 2011, 6(5):e19523.
53. Song C, Wang C, Zhang C, Korir NK, Yu H, Ma Z, Fang J. Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics 2010, 11:431.
54. The Rfam database ftp://ftp.sanger.ac.uk/pub/databases/Rfam/9.1/.
55. The Repbase database http://www.girinst.org/repbase/update/index.html.
56. The Glysince max database ftp://ftp.jgi-psf.org/pub/JGI_data/phytozome/v7.0/Gmax/annotation/Gmax_109_transcript.fa.gz.
57. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, et al. Criteria for Annotation of Plant MicroRNAs. Plant Cell 2008, 20:3186-3190.
58. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 2006, 20(24):3407-3425.
59. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, et al. A uniform system for microRNA annotation. RNA 2003, 9(3):277-279.
60. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003, 31(13):3406-3415.
61. Addo-Quaye C, Snyder JA, Park YB, Li YF, Sunkar R, Axtell MJ. Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 2009, 15(12):2112-2121.
62. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38(Web Server issue):W64-W70.
63. Zhou ZS, Huang SQ, Yang ZM. Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochemical and Biophysical Research Communication 2008, 374(3):538-542.
64. Sabehat A, Weiss D, Lurie S. Heat-shock proteins and cross-tolerance in plants. Physiol Plant 1998, 103:437-441.
65. Ding Y, Chen Z, Zhu C. Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 2011, 62(10):3563-3573.
66. Guo HS, Xie Q, Fei JF, Chua NH. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to down-regulate auxin signals for Arabidopsis lateral root development. Plant Cell 2005, 17(5):1376-1386.
67. Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y. Identification of drought-induced microRNAs in rice. Biochemical and Biophysical Research Communication 2007, 354(2):585-590.
68. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 2008, 14(5):836-843.
69. Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y. Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 2009, 10:29.
70. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L. Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 2010, 61:4157-4168.
71. Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post-transcriptionally to promote drought resistance. Plant Cell 2008, 20(8):2238-2251.
72. Zhang W, Gao S, Zhou X, Chellappan P, Chen Z, Zhou X, Zhang X, Fromuth N, Coutino G, Coffey M, et al. Bacteria-responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol Biol 2011, 75(1-2):93-105.
73. Radwan O, Liu Y, Clough SJ. Transcriptional analysis of soybean root response to Fusarium virguliforme, the causal agent of sudden death syndrome. Molecula Plant-Microbe Interactions 2011, 24(8):958-972.
74. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. Prediction of plant microRNA targets. Cell 2002, 110(4):513-520.
75. Jones-Rhoades MW, Bartel DP. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 2004, 14(6):787-799.
76. Sunkar R, Girke T, Jain PK, Zhu JK. Cloning and characterization of microRNAs from rice. Plant Cell 2005, 17(5):1397-1411.
77. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 2008, 53(5):739-749.
78. Kurihara Y, Kaminuma E, Matsui A, Kawashima M, Tanaka M, Morosawa T, Ishida J, Mochizuki Y, Shinozaki K, Toyoda T, et al. Transcriptome Analyses Revealed Diverse Expression Changes in ago1 and hyl1 Arabidopsis Mutants. Plant and Cell Phydiology 2009, 50:1715-1720.
79. Erik A, Van Der B, Jonathan DGJ. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 1998, 8:226-667.
80. Swiderski MR, Doris B, Jonathan DGJ. The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Molecular Plant-Microbe Interations 2009, 22:157-165.
81. Tang P, Zhang Y, Sun X, Tian C, Yang S, Ding J. Disease resistance signature of the leucine-rich repeat receptor-like kinase genes in four plant species. Plant Sci 2010, 179:399-406.
82. Kollmeier M, Felle HH, Horst WJ. Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum?. Plant Physiol 2000, 122(3):945-956.
83. Sun P, Tian QY, Chen J, Zhang WH. Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. Journal of Experimental Botony 2010, 61(2):347-356.
84. Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY. Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 2005, 17(8):2204-2216.
85. Xie Q, Frugis G, Colgan D, Chua NH. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 2000, 14(23):3024-3036.
86. Duval M, Hsieh TF, Kim SY, Thomas TL. Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol 2002, 50(2):237-248.
87. Hou N, You J, Pang J, Xu M, Chen G, Yang Z. The accumulation and transport of abscisic acid in soybean (Glycine max L.) under aluminum stress. Plant Soil 2010, 330:127-137.
88. Reyes JL, Chua N. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 2007, 49:592-606.
89. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002, 7:405-410.
90. Beffagna N, Buffoli B, Busi C. Modulation of reactive oxygen species production during osmotic stress in Arabidopsis thaliana cultured cells: involvement of the plasma membrane Ca2+-ATPase and H+-ATPase. Plant Cell Physiol 2005, 46(8):1326-1339.
91. Shabala S, Baekgaard L, Shabala L, Fuglsang AT, Cuin TA, Nemchinov LG, Palmgren MG. Endomembrane Ca2+-ATPases play a significant role in virus-induced adaptation to oxidative stress. Plant Signal Behav 2011, 6(7):1053-1056.
92. ESTs and GSSs of Glycine soja registered in ncbi http://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?id=3848.