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Identification of Glycine Max MicroRNAs in response to phosphorus deficiency

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Abstract

MicroRNAs (miRNAs) are endogenous small RNAs regulating plant development and stress responses. In addition, phosphorus (P) is an important macronutrient for plant growth and development. More than two hundred miRNAs have been identified in Glycine Max and a few of miRNAs have been shown to respond to P deficiency, however, whether there are other miRNAs involved in P deficiency response is largely unknown. In this study, we used high-throughput small RNA sequencing and whole-genome-wide mining to identify the potential miRNAs in response to P deficiency. After sequencing, we deduced 183 known, 99 conserved and 126 novel miRNAs in Glycine Max. Among them, in response to P deficiency, the expressions of 27 known, 16 conserved and 12 novel miRNAs showed significant changes in roots, whereas the expressions of 34 known, 14 conserved and 7 novel miRNAs were significantly different in shoots. Furthermore, we validated the predicated novel miRNAs and found that three miRNAs in roots and five miRNAs in shoots responded to P deficiency. Some miRNAs were P-induced whereas some were P-suppressed. Together these results indicated that the miRNAs identified might play important roles in regulating P signaling pathway.

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References

  • Abel S, Ticconi CA, Delatorre CA (2002) Phosphate sensing in higher plants. Physiol Plantarum 115:1–8

    Article  CAS  Google Scholar 

  • Arenas-Huertero C, Perez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401

    Article  PubMed  CAS  Google Scholar 

  • Boualem A, Laporte P, Jovanovic M, Laffont C, Plet J, Combier JP, Niebel A, Crespi M, Frugier F (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J 54:876–887

    Article  PubMed  CAS  Google Scholar 

  • Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179

    Article  PubMed  Google Scholar 

  • Chen YF, Wang Y, Wu WH (2008) Membrane transporters for nitrogen, phosphate and potassium uptake in plants. J Integr Plant Biol 50:835–848

    Article  PubMed  CAS  Google Scholar 

  • Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38

    Article  PubMed  CAS  Google Scholar 

  • Dong DF, Yan XL, Peng XX (2004) Organic acid exudation induced by phosphorus deficiency and/or aluminium toxicity in two contrasting soybean genotypes. Physiol Plantarum 122:190–199

    Article  CAS  Google Scholar 

  • Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    Article  PubMed  CAS  Google Scholar 

  • Ge Y, Li Y, Zhu YM, Bai X, Lv DK, Guo D, Ji W, Cai H (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol 10:153

    Article  PubMed  Google Scholar 

  • Griffiths-Jones S (2004) The microRNA Registry. Nucleic Acids Res 32(Database issue):D109–111

    Article  PubMed  CAS  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34(Database issue):D140–144

    Article  PubMed  CAS  Google Scholar 

  • Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36(Database issue):D154–158

    PubMed  CAS  Google Scholar 

  • Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138:226–237

    Article  PubMed  CAS  Google Scholar 

  • Guo WB, Zhang LN, Zhao J, Liao H, Zhuang CX, Yan XL (2008) Identification of temporally and spatially phosphate-starvation responsive genes in Glycine max. Plant Sci 175:574–584

    Article  CAS  Google Scholar 

  • Ha M, Pang MX, Agarwal V, Chen ZJ (2008) Interspecies regulation of microRNAs and their targets. Bba-Gene Regul Mech 1779: 735–742

    CAS  Google Scholar 

  • Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P (1994) Fast folding and comparison of RNA secondary structures. Monatsh Chem 125:167–188

    Article  CAS  Google Scholar 

  • Hsieh LC, Lin SI, Shih ACC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-Mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology 151:2120–2132

    Article  PubMed  Google Scholar 

  • Jin H (2008) Endogenous small RNAs and antibacterial immunity in plants. FEBS Lett 582:2679–2684

    Article  PubMed  CAS  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799

    Article  PubMed  CAS  Google Scholar 

  • Joshi T, Yan Z, Libault M, Jeong DH, Park S, Green PJ, Sherrier DJ, Farmer A, May G, Meyers BC, Xu D, Stacey G (2010) Prediction of novel miRNAs and associated target genes in Glycine max. BMC Bioinformatics 11 Suppl 1:S14

    Article  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 39(Database issue):D152–157

    Article  PubMed  Google Scholar 

  • Kulcheski FR, de Oliveira LF, Molina LG, Almerao MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimaraes FC, Abdelnoor RV, Nascimento LC, Carazzolle MF, Pereira GA, Margis R (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307

    Article  PubMed  CAS  Google Scholar 

  • Kulcheski FR, Marcelino-Guimaraes FC, Nepomuceno AL, Abdelnoor RV, Margis R (2010) The use of microRNAs as reference genes for quantitative polymerase chain reaction in soybean. Anal Biochem 406:185–192

    Article  PubMed  CAS  Google Scholar 

  • Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714

    Article  PubMed  CAS  Google Scholar 

  • Li T, Li H, Zhang YX, Liu JY (2011) Identification and analysis of seven HO-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Li C, Ding G, Jin Y (2011) Evolution of MIR159/319 microRNA genes and their post-transcriptional regulatory link to siRNA pathways. BMC Evol Biol 11:122

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55(1):131–151

    Article  PubMed  CAS  Google Scholar 

  • Lundmark M, Korner CJ, Nielsen TH (2010) Global analysis of microRNA in Arabidopsis in response to phosphate starvation as studied by locked nucleic acid-based microarrays. Physiol Plant 140:57–68

    Article  PubMed  CAS  Google Scholar 

  • Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zhu YM (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459:39–47

    Article  PubMed  CAS  Google Scholar 

  • Maizel A, Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22:1104–1117

    Article  PubMed  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant Journal 53:731–738

    Article  PubMed  CAS  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed MicroRNAs by comprehensive realtime polymerase chain reaction profiling and small RNA sequencing. Plant Physiology 150:1541–1555

    Article  PubMed  Google Scholar 

  • Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597

    Article  PubMed  CAS  Google Scholar 

  • Rice P, Longden I, Bleasby A (2000) EMBOSS: the european molecular biology open software suite. Trends Genet 16:276–277

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  PubMed  CAS  Google Scholar 

  • Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69

    Article  PubMed  CAS  Google Scholar 

  • Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183

    Article  PubMed  CAS  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    Article  PubMed  CAS  Google Scholar 

  • Shen J, Xie K, Xiong L (2010) Global expression profiling of rice microRNAs by one-tube stem-loop reverse transcription quantitative PCR revealed important roles of microRNAs in abiotic stress responses. Mol Genet Genomics 284:477–488

    Article  PubMed  CAS  Google Scholar 

  • Shukla LI, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta 1779:743–748

    PubMed  CAS  Google Scholar 

  • Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu JK, Yu O (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9:160

    Article  PubMed  Google Scholar 

  • Sunkar R, Chinnusamy V, Zhu JH, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12:301–309

    Article  PubMed  CAS  Google Scholar 

  • Sunkar R, Jagadeeswaran G (2008) In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol 8:37

    Article  PubMed  Google Scholar 

  • Valdes-Lopez O, Arenas-Huertero C, Ramirez M, Girard L, Sanchez F, Vance CP, Reyes JL, Hernandez G (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell Environ 31:1834–1843

    Article  PubMed  CAS  Google Scholar 

  • Valdes-Lopez O, Hernandez G (2008) Transcriptional regulation and signaling in phosphorus starvation: what about legumes? J Integr Plant Biol 50:1213–1222

    Article  PubMed  CAS  Google Scholar 

  • Valdes-Lopez O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernandez G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187:805–818

    Article  PubMed  CAS  Google Scholar 

  • Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397

    CAS  Google Scholar 

  • Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447

    Article  CAS  Google Scholar 

  • Vaucheret H (2009) AGO1 homeostasis involves differential production of 21-nt and 22-nt miR168 species by MIR168a and MIR168b. PLoS One 4:e6442

    Article  PubMed  Google Scholar 

  • Voinnet O, Brodersen P (2006) The diversity of RNA silencing pathways in plants. Trends in Genetics 22:268–280

    Article  PubMed  Google Scholar 

  • Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Li P, Cao X, Wang X, Zhang A, Li X (2009) Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem Biophys Res Commun 378:799–803

    Article  PubMed  CAS  Google Scholar 

  • Yan X, Wu P, Ling H, Xu G, Xu F, Zhang Q (2006) Plant nutriomics in China: an overview. Ann Bot 98:473–482

    Article  PubMed  CAS  Google Scholar 

  • Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, Lee WS (2010) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res 38:1382–1391

    Article  PubMed  CAS  Google Scholar 

  • Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50:849–859

    Article  PubMed  CAS  Google Scholar 

  • Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167:1289–1297

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16

    Article  PubMed  CAS  Google Scholar 

  • Zhang B, Pan X, Stellwag EJ (2008) Identification of soybean microRNAs and their targets. Planta 229:161–182

    Article  PubMed  CAS  Google Scholar 

  • Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29

    Article  PubMed  Google Scholar 

  • Zhao J, Fu JB, Liao H, He Y, Nian H, Hu YM, Qiu LJ, Dong YS, Yan XL (2004) Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm. Chinese Sci Bull 49:1611–1620

    CAS  Google Scholar 

  • Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143:1–9

    Article  PubMed  CAS  Google Scholar 

  • Zhu YY, Zeng HQ, Dong CX, Yin XM, Shen QR, Yang ZM (2010) microRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.). Plant Sci 178: 23–29

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan, 430062, P.R, China

    Aihua Sha, Hongping Ba, Zhihui Shan, Xiaojuan Zhang, Xuejun Wu, Dezheng Qiu & Xinan Zhou

  2. Key Laboratory of Oil Crop Biology of the Ministry of Agriculture, Wuhan, 430062, P.R, China

    Aihua Sha, Hongping Ba, Zhihui Shan, Xiaojuan Zhang, Xuejun Wu & Xinan Zhou

  3. College of Agriculture, Hainan University, Haikou, 570228, P.R, China

    Yinhua Chen

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  1. Aihua Sha
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  2. Yinhua Chen
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  3. Hongping Ba
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  4. Zhihui Shan
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  8. Shuilian Chen
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  9. Xinan Zhou
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Correspondence to Aihua Sha or Xinan Zhou.

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Sha, A., Chen, Y., Ba, H. et al. Identification of Glycine Max MicroRNAs in response to phosphorus deficiency. J. Plant Biol. 55, 268–280 (2012). https://doi.org/10.1007/s12374-011-0255-4

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