Advertisement

Molecular Genetics and Genomics

, Volume 290, Issue 5, pp 1639–1657 | Cite as

miRNAome analysis associated with anatomic and transcriptomic investigations reveal the polar exhibition of corky split vein in boron deficient Citrus sinensis

  • Chengquan Yang
  • Tao Liu
  • Fuxi Bai
  • Nannan Wang
  • Zhiyong Pan
  • Xiang Yan
  • ShuAng PengEmail author
Original Paper

Abstract

Corky split vein can develop under long-term boron deficient conditions in Citrus sinensis L. Osbeck cv. Newhall. This symptom only occurs in the upper rather than the lower epidermis of old leaves. Our previous study demonstrated that vascular hypertrophy was involved in the symptoms, and the 3rd developmental stage of corky split vein (BD3) was the critical stage for phenotype formation. Here, we performed an intensive study on the BD3 vein and its control sample (CK3 vein). A lignin test demonstrated that the lignin content in BD3 vein was approximately 1.7 times more than the CK3 vein. Anatomical investigation of the corky split vein indicated that the upper epidermis was destroyed by overgrowing vascular cells, and the increased lignin may contribute to vascular cell differentiation and wounding-induced lignification. In a subsequent small RNA sequencing of the BD3 and CK3 veins, 99 known miRNAs and 22 novel miRNAs were identified. Comparative profiling of these miRNAs demonstrated that the 57 known miRNAs and all novel miRNAs exhibited significant expression differences between the two small RNAs libraries of the BD3 and CK3 veins. Associated with our corresponding digital gene expression data, we propose that the decreased expression of two miRNAs, csi-miR156b and csi-miR164, which leads to the up-regulation of their target genes, SPLs (csi-miR156b-targeted) and CUC2 (csi-miR164-targeted), may promote vascular cell division and orderless stage transition in old leaves.

Keywords

Corky split vein Anatomy miRNAome Lignification Cell division Orderless stage transition 

Notes

Acknowledgments

This research was financially supported by the National Modern Citrus Industry System, the Ministry of Education Innovation Team (IRT13065), the National NSF of China (No. 31071761 and 31272121).

Supplementary material

438_2015_1024_MOESM1_ESM.xlsx (12 kb)
Supplementary Table S1 Primer sequences of the miRNAs and their targets for qRT-PCR analysis (XLSX 11 kb)
438_2015_1024_MOESM2_ESM.xlsx (5.4 mb)
Supplementary Table S2 Known miRNAs in the C. sinensis vein (XLSX 5490 kb)
438_2015_1024_MOESM3_ESM.xlsx (11 kb)
Supplementary Table S3 Novel miRNAs in the C. sinensis vein (XLSX 10 kb)
438_2015_1024_MOESM4_ESM.xlsx (2.7 mb)
Supplementary Table S4 Differentially expressed known miRNA list (XLSX 2748 kb)
438_2015_1024_MOESM5_ESM.xlsx (10 kb)
Supplementary Table S5 Differentially expressed novel miRNA list (XLSX 10 kb)
438_2015_1024_MOESM6_ESM.xlsx (524 kb)
Supplementary Table S6 Differentially expressed gene list (XLSX 523 kb)
438_2015_1024_MOESM7_ESM.xlsx (14 kb)
Supplementary Table S7 Predicted target genes of differentially expressed known miRNAs (XLSX 13 kb)
438_2015_1024_MOESM8_ESM.xlsx (12 kb)
Supplementary Table S8 Predicted target genes of novel miRNAs (XLSX 12 kb)

References

  1. Aida M, Ishida T, Tasaka M (1999) Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126:1563–1570PubMedGoogle Scholar
  2. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221CrossRefPubMedGoogle Scholar
  3. Barceló AR (1997) Lignification in plant cell walls. Int Rev Cytol 176:87–132CrossRefGoogle Scholar
  4. Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P (2008) A conserved molecular framework for compound leaf development. Science 322:1835–1839CrossRefPubMedGoogle Scholar
  5. Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible W-R, Krajinski F (2010) Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant Microbe Interact 23:915–926CrossRefPubMedGoogle Scholar
  6. Cajuste JF, Lafuente MT (2007) Ethylene-induced tolerance to non-chilling peel pitting as related to phenolic metabolism and lignin content in ‘Navelate’ fruit. Postharvest Biol Technol 45:193–203CrossRefGoogle Scholar
  7. Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321PubMedCentralCrossRefPubMedGoogle Scholar
  8. Çetin E (2009) Effects of boron stress on the anatomical structure of Medicago sativa L. IUFS J Biol 68:27–35Google Scholar
  9. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Sci Signal 303:2022–2025Google Scholar
  10. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179PubMedCentralCrossRefPubMedGoogle Scholar
  11. Chen X, Zhang Z, Liu D, Zhang K, Li A, Mao L (2010) SQUAMOSA promoter-binding protein-like transcription factors: star players for plant growth and development. J Integr Plant Biol 52:946–951CrossRefPubMedGoogle Scholar
  12. Chen L, Ren Y, Zhang Y, Xu J, Sun F, Zhang Z, Wang Y (2012) Genome-wide identification and expression analysis of heat-responsive and novel microRNAs in Populus tomentosa. Gene 504:160–165CrossRefPubMedGoogle Scholar
  13. Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549CrossRefPubMedGoogle Scholar
  14. CunCang J, YunHua W, GuiDong L, Ying X, Shuang P, BaLian Z, QingLuan Z (2009) Effect of boron on the leaf etiolation and fruit drop of Newhall navel orange in southern Jiangxi. Plant Nutr Fertil Sci 15:656–711Google Scholar
  15. Dean R, Kuć J (1987) Rapid lignification in response to wounding and infection as a mechanism for induced systemic protection in cucumber. Physiol Mol Plant P 31:69–81CrossRefGoogle Scholar
  16. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037CrossRefPubMedGoogle Scholar
  17. Fujii H, Chiou T-J, Lin S-I, Aung K, Zhu J-K (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043CrossRefPubMedGoogle Scholar
  18. Fukuda H, Komamine A (1982) Lignin synthesis and its related enzymes as markers of tracheary-element differentiation in single cells isolated from the mesophyll of Zinnia elegans. Planta 155:423–430CrossRefPubMedGoogle Scholar
  19. Gandikota M, Birkenbihl RP, Höhmann S, Cardon GH, Saedler H, Huijser P (2007) The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. Plant J 49:683–693CrossRefPubMedGoogle Scholar
  20. Garg O, Sharma A, Kona GR (1979) Effect of boron on the pollen vitality and yield of rice plants (Oryza sativa L. var. Jaya). Plant Soil 52:591–594CrossRefGoogle Scholar
  21. Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. P Natl Acad Sci 105:803–808CrossRefGoogle Scholar
  22. Gupta UC, Jame Y, Campbell C, Leyshon A, Nicholaichuk W (1985) Boron toxicity and deficiency: a review. Can J Soil Sci 65:381–409CrossRefGoogle Scholar
  23. Hasson A, Plessis A, Blein T, Adroher B, Grigg S, Tsiantis M, Boudaoud A, Damerval C, Laufs P (2011) Evolution and diverse roles of the CUP-SHAPED COTYLEDON genes in Arabidopsis leaf development. Plant Cell 23:54–68PubMedCentralCrossRefPubMedGoogle Scholar
  24. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular 347. http://www.cabdirect.org/abstracts/19500302257.html;jsessionid=21CFE13CEF4FFD33BD6D3D3CB052E64D
  25. Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C (2011) LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol 156:1101–1115PubMedCentralCrossRefPubMedGoogle Scholar
  26. Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129CrossRefPubMedGoogle Scholar
  27. Jung J-H, Park C-M (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225:1327–1338CrossRefPubMedGoogle Scholar
  28. Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7:e1002021. doi: 10.1371/journal.pgen.1002021 PubMedCentralCrossRefPubMedGoogle Scholar
  29. Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA 395 and one of its target genes but in different cell types. Plant J 57:313–321CrossRefPubMedGoogle Scholar
  30. Kawashima CG, Matthewman CA, Huang S, Lee B-R, Yoshimoto N, Koprivova A, Rubio-Somoza I, Todesco M, Rathjen T, Saito K (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876CrossRefPubMedGoogle Scholar
  31. Kim JY, Kwak KJ, Jung HJ, Lee HJ, Kang H (2010) MicroRNA402 affects seed germination of Arabidopsis thaliana under stress conditions via targeting DEMETER-LIKE Protein3 mRNA. Plant Cell Physiol 51:1079–1083CrossRefPubMedGoogle Scholar
  32. Ko JH, Prassinos C, Han KH (2006) Developmental and seasonal expression of PtaHB1, a Populus gene encoding a class III HD-Zip protein, is closely associated with secondary growth and inversely correlated with the level of microRNA (miR166). New Phytol 169:469–478CrossRefPubMedGoogle Scholar
  33. Kobayashi M, Matoh T, Azuma J (1996) Two chains of rhamnogalacturonan II are cross-linked by borate-diol ester bonds in higher plant cell walls. Plant Physiol 110:1017–1020PubMedCentralPubMedGoogle Scholar
  34. Laufs P, Peaucelle A, Morin H, Traas J (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131:4311–4322CrossRefPubMedGoogle Scholar
  35. Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714CrossRefPubMedGoogle Scholar
  36. Li C, Li Y, Bai L, Zhang T, He C, Yan Y, Yu X (2013) Grafting-responsive miRNAs in cucumber and pumpkin seedlings identified by high-throughput sequencing at whole genome level. Physiol Plant 151:406–422CrossRefPubMedGoogle Scholar
  37. Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 7:e48951. doi: 10.1371/journal.pone.0048951 PubMedCentralCrossRefPubMedGoogle Scholar
  38. Liu Z, Zhu Q, Tong L (1980) Boron-deficient soils and their distribution in China. Acta Pedol Sin 17:228–239Google Scholar
  39. Liu Y, Wang L, Chen D, Wu X, Huang D, Chen L, Li L, Deng X, Xu Q (2014) Genome-wide comparison of microRNAs and their targeted transcripts among leaf, flower and fruit of sweet orange. BMC Genom 15:695. doi: 10.1186/1471-2164-15-695 CrossRefGoogle Scholar
  40. Lorrain S, Lin B, Auriac MC, Kroj T, Saindrenan P, Nicole M, Balagué C, Roby D (2004) Vascular associated death1, a novel GRAM domain-containing protein, is a regulator of cell death and defense responses in vascular tissues. Plant Cell 16:2217–2232PubMedCentralCrossRefPubMedGoogle Scholar
  41. Lu YB, Yang LT, Qi YP, Li Y, Li Z, Chen YB, Huang ZR, Chen LS (2014) Identification of boron-deficiency-responsive microRNAs in Citrus sinensis roots by Illumina sequencing. BMC Plant Biol 14:123. doi: 10.1186/1471-2229-14-123 PubMedCentralCrossRefPubMedGoogle Scholar
  42. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190PubMedCentralCrossRefPubMedGoogle Scholar
  43. Nable RO, Bañuelos GS, Paull JG (1997) Boron toxicity. Plant Soil 193:181–198CrossRefGoogle Scholar
  44. Niu Q-W, Lin S-S, Reyes JL, Chen K-C, Wu H-W, Yeh S-D, Chua N-H (2006) Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance. Nat Biotechnol 24:1420–1428CrossRefPubMedGoogle Scholar
  45. O’Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that is covalently cross-linked by a borate ester in vitro conditions for the formation and hydrolysis of the dimer. J Biol Chem 271:22923–22930CrossRefPubMedGoogle Scholar
  46. O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsisgrowth. Science 294:846–849CrossRefPubMedGoogle Scholar
  47. Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690CrossRefPubMedGoogle Scholar
  48. Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263CrossRefPubMedGoogle Scholar
  49. Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62:960–976PubMedGoogle Scholar
  50. Peng T, Lv Q, Zhang J, Li J, Du Y, Zhao Q (2011) Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa). J Exp Bot 62:4943–4954CrossRefPubMedGoogle Scholar
  51. Rajewsky N, Socci ND (2004) Computational identification of microRNA targets. Genome Biol 5:P5. doi:http://genomebiology.com/2004/5/2/P5
  52. Ride J (1975) Lignification in wounded wheat leaves in response to fungi and its possible role in resistance. Physiol Plant 5:125–134Google Scholar
  53. Rogers LA, Campbell MM (2004) The genetic control of lignin deposition during plant growth and development. New Phytol 164:17–30CrossRefGoogle Scholar
  54. Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16:258–264CrossRefPubMedGoogle Scholar
  55. Sheng O, Song S, Peng S, Deng X (2009) The effects of low boron on growth, gas exchange, boron concentration and distribution of ‘Newhall’ navel orange (Citrus sinensis Osb.) plants grafted on two rootstocks. Sci Hortic Amst 121:278–283CrossRefGoogle Scholar
  56. Shi L-X, Lorković ZJ, Oelmüller R, Schröder WP (2000) The low molecular mass PsbW protein is involved in the stabilization of the dimeric photosystem II complex in Arabidopsis thaliana. J Biol Chem 275:37945–37950CrossRefPubMedGoogle Scholar
  57. Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148CrossRefGoogle Scholar
  58. Silva DHd, Rossi ML, Boaretto AE, Nogueira NdL, Muraoka T (2008) Boron affects the growth and ultrastructure of castor bean plants. Sci Agr 65:659–664Google Scholar
  59. Smith CG, Rodgers MW, Zimmerlin A, Ferdinando D, Bolwell GP (1994) Tissue and subcellular immunolocalisation of enzymes of lignin synthesis in differentiating and wounded hypocotyl tissue of French bean (Phaseolus vulgaris L.). Planta 192:155–164CrossRefGoogle Scholar
  60. Song C, Jia Q, Fang J, Li F, Wang C, Zhang Z (2010) Computational identification of citrus microRNAs and target analysis in citrus expressed sequence tags. Plant Biol 12:927–934CrossRefPubMedGoogle Scholar
  61. Souer E, van Houwelingen A, Kloos D, Mol J, Koes R (1996) The No Apical Meristem gene of Petunia is required for pattern formation in embryos and flowers and Is expressed at meristem and primordia boundaries. Cell 85:159–170CrossRefPubMedGoogle Scholar
  62. Spanjers A, Pierson E (1982) Lignified cells in Lilium longiflorum Thunb. styles and their relation to bioelectric potential changes. Planta 156:193–198CrossRefPubMedGoogle Scholar
  63. Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065PubMedCentralCrossRefPubMedGoogle Scholar
  64. Takada S, K-i Hibara, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135PubMedGoogle Scholar
  65. Vidal EA, Araus V, Lu C, Parry G, Green PJ, Coruzzi GM, Gutiérrez RA (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. P Natl Acad Sci 107:4477–4482CrossRefGoogle Scholar
  66. Voxeur A, Fry SC (2014) Glycosylinositol phosphorylceramides (GIPCs) from Rosa cell cultures are boron-bridged in the plasma membrane and form complexes with rhamnogalacturonan-II. Plant J 79:139–149PubMedCentralCrossRefPubMedGoogle Scholar
  67. Wang J-W, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749CrossRefPubMedGoogle Scholar
  68. Wang J-W, Park MY, Wang L-J, Koo Y, Chen X-Y, Weigel D, Poethig RS (2011) miRNA control of vegetative phase change in trees. PLoS Genet 7:e1002012. doi: 10.1371/journal.pgen.1002012 PubMedCentralCrossRefPubMedGoogle Scholar
  69. Warington K (1923) The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot Lond 37:629–672Google Scholar
  70. Waters BM, McInturf SA, Stein RJ (2012) Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. J Exp Bot 63:5903–5918PubMedCentralCrossRefPubMedGoogle Scholar
  71. Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B (2004) CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131:915–922CrossRefPubMedGoogle Scholar
  72. Whetten R, Sederoff R (1995) Lignin biosynthesis. Plant Cell 7:1001PubMedCentralCrossRefPubMedGoogle Scholar
  73. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547PubMedCentralCrossRefPubMedGoogle Scholar
  74. Wu G, Park MY, Conway SR, Wang J-W, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–759PubMedCentralCrossRefPubMedGoogle Scholar
  75. Wu X-M, Liu M-Y, Ge X-X, Xu Q, Guo W-W (2011) Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of Valencia sweet orange. Planta 233:495–505CrossRefPubMedGoogle Scholar
  76. Xiao JX, Yan X, Peng SA, Fang YW (2007) Seasonal changes of mineral nutrients in fruit and leaves of ‘Newhall’ and ‘Skagg’s Bonanza’ navel oranges. J Plant Nut 30:671–690CrossRefGoogle Scholar
  77. Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293PubMedCentralCrossRefPubMedGoogle Scholar
  78. Xu Q, Liu Y, Zhu A, Wu X, Ye J, Yu K, Guo W, Deng X (2010) Discovery and comparative profiling of microRNAs in a sweet orange red-flesh mutant and its wild type. BMC Genom 11:246CrossRefGoogle Scholar
  79. Xu Q, Chen L-L, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao W-B, Hao B-H, Lyon MP (2012) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66CrossRefPubMedGoogle Scholar
  80. Xu L, Wang Y, Zhai L, Xu Y, Wang L, Zhu X, Gong Y, Yu R, Limera C, Liu L (2013) Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J Exp Bot 64:4271–4287PubMedCentralCrossRefPubMedGoogle Scholar
  81. Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M (2007) Regulation of copper homeostasis by micro-RNA in Arabidopsis. J Biol Chem 282:16369–16378CrossRefPubMedGoogle Scholar
  82. Yang C-Q, Liu Y-Z, An J-C, Li S, Jin L-F, Zhou G-F, Wei Q-J, Yan H-Q, Wang N-N, Fu L-N (2013a) Digital gene expression analysis of corky split vein caused by boron deficiency in ‘Newhall’ navel orange (Citrus sinensis Osbeck) for selecting differentially expressed genes related to vascular hypertrophy. PLoS One 8:e65737. doi: 10.1371/journal.pone.0065737 PubMedCentralCrossRefPubMedGoogle Scholar
  83. Yang X, Wang L, Yuan D, Lindsey K, Zhang X (2013b) Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. J Exp Bot 64:1521–1536PubMedCentralCrossRefPubMedGoogle Scholar
  84. Yu X, Wang H, Lu Y, de Ruiter M, Cariaso M, Prins M, van Tunen A, He Y (2012) Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J Exp Bot 63:1025–1038PubMedCentralCrossRefPubMedGoogle Scholar
  85. Zeng H, Wang G, Hu X, Wang H, Du L, Zhu Y (2014) Role of microRNAs in plant responses to nutrient stress. Plant Soil 374:1005–1021CrossRefGoogle Scholar
  86. Zhang X, Li H, Zhang J, Zhang C, Gong P, Ziaf K, Xiao F, Ye Z (2011) Expression of artificial microRNAs in tomato confers efficient and stable virus resistance in a cell-autonomous manner. Transgenic Res 20:569–581CrossRefPubMedGoogle Scholar
  87. Zhang X-N, Li X, Liu J-H (2013) Identification of conserved and novel cold-responsive microRNAs in Trifoliate Orange (Poncirus trifoliata (L.) Raf.) using high-throughput sequencing. Plant Mol Biol Rep 32:328–341CrossRefGoogle Scholar
  88. Zhao M, Tai H, Sun S, Zhang F, Xu Y, Li W-X (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS One 7:e29669. doi: 10.1371/journal.pone.0029669 PubMedCentralCrossRefPubMedGoogle Scholar
  89. Zhcng L, Qiqing Z, Lihua T (1989) Regularities of content and distribuition of boron in soils. Acta Pedol Sin 4:006Google Scholar
  90. Zhou G-K, Kubo M, Zhong R, Demura T, Ye Z-H (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48:391–404CrossRefPubMedGoogle Scholar
  91. Zhu Q-H, Upadhyaya NM, Gubler F, Helliwell CA (2009) Over-expression of miR172 causes loss of spikelet determinacy and floral organ abnormalities in rice (Oryza sativa). BMC Plant Biol 9:149PubMedCentralCrossRefPubMedGoogle Scholar
  92. Zhu H, Hu F, Wang R, Zhou X, Sze S-H, Liou LW, Barefoot A, Dickman M, Zhang X (2011)Arabidopsisargonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145:242–256PubMedCentralCrossRefPubMedGoogle Scholar
  93. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Chengquan Yang
    • 1
    • 2
    • 3
  • Tao Liu
    • 1
    • 2
    • 3
  • Fuxi Bai
    • 1
    • 2
    • 3
  • Nannan Wang
    • 1
    • 2
    • 3
  • Zhiyong Pan
    • 1
    • 2
    • 3
  • Xiang Yan
    • 1
    • 2
    • 3
  • ShuAng Peng
    • 1
    • 2
    • 3
    Email author
  1. 1.College of Horticulture and Forestry SciencesHuazhong Agricultural UniversityWuhanChina
  2. 2.Key Laboratory of Horticultural Plant BiologyMinistry of EducationWuhanChina
  3. 3.Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region)MOAWuhanChina

Personalised recommendations