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

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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.

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References

  • 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 126:1563–1570

    CAS  PubMed  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    Article  CAS  PubMed  Google Scholar 

  • Barceló AR (1997) Lignification in plant cell walls. Int Rev Cytol 176:87–132

    Article  Google Scholar 

  • 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 322:1835–1839

    Article  CAS  PubMed  Google Scholar 

  • 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 23:915–926

    Article  CAS  PubMed  Google Scholar 

  • 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 45:193–203

    Article  CAS  Google Scholar 

  • 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 465:316–321

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Çetin E (2009) Effects of boron stress on the anatomical structure of Medicago sativa L. IUFS J Biol 68:27–35

    Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Sci Signal 303:2022–2025

    CAS  Google Scholar 

  • 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:e179

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 52:946–951

    Article  CAS  PubMed  Google Scholar 

  • 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 504:160–165

    Article  CAS  PubMed  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    Article  CAS  PubMed  Google Scholar 

  • 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 15:656–711

    Google Scholar 

  • 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 31:69–81

    Article  CAS  Google Scholar 

  • 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 39:1033–1037

    Article  CAS  PubMed  Google Scholar 

  • 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 15:2038–2043

    Article  CAS  PubMed  Google Scholar 

  • 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 155:423–430

    Article  CAS  PubMed  Google Scholar 

  • 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 49:683–693

    Article  CAS  PubMed  Google Scholar 

  • 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 52:591–594

    Article  Google Scholar 

  • Gifford ML, Dean A, Gutierrez RA, Coruzzi GM, Birnbaum KD (2008) Cell-specific nitrogen responses mediate developmental plasticity. P Natl Acad Sci 105:803–808

    Article  CAS  Google Scholar 

  • Gupta UC, Jame Y, Campbell C, Leyshon A, Nicholaichuk W (1985) Boron toxicity and deficiency: a review. Can J Soil Sci 65:381–409

    Article  CAS  Google Scholar 

  • 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 23:54–68

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

  • 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 156:1101–1115

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129

    Article  CAS  PubMed  Google Scholar 

  • 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 225:1327–1338

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 57:313–321

    Article  CAS  PubMed  Google Scholar 

  • 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 66:863–876

    Article  CAS  PubMed  Google Scholar 

  • 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 51:1079–1083

    Article  CAS  PubMed  Google Scholar 

  • 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 169:469–478

    Article  CAS  PubMed  Google Scholar 

  • 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 110:1017–1020

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 131:4311–4322

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 151:406–422

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Z, Zhu Q, Tong L (1980) Boron-deficient soils and their distribution in China. Acta Pedol Sin 17:228–239

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 16:2217–2232

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 20:3186–3190

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nable RO, Bañuelos GS, Paull JG (1997) Boron toxicity. Plant Soil 193:181–198

    Article  CAS  Google Scholar 

  • 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 24:1420–1428

    Article  CAS  PubMed  Google Scholar 

  • 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 271:22923–22930

    Article  PubMed  Google Scholar 

  • O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsisgrowth. Science 294:846–849

    Article  PubMed  Google Scholar 

  • Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53:674–690

    Article  CAS  PubMed  Google Scholar 

  • Palatnik JF, Allen E, Wu X, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  CAS  PubMed  Google Scholar 

  • 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 62:960–976

    CAS  PubMed  Google Scholar 

  • 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 62:4943–4954

    Article  CAS  PubMed  Google Scholar 

  • Rajewsky N, Socci ND (2004) Computational identification of microRNA targets. Genome Biol 5:P5. doi:http://genomebiology.com/2004/5/2/P5

  • Ride J (1975) Lignification in wounded wheat leaves in response to fungi and its possible role in resistance. Physiol Plant 5:125–134

    CAS  Google Scholar 

  • Rogers LA, Campbell MM (2004) The genetic control of lignin deposition during plant growth and development. New Phytol 164:17–30

    Article  CAS  Google Scholar 

  • Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16:258–264

    Article  CAS  PubMed  Google Scholar 

  • 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 121:278–283

    Article  CAS  Google Scholar 

  • 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 275:37945–37950

    Article  CAS  PubMed  Google Scholar 

  • Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148

    Article  CAS  Google Scholar 

  • Silva DHd, Rossi ML, Boaretto AE, Nogueira NdL, Muraoka T (2008) Boron affects the growth and ultrastructure of castor bean plants. Sci Agr 65:659–664

    Google Scholar 

  • 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 192:155–164

    Article  CAS  Google Scholar 

  • 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 12:927–934

    Article  CAS  PubMed  Google Scholar 

  • 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 85:159–170

    Article  CAS  PubMed  Google Scholar 

  • Spanjers A, Pierson E (1982) Lignified cells in Lilium longiflorum Thunb. styles and their relation to bioelectric potential changes. Planta 156:193–198

    Article  CAS  PubMed  Google Scholar 

  • 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 18:2051–2065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takada S, K-i Hibara, Ishida T, Tasaka M (2001) The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128:1127–1135

    CAS  PubMed  Google Scholar 

  • 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 107:4477–4482

    Article  CAS  Google Scholar 

  • 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 79:139–149

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang J-W, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Warington K (1923) The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot Lond 37:629–672

    Google Scholar 

  • 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 63:5903–5918

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weir I, Lu J, Cook H, Causier B, Schwarz-Sommer Z, Davies B (2004) CUPULIFORMIS establishes lateral organ boundaries in Antirrhinum. Development 131:915–922

    Article  CAS  PubMed  Google Scholar 

  • Whetten R, Sederoff R (1995) Lignin biosynthesis. Plant Cell 7:1001

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 138:750–759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 233:495–505

    Article  CAS  PubMed  Google Scholar 

  • 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 30:671–690

    Article  CAS  Google Scholar 

  • 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 142:280–293

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 11:246

    Article  Google Scholar 

  • 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 45:59–66

    Article  PubMed  Google Scholar 

  • 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 64:4271–4287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 282:16369–16378

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 64:1521–1536

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 63:1025–1038

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zeng H, Wang G, Hu X, Wang H, Du L, Zhu Y (2014) Role of microRNAs in plant responses to nutrient stress. Plant Soil 374:1005–1021

    Article  CAS  Google Scholar 

  • 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 20:569–581

    Article  CAS  PubMed  Google Scholar 

  • 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 32:328–341

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhcng L, Qiqing Z, Lihua T (1989) Regularities of content and distribuition of boron in soils. Acta Pedol Sin 4:006

    Google Scholar 

  • 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 48:391–404

    Article  CAS  PubMed  Google Scholar 

  • 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 9:149

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 145:242–256

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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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).

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  1. College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China

    Chengquan Yang, Tao Liu, Fuxi Bai, Nannan Wang, Zhiyong Pan, Xiang Yan & ShuAng Peng

  2. Key Laboratory of Horticultural Plant Biology, Ministry of Education, Wuhan, 430070, China

    Chengquan Yang, Tao Liu, Fuxi Bai, Nannan Wang, Zhiyong Pan, Xiang Yan & ShuAng Peng

  3. Key Laboratory of Horticultural Crop Biology and Genetic Improvement (Central Region), MOA, Wuhan, 430070, China

    Chengquan Yang, Tao Liu, Fuxi Bai, Nannan Wang, Zhiyong Pan, Xiang Yan & ShuAng Peng

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Yang, C., Liu, T., Bai, F. et al. miRNAome analysis associated with anatomic and transcriptomic investigations reveal the polar exhibition of corky split vein in boron deficient Citrus sinensis . Mol Genet Genomics 290, 1639–1657 (2015). https://doi.org/10.1007/s00438-015-1024-8

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