MicroRNAs associated with molecular mechanisms for plant root formation and growth

Abstract

Although roots are so important for plant growth and crop productivity, the molecular mechanism(s) of root formation and growth is not fully understood. To increase our understanding of the underlying molecular mechanisms, here we review microRNA regulation of processes related to root formation: the regulation of transcription factors, nutrient uptake, stress signaling, and growth signaling. We have summarized the interaction, expression, transport, and signaling events that involve microRNAs in ideal and stressed conditions in a number of model plants, highlighting the involvement of microRNAs in root formation. MicroRNAs are now known to be important players in root initiation, development, and growth; understanding the precise mechanisms involved will be valuable for plant molecular breeding to develop high-yielding crops with high stress resistance and low nutrient requirements.

Keywords

MicroRNAs / Nutrient / Root formation / Stress response / Transcription factor

References

[1] Akdogan G, Tufekci ED, Uranbey S, Unver T (2015) miRNA-based drought regulation in wheat. Funct Integr Genomics. doi:10.1007/s10142-015-0452-1

[2] Alaba S, Piszczalka P, Pietrykowska H, Pacak AM, Sierocka I, Nuc PW, Singh K, Plewka P, Sulkowska A, Jarmolowski A, Karlowski WM, Szweykowska-Kulinska Z. The liverwort Pellia endiviifolia shares microtranscriptomic traits that are common to green algae and land plants. New Phytol, 2015, 206: 352-367.

[3] Ariel F, Brault-Hernandez M, Laffont C, Huault E, Brault M, Plet J, Moison M, Blanchet S, Ichante JL, Chabaud M, Carrere S, Crespi M, Chan RL, Frugier F. Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell, 2012, 24: 3838-3852.

[4] Bao M, Bian H, Zha Y, Li F, Sun Y, Bai B, Chen Z, Wang J, Zhu M, Han N. miR396a-Mediated basic helix-loop-helix transcription factor bHLH74 repression acts as a regulator for root growth in Arabidopsis seedlings. Plant Cell Physiol, 2014, 55: 1343-1353.

[5] Bari R, Datt Pant B, Stitt M, Scheible WR. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol, 2006, 141: 988-999.

[6] Bian H, Xie Y, Guo F, Han N, Ma S, Zeng Z, Wang J, Yang Y, Zhu M. Distinctive expression patterns and roles of the miRNA393/TIR1 homolog module in regulating flag leaf inclination and primary and crown root growth in rice (Oryza sativa). New Phytol, 2012, 196: 149-161.

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

[8] Burklew CE, Ashlock J, Winfrey WB, Zhang B. Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum). PLoS One, 2012, 7 e34783

[9] Chen J, Lin HJ, Pan GT, Zhang ZM, Zhang B, Shen YO, Qin C, Zhang Q, Zhao MJ. Identification of known microRNAs in root and leaf of maize by deep sequencing. Yi Chuan, 2010, 32: 1175-1186.

[10] Chen ZH, Bao ML, Sun YZ, Yang YJ, Xu XH, Wang JH, Han N, Bian HW, Zhu MY. Regulation of auxin response by miR393-targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Mol Biol, 2011, 77: 619-629.

[11] Chen L, Wang T, Zhao M, Zhang W. Ethylene-responsive miRNAs in roots of Medicago truncatula identified by high-throughput sequencing at whole genome level. Plant Sci, 2012, 184: 14-19.

[12] da Costa CT, de Almeida MR, Ruedell CM, Schwambach J, Maraschin FS, Fett-Neto AG. When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci, 2013, 4 133

[13] Deepa K, Sheeja TE, Santhi R, Sasikumar B, Cyriac A, Deepesh PV, Prasath D. A simple and efficient protocol for isolation of high quality functional RNA from different tissues of turmeric (Curcuma longa L.). Physiol Mol Biol Plants, 2014, 20: 263-271.

[14] Degenhardt RF, Bonham-Smith PC. Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development. Plant Physiol, 2008, 147: 128-142.

[15] Devers EA, Branscheid A, May P, Krajinski F. Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol, 2011, 156: 1990-2010.

[16] Devers EA, Teply J, Reinert A, Gaude N, Krajinski F. An endogenous artificial microRNA system for unraveling the function of root endosymbioses related genes in Medicago truncatula. BMC Plant Biol, 2013, 13 82

[17] Eyles RP, Williams PH, Ohms SJ, Weiller GF, Ogilvie HA, Djordjevic MA, Imin N. microRNA profiling of root tissues and root forming explant cultures in Medicago truncatula. Planta, 2013, 238: 91-105.

[18] Frazier TP, Burklew CE, Zhang B. Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum). Funct Integr Genomics, 2014, 14: 75-83.

[19] Gao J, Yin F, Liu M, Luo M, Qin C, Yang A, Yang S, Zhang Z, Shen Y, Lin H, Pan G. Identification and characterisation of tobacco microRNA transcriptome using high-throughput sequencing. Plant Biol (Stuttg), 2015, 17: 591-598.

[20] Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell, 2009, 21: 3119-3132.

[21] Gutierrez L, Mongelard G, Flokova K, Pacurar DI, Novak O, Staswick P, Kowalczyk M, Pacurar M, Demailly H, Geiss G, Bellini C. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell, 2012, 24: 2515-2527.

[22] He Q, Zhu S, Zhang B. MicroRNA-target gene responses to lead-induced stress in cotton (Gossypium hirsutum L.). Funct Integr Genomics, 2014, 14: 507-515.

[23] Hewezi T, Maier TR, Nettleton D, Baum TJ. The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiol, 2012, 159: 321-335.

[24] Hwang DG, Park JH, Lim JY, Kim D, Choi Y, Kim S, Reeves G, Yeom SI, Lee JS, Park M, Kim S, Choi IY, Choi D, Shin C. The hot pepper (Capsicum annuum) microRNA transcriptome reveals novel and conserved targets: a foundation for understanding MicroRNA functional roles in hot pepper. PLoS One, 2013, 8 e64238

[25] Ivanova D, Milev I, Vachev T, Baev V, Yahubyan G, Minkov G, Gozmanova M. Small RNA analysis of Potato spindle tuber viroid infected Phelipanche ramosa. Plant Physiol Biochem, 2014, 74: 276-282.

[26] Jia F, Rock CD. Jacalin lectin At5g28520 is regulated by ABA and miR846. Plant Signal Behav, 2013, 8 e24563

[27] Kim BH, Kwon Y, Lee BH, Nam KH. Overexpression of miR172 suppresses the brassinosteroid signaling defects of bak1 in Arabidopsis. Biochem Biophys Res Commun, 2014, 447: 479-484.

[28] Krajinski F, Courty PE, Sieh D, Franken P, Zhang H, Bucher M, Gerlach N, Kryvoruchko I, Zoeller D, Udvardi M, Hause B. The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell, 2014, 26: 1808-1817.

[29] Kulcheski FR, Correa R, Gomes IA, de Lima JC, Margis R. NPK macronutrients and microRNA homeostasis. Front Plant Sci, 2015, 6 451

[30] Latijnhouwers M, Xu XM, Moller SG. Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta, 2010, 232: 567-578.

[31] Lauressergues D, Delaux PM, Formey D, Lelandais-Briere C, Fort S, Cottaz S, Becard G, Niebel A, Roux C, Combier JP. The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant J, 2012, 72: 512-522.

[32] Lee JY, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN. Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc Natl Acad Sci U S A, 2006, 103: 6055-6060.

[33] Levy A, Szwerdszarf D, Abu-Abied M, Mordehaev I, Yaniv Y, Riov J, Arazi T, Sadot E. Profiling microRNAs in Eucalyptus grandis reveals no mutual relationship between alterations in miR156 and miR172 expression and adventitious root induction during development. BMC Genomics, 2014, 15 524

[34] Li R, Liu P, Wan Y, Chen T, Wang Q, Mettbach U, Baluska F, Samaj J, Fang X, Lucas WJ, Lin J. A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell, 2012, 24: 2105-2122.

[35] Liang RQ, Li W, Li Y, Tan CY, Li JX, Jin YX, Ruan KC. An oligonucleotide microarray for microRNA expression analysis based on labeling RNA with quantum dot and nanogold probe. Nucleic Acids Res, 2005, 33 e17

[36] Lin LL, Wu CC, Huang HC, Chen HJ, Hsieh HL, Juan HF. Identification of MicroRNA 395a in 24-Epibrassinolide-Regulated Root Growth of Arabidopsis thaliana Using MicroRNA Arrays. Int J Mol Sci, 2013, 14: 14270-14286.

[37] Lin WY, Huang TK, Leong SJ, Chiou TJ. Long-distance call from phosphate: systemic regulation of phosphate starvation responses. J Exp Bot, 2014, 65: 1817-1827.

[38] Liu Z, Kumari S, Zhang L, Zheng Y, Ware D. Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea mays. PLoS One, 2012, 7 e39786

[39] Long RC, Li MN, Kang JM, Zhang TJ, Sun Y, Yang QC. Small RNA deep sequencing identifies novel and salt-stress-regulated microRNAs from roots of Medicago sativa and Medicago truncatula. Physiol Plant, 2015, 154: 13-27.

[40] Ma X, Shao C, Wang H, Jin Y, Meng Y. Construction of small RNA-mediated gene regulatory networks in the roots of rice (Oryza sativa). BMC Genomics, 2013, 14 510

[41] Mallory AC, Bartel DP, Bartel B. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell, 2005, 17: 1360-1375.

[42] Melito S, Heuberger AL, Cook D, Diers BW, MacGuidwin AE, Bent AF. A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1 locus LRR-Kinase on soybean cyst nematode resistance. BMC Plant Biol, 2010, 10 104

[43] Meng Y, Huang F, Shi Q, Cao J, Chen D, Zhang J, Ni J, Wu P, Chen M. Genome-wide survey of rice microRNAs and microRNA-target pairs in the root of a novel auxin-resistant mutant. Planta, 2009, 230: 883-898.

[44] Meng Y, Chen D, Ma X, Mao C, Cao J, Wu P, Chen M. Mechanisms of microRNA-mediated auxin signaling inferred from the rice mutant osaxr. Plant Signal Behav, 2010, 5: 252-254.

[45] Meng Y, Ma X, Chen D, Wu P, Chen M. MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun, 2010, 393: 345-349.

[46] Miyashima S, Koi S, Hashimoto T, Nakajima K. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development, 2011, 138: 2303-2313.

[47] Miyashima S, Honda M, Hashimoto K, Tatematsu K, Hashimoto T, Sato-Nara K, Okada K, Nakajima K. A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function. Plant Cell Physiol, 2013, 54: 375-384.

[48] Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW. Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot, 2010, 61: 165-177.

[49] Moreno-Risueno MA, Van Norman JM, Benfey PN. Transcriptional switches direct plant organ formation and patterning. Curr Top Dev Biol, 2012, 98: 229-257.

[50] Muraro D, Mellor N, Pound MP, Help H, Lucas M, Chopard J, Byrne HM, Godin C, Hodgman TC, King JR, Pridmore TP, Helariutta Y, Bennett MJ, Bishopp A. Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. Proc Natl Acad Sci U S A, 2014, 111: 857-862.

[51] Nath M, Tuteja N (2015) NPKS uptake, sensing, and signaling and miRNAs in plant nutrient stress. Protoplasma. doi:10.1007/s00709-015-0845-y

[52] Nilsson L, Muller R, Nielsen TH. Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant Cell Environ, 2007, 30: 1499-1512.

[53] Ochando I, Jover-Gil S, Ripoll JJ, Candela H, Vera A, Ponce MR, Martinez-Laborda A, Micol JL. Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in arabidopsis. Plant Physiol, 2006, 141: 607-619.

[54] Omidbakhshfard MA, Proost S, Fujikura U, Mueller-Roeber B. Growth-regulating factors (GRFs): a small transcription factor family with important functions in plant biology. Mol Plant, 2015, 8: 998-1010.

[55] Ou-Yang F, Luo QJ, Zhang Y, Richardson CR, Jiang Y, Rock CD. Transposable element-associated microRNA hairpins produce 21-nt sRNAs integrated into typical microRNA pathways in rice. Funct Integr Genomics, 2013, 13: 207-216.

[56] Pant BD, Buhtz A, Kehr J, Scheible WR. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J, 2008, 53: 731-738.

[57] Paul S, Kundu A, Pal A. Identification and expression profiling of Vigna mungo microRNAs from leaf small RNA transcriptome by deep sequencing. J Integr Plant Biol, 2014, 56: 15-23.

[58] Pei L, Jin Z, Li K, Yin H, Wang J, Yang A. Identification and comparative analysis of low phosphate tolerance-associated microRNAs in two maize genotypes. Plant Physiol Biochem, 2013, 70: 221-234.

[59] Pinweha N, Asvarak T, Viboonjun U, Narangajavana J. Involvement of miR160/miR393 and their targets in cassava responses to anthracnose disease. J Plant Physiol, 2015, 174: 26-35.

[60] Radwan O, Liu Y, Clough SJ. Transcriptional analysis of soybean root response to Fusarium virguliforme, the causal agent of sudden death syndrome. Mol Plant Microbe Interact, 2011, 24: 958-972.

[61] Ramírez M, Flores-Pacheco G, Reyes JL, Luzlvarez A, Drevon JJ, Girard L, Hernandez G. Two common bean genotypes with contrasting response to phosphorus deficiency show variations in the microRNA 399-mediated PvPHO2 regulation within the PvPHR1 signaling pathway. Int J Mol Sci, 2013, 14: 8328-8344.

[62] Salemme M, Sica M, Iazzetti G, Gaudio L, Aceto S. The AP2-like gene OitaAP2 is alternatively spliced and differentially expressed in inflorescence and vegetative tissues of the orchid Orchis italica. PLoS One, 2013, 8 e77454

[63] Schoor S, Farrow S, Blaschke H, Lee S, Perry G, von Schwartzenberg K, Emery N, Moffatt B. Adenosine kinase contributes to cytokinin interconversion in Arabidopsis. Plant Physiol, 2011, 157: 659-672.

[64] Sharma N, Tripathi A, Sanan-Mishra N. Profiling the expression domains of a rice-specific microRNA under stress. Front Plant Sci, 2015, 6 333

[65] Singh A, Singh S, Panigrahi KC, Reski R, Sarkar AK. Balanced activity of microRNA166/165 and its target transcripts from the class III homeodomain-leucine zipper family regulates root growth in Arabidopsis thaliana. Plant Cell Rep, 2014, 33: 945-953.

[66] Sorin C, Declerck M, Christ A, Blein T, Ma L, Lelandais-Briere C, Njo MF, Beeckman T, Crespi M, Hartmann C. A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol, 2014, 202: 1197-1211.

[67] Sun Y, Qiu Y, Zhang X, Chen X, Shen D, Wang H, Li X. Genome-wide identification of microRNAs associated with taproot development in radish (Raphanus sativus L.). Gene, 2015, 569: 118-126.

[68] Van Norman JM, Breakfield NW, Benfey PN. Intercellular communication during plant development. Plant Cell, 2011, 23: 855-864.

[69] Vidal EA, Moyano TC, Krouk G, Katari MS, Tanurdzic M, McCombie WR, Coruzzi GM, Gutierrez RA. Integrated RNA-seq and sRNA-seq analysis identifies novel nitrate-responsive genes in Arabidopsis thaliana roots. BMC Genomics, 2013, 14 701

[70] Wang CY, Chen YQ, Liu Q. Sculpting the meristem: the roles of miRNAs in plant stem cells. Biochem Biophys Res Commun, 2011, 409: 363-366.

[71] Wang Q, Zhao Y, Luo W, Li R, He Q, Fang X, Michele RD, Ast C, von Wiren N, Lin J. Single-particle analysis reveals shutoff control of the Arabidopsis ammonium transporter AMT1;3 by clustering and internalization. Proc Natl Acad Sci U S A, 2013, 110: 13204-13209.

[72] Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J, Liao H. Genome-wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics, 2013, 14 66

[73] Yan Z, Hossain MS, Arikit S, Valdes-Lopez O, Zhai J, Wang J, Libault M, Ji T, Qiu L, Meyers BC, Stacey G. Identification of microRNAs and their mRNA targets during soybean nodule development: functional analysis of the role of miR393j-3p in soybean nodulation. New Phytol, 2015, 207: 748-759.

[74] Yang L, Conway SR, Poethig RS. Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156. Development, 2011, 138: 245-249.

[75] Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y. Submergence-responsive MicroRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot, 2008, 102: 509-519.

[76] Zhang JF, Yuan LJ, Shao Y, Du W, Yan DW, Lu YT. The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis. Plant Cell Environ, 2008, 31: 562-574.

[77] Zhang Y, Wang W, Chen J, Liu J, Xia M, Shen F. Identification of miRNAs and their targets in cotton inoculated with Verticillium dahliae by high-throughput sequencing and degradome analysis. Int J Mol Sci, 2015, 16: 14749-14768.

[78] Zhou B, Fan P, Li Y. High-throughput sequence analysis of small RNAs in skotomorphogenic seedlings of Brassica rapa ssp. rapa. Gene, 2014, 548: 68-74.