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Journal of Integrative Agriculture  2022, Vol. 21 Issue (4): 901-916    DOI: 10.1016/S2095-3119(21)63818-2
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The roles of microRNAs in regulating root formation and growth in plants
YAN Xiao-xiao, LIU Xiang-yang, CUI Hong, ZHAO Ming-qin
College of Tobacco Science, Henan Agricultural University/National Tobacco Cultivation and Physiology and Biochemistry Research Center/Key Laboratory for Tobacco Cultivation of Tobacco Industry, Zhengzhou 450002, P.R.China
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摘要  

MicroRNAs (miRNAs)是一类长度较小的非编码RNAs(约20-24个核苷酸),近年来被认为是基因表达的关键转录后调节因子,参与了植物多种生理生化过程,如根系生长与发育。miRNAs通过参与应答激素信号、营养吸收和生物/非生物胁迫反应来调节根系的伸长、侧根(AR)形成和不定根(AR)的发育。本文汇总了miRNAs参与调控植物根系生长发育的多方面的研究进展,还讨论了根系生长发育过程中miRNAs发挥功能的若干关键调控机制,miRNAs与转录因子的调控关系,以及与其靶基因介导的激素信号之间的相互调控作用。




Abstract  MicroRNAs (miRNAs) are small (ca. 20–24 nucleotides) non-coding RNAs that have recently been recognized as key post-transcriptional modulators of gene expression; and they are involved in many biological processes in plants, such as root growth and development.  The miRNAs regulate root elongation, lateral root (LR) formation and adventitious root (AR) development in response to hormone signaling, nutrient uptake and biotic/abiotic stress.  This review provides multiple perspectives on the involvement of miRNAs in regulating root growth and development in plants.  We also discuss several crucial mechanisms of miRNAs, their relationships with transcription factors and the target gene-mediated hormone signaling interactions in the regulation of root growth and development.
Keywords:  microRNAs       adventitious root       lateral root       primary root  
Received: 01 May 2021   Accepted: 06 August 2021
Fund: This work was funded by the Science and Technology Department of Henan Province, China (212102110046), the State Tobacco Monopoly Administration of China (110202101005 (JY-05)), the Science and Technology Project of China National Tobacco Corporation Henan Tobacco Company, China (2018410000270095), and the Undergraduate Innovation and Entrepreneurship Project of Henan Province, China (202110466042).  
About author:  YAN Xiao-xiao, Tel: +86-371-63555763, E-mail: xiaoxyan@henau.edu.cn; Correspondence CUI Hong, Tel: +86-371-63555763, E-mail: cuihong@henau.edu.cn; ZHAO Ming-qin, Tel: +86-371-63555763, E-mail: zhaomingqin@henau.edu.cn

Cite this article: 

YAN Xiao-xiao, LIU Xiang-yang, CUI Hong, ZHAO Ming-qin. 2022. The roles of microRNAs in regulating root formation and growth in plants. Journal of Integrative Agriculture, 21(4): 901-916.

Alptekin B, Langridge P, Budak H. 2017. Abiotic stress miRNomes in the Triticeae. Functional & Integrative Genomics, 17, 145–170. 
An L J, Zhou Z J, Sun L L, Yan A, Xi W Y, Yu N, Cai W J, Chen X Y, Yu H, Schiefelbein J, Gan Y B. 2012. A zinc finger protein gene ZFP5 integrates phytohormone signalling to control root hair development in Arabidopsis. Plant Journal, 72, 474–490.
Antoniadi I, Plackova L, Simonovic B, Dolezal K, Turnbull C, Ljung K, Novak O. 2015. Cell-type-specific cytokinin distribution within the Arabidopsis primary root apex. Plant Cell, 27, 1955–1967.
Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A. 2013. ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Frontiers in Plant Science, 4, 63–81.
Aung B, Gao R, Gruber M Y, Yuan Z C, Sumarah M, Hannoufa A. 2017. MsmiR156 affects global gene expression and promotes root regenerative capacity and nitrogen fixation activity in alfalfa. Transgenic Research, 26, 541–557.
Bai B, Bian H, Zeng Z, Hou N, Shi B, Wang J, Zhu M, Han N. 2017. miR393-mediated auxin signaling regulation is involved in root elongation inhibition in response to toxic aluminum stress in barley. Plant and Cell Physiology, 58, 426–439.
Barakat A, Wall P K, Diloreto S, Depamphilis C W, Carlson J E. 2007. Conservation and divergence of microRNAs in Populus. BMC Genomics, 8, 481–496.
Barrera-Rojas C H, Rocha G H B, Polverari L, Brito D A P, Batista D S, Notini M M, da Cruz A C F, Morea E G O, Sabatini S, Otoni W C, Nogueira F T S. 2020. miR156-targeted SPL10 controls Arabidopsis root meristem activity and root-derived de novo shoot regeneration via cytokinin responses. Journal of Experimental Botany, 71, 934–950.
Bartel D P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.
Bazin J, Khan G A, Combier J P, Bustos-Sanmamed P, Debernardi J M, Rodriguez R, Sorin C, Palatnik J, Hartmann C, Crespi M. 2013. miR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula. Plant Journal, 74, 920–934. 
Bellini C, Pacurar D I, Perrone I. 2014. Adventitious roots and lateral roots: Similarities and differences. Annual Review of Plant Biology, 65, 639–666.
Bian H, Xie Y, Guo F, Han N, Ma S, Zeng Z, Wang J, Yang Y, Zhu M. 2012. 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 Phytologist, 196, 149–161. 
Brant E J, Budak H. 2018. Plant small non-coding RNAs and their roles in biotic stresses. Frontiers in Plant Science, 9, 1038–1046. 
Budak H, Akpinar A. 2011. Dehydration stress-responsive miRNA in brachypodium distachyon: Evident by genome-wide screening of microRNAs expression. OMICS (A Journal of Integrative Biology), 15, 791–799. 
Budak H, Kantar M, Bulut R, Akpinar B A. 2015. Stress responsive miRNAs and isomiRs in cereals. Plant Science, 235, 1–13. 
Bustillo-Avendano E, Ibáñez S, Sanz O, Barros J A S, Gude I, Perianez-Rodriguez J, Micol J L, Del Pozo J C, Moreno-Risueno M A, Pérez-Pérez J M. 2018. Regulation of hormonal control, cell reprogramming, and patterning during de novo root organogenesis. Plant Physiology, 176, 1709–1727. 
Carlsbecker A, Lee J Y, Roberts C J, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno M A, Vatén A, Thitamadee S, Campilho A, Sebastian J, Bowman J L, Helariutta Y, Benfey P N. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature, 465, 316–321.
Chaiwanon J, Wang Z Y. 2015. Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Current Biology, 25, 1031–1042.
Chen H, Li Z, Xiong L. 2012. A plant microRNA regulates the adaptation of roots to drought stress. FEBS Letters, 586, 1742–1747.
Chen H, Ma B, Zhou Y, He S J, Tang S Y, Lu X, Xie Q, Chen S Y, Zhang J S. 2018. E3 ubiquitin ligase SOR1 regulates ethylene response in rice root by modulating stability of Aux/IAA protein. Proceedings of the National Academy of Sciences of the United States of America, 115, 4513–4518.
Chen Q, Deng B, Gao J, Zhao Z, Chen Z, Song S, Wang L, Zhao L, Xu W, Zhang C, Ma C, Wang S. 2020. A miRNA-encoded small peptide, vvi-miPEP171d1, regulates adventitious root formation. Plant Physiology, 183, 656–670.
Chung P J, Park B, Wang H, Liu J, Jang I C, Chua N H. 2016. Light-inducible miR163 targets PXMT1 transcripts to promote seed germination and primary root elongation in Arabidopsis. Plant Physiology, 170, 1772–1782.
Coudert Y, Le T V A, Gantet P. 2013. Rice: A model plant to decipher the hidden origin of adventitious roots. In: Eshel A, Beeckman T, eds., Plant Roots (The Hidden Half). CRC Press, USA. pp. 157–166.
Coudert Y, Périn C, Courtois B, Khong N G, Gantet P. 2010. Genetic control of root development in rice, the model cereal. Trends in Plant Science, 15, 219–226. 
Couzigou J M, Combier J P. 2016. Plant microRNAs: Key regulators of root architecture and biotic interactions. New Phytologist, 212, 22–35.
De Cuper C, Fromention J, Yocgo R, De Keyser A, Guillotin B, Kunert K, Goormachtig S. 2015. From lateral density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncayula. Journal of Experimental Botany, 66, 137–146.
Cuperus J T, Fahlgren N, Carrington J C. 2011. Evolution and functional diversification of MIRNA genes. Plant Cell, 23, 431–442.
Curaba J, Singh M B, Bhalla P L. 2014. miRNAs in the crosstalk between phytohormone signalling pathways. Journal of Experimental Botany, 65, 1425–1438.
Dello Ioio R, Galinha C, Fletcher A G, Grigg S P, Molnar A, Willemsen V, Scheres B, Sabatini S, Baulcombe D, Maini P K, Tsiantis M. 2012. A PHABULOSA/cytokinin feedback loop controls root growth in Arabidopsis. Current Biology, 22, 1699–1704.
Dominik K G, Jan P. 2019. Auxins and cytokinins - the dynamic duo of growth-regulating phytohormones heading for new shores. New Phytologist, 221, 1187–1190.
Dubois M, Van den Broeck L, Inzé D. 2018. The pivotal role of ethylene in plant growth. Trends in Plant Science, 23, 311–323.
Ebert M, Sharp P. 2012. Roles for microRNAs in conferring robustness to biological processes. Cell, 149, 515–524.
Fan P, Aguilar E, Bradai M, Xue H, Lozano-Duran R. 2021. The receptor-like kinases BAM1 and BAM2 are required for root xylem patterning. Proceedings of the National Academy of Sciences of the United States of America, 118, e2022547118.
Fattorini L, Falasca G, Kevers C, Rocca L M, Zadra C, Altamura M M. 2009. Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers. Planta, 231, 155–168.
Fendrych M, Akhmanova M, Merrin J, Glanc M, Hagihara S, Takahashi K, Uchida N, Torii K U, Friml J. 2018. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nature Plants, 4, 453–459.
Feng S, Xu Y, Guo C, Zheng J, Zhou B, Zhang Y, Ding Y, Zhang L, Zhu Z, Wang H, Wu G. 2016. Modulation of miR156 to identify traits associated with vegetative phase change in tobacco (Nicotiana tabacum). Journal of Experimental Botany, 67, 1493–1504. 
Feng Y, Xu P, Li B S, Li P P, Wen X, An F Y, Gong Y, Xin Y, Zhu Z Q, Wang Y C, Guo H W. 2017. Ethylene promotes root hair growth through coordinated EIN3/EIL1 and RHD6/RSL1 activity in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 114, 13834–13839.
Friedman R C, Farh K K, Burge C B, Bartel D P. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Research, 19, 92–105.
Galstyan A, Nemhauser J L. 2019. Auxin promotion of seedling growth via ARF5 is dependent on the brassinosteroid-regulated transcription factors BES1 and BEH4. Plant Direct, 3, 1–11.
Gao R, Wang Y, Gruber M Y, Hannoufa A. 2018. miR156/SPL10 modulates lateral root development, branching and leaf morphology in Arabidopsis by silencing AGAMOUS-LIKE 79. Frontier in Plant Science, 8, 2226–2237.
Gao S, Fang J, Xu F, Wang W, Sun X, Chu J, Cai B, Feng Y, Chu C. 2014. Cytokinin oxidase/dehydrogenase 4 integrates cytokinin and auxin signaling to control rice crown root formation. Plant Physiology, 165, 1035–1046.
Gautam V, Singh A, Verma S, Kumar A, Kumar P, Mahima Singh S, Mishra V, Sarkar A K. 2017. Role of miRNAs in root development of model plant Arabidopsis thaliana. Indian Journal of Plant Physiology, 22, 382–392.
Ghildiyal M, Zamore P D. 2009. Small silencing RNAs: An expanding universe. Nature Review Genetics, 10, 94–108.
Gifford M L, Dean A, Gutierrez R A, Coruzzi G M, Birnbaum K D. 2008. Cell-specific nitrogen responses mediate developmental plasticity. Proceedings of the National Academy of Sciences of the United States of America, 105, 803–808.
Giri J, Bhosale R, Huang G, Pandey B, Parker H, Zappala S, Yang J, Dievart A, Bureau C, Ljung K, Price A, Rose T, Larrieu A, Mairhofer S, Sturrock C J, White P, Dupuy L, Hawkesford M, Perin C, Liang W, et al. 2018. The rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nature Communication, 9, 1408–1414. 
Goldfarb B, Hackett W P, Furnier G R, Mohn C A, Plietzsch A. 1998. Adventitious root initiation in hypocotyl and epicotyl cuttings of eastern white pine (Pinus strobus) seedlings. Physiologia Plantarum, 102, 513–522. 
Gonin M, Bergougnoux V, Nguyen T D, Gantet P, Champion A. 2019. What makes adventitious roots. Plants, 8, 240.
Guo H S, Xie Q, Fei J F, Chua N H. 2005. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell, 17, 1376–1386.
Gutierrez L, Bussell J D, Pacurar D I, Schwambach J, Pacurar M, Bellini C. 2009. Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell, 21, 3119–3132. 
Gutierrez L, Mongelard G, Floková K, Păcurar D I, Novák O, Staswick P, Kowalczyk M, Păcurar M, Demailly H, Geiss G, Bellini C. 2012. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell, 24, 2515–2527. 
Hetherington F M, Kakkar M, Topping J F, Lindsey K. 2021. Gibberellin signaling mediates lateral root inhibition in response to K+-deprivation. Plant Physiology, 185, 1198–1215.
Hobecker K V, Reynoso M A, Bustos-Sanmamed P, Wen J, Mysore K S, Crespi M, Blanco F A, Zanetti M E. 2017. The microRNA390/TAS3 pathway mediates symbiotic nodulation and lateral root growth. Plant Physiology, 174, 2469–2486. 
Hochholdinger F, Zimmermann R. 2008. Conserved and diverse mechanisms in root development. Current Opinion in Plant Biology, 11, 70–74. 
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 Physiology, 156, 1101–1115.
Huang J, Li Z, Zhao D. 2016. Deregulation of the OsmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice. Scientific Reports, 6, 29938–29951.
Jean-Malo C, Jean-Philippe C. 2016. Plant microRNAs: Key regulators of root architecture and biotic interactions. New Phytologist, 212, 22–35.
Jeong D H, Park S, Zhai J, Gurazada S G R, Paoli E D, Meyers B C, Green P J. 2011. Massive analysis of rice small RNAs: Mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell, 23, 4185–4207.
Jiang L, Matthys C, Marquez-Garcia B, De Cuyper C, Smet L, De Keyser A, Boyer F D, Beeckman T, Depuydt S, Goormachtig S. 2016. Strigolactones spatially influence lateral root development through the cytokinin signaling network. Journal of Experimental Botany, 67, 379–389.
Jiao X, Wang H, Yan J, Kong X, Liu Y, Chu J, Chen X, Fang R, Yan Y. 2020. Promotion of BR biosynthesis by miR444 is required for ammonium-triggered inhibition of root growth. Plant Physiology, 182, 1454–1466.
Joshi-Saha A, Valon C, Leung J. 2011. Abscisic acid signal off the STARTing block. Molecular Plant, 4, 562–580.
Kantar M, Lucas S J, Budak H. 2011. miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta, 233, 471–484. 
Kantar M, Unver T, Budak H. 2010. Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Functional & Integrative Genomics, 10, 493–507.
Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H. 2011. Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. Journal of Experimental Botany, 62, 2915–2924.
Kawamata T, Tomari Y. 2010. Making RISC. Trends in Biochemical Sciences, 35, 368–376.
Kenrick P. 2013. The origin of roots. In: Eshel A, Beeckman T, eds., Plant Roots (The Hidden Half). CRC Press, USA. pp. 1–13.
Kim V N, Han J, Siomi M C. 2009. Biogenesis of small RNAs in animals. Nature Reviews Molecular Cell Biology, 10, 126–139.
De Klerk G J, Guan H Y, Huisman P, Marinova S. 2011. Effects of phenolic compounds on adventitious root formation and oxidative decarboxylation of applied indoleacetic acid in Malus ‘Jork 9’. Plant Growth Regulation, 63, 175–185.
Lachowiec J, Mason G A, Schultz K, Queitsch C. 2018. Redundancy, feedback, and robustness in the Arabidopsis thaliana BZR/BEH gene family. Frontiers in Genetics, 2018, 523–552.
Lakehal A, Bellini C. 2019. Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiologia Plantarum, 165, 90–100. 
Lauressergues D, Couzigou J M, Clemente H S, Martinez Y, Dunand C, Becard G, Combier J P. 2015. Primary transcripts of microRNAs encode regulatory peptides. Nature, 520, 90–93.
Li H, Gao Z, Zahid M S, Li D, Javed H U, Wang L, Song S, Zhao L, Xu W, Zhang C, Ma C, Wang S. 2020. Small RNA sequencing analysis of miRNA expression reveals novel insihts into root formation under root restriction cultivation in grapevine (Vitis vinifera L.). International Journal of Molecular Sciences, 21, 3513–3537. 
Li H, Hu B, Wang W, Zhang Z, Liang Y, Gao X, Li P, Liu Y, Zhang L, Chu C. 2016. Identification of microRNAs in rice root in response to nitrate and ammonium. Journal of Genetics and Genomics, 43, 651–661. 
Li J, Guo G, Guo W, Guo G, Tong D, Ni Z, Sun Q, Yao Y. 2012. miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biology, 12, 220.
Li J, Xu H H, Liu W C, Zhang X W, Lu Y T. 2015. Ethylene inhibits root elongation during alkaline stress through AUXIN1 and associated changes in auxin accumulation. Plant Physiology, 168, 1777–1791.
Li K, Liu Z, Xing L, Wei Y, Mao J, Meng Y, Bao L, Han M, Zhao C, Zhang D. 2019. miRNAs associated with auxin signaling, stress response, and cellular activities mediate adventitious root formation in apple rootstocks. Plant Physiology and Biochemistry, 139, 66–81.
Li T, Lian H, Li H, Xu Y, Zhang H. 2021. HY5 regulates light-responsive transcription of microRNA163 to promote primary root elongation in Arabidopsis seedlings. Journal of Integrative Plant Biology, doi: 10.1111/jipb.13099. 
Li X, Guo Z, Lv Y, Cen X, Ding X, Wu H, Li X. 2017. Genetic control of the root system in rice under normal and drought stress conditions by genome-wide association study. PLoS Genetics, 13, e1006889.
Liang G, He H, Yu D. 2012. Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS ONE, 7, e48951.
Lin C, Sauter M. 2019. Polar auxin transport determines adventitious root emergence and growth in rice. Frontiers in Plant Science, 10, 444–455. 
Lischweski S, Muchow A, Guthörl D, Hause B. 2015. Jasmonates act positively in adventitious root formation in petunia cuttings. BMC Plant Biology, 15, 1–10.
Liu J, Moore S, Chen C, Lindsey K. 2017. Crosstalk complexities between auxin, cytokinin, and ethylene in Arabidopsis root development: From experiments to systems modeling, and back again. Molecular Plant, 10, 1480–1496.
Liu Q, Zhang Y C, Wang C Y, Luo Y C, Huang Q J, Chen S Y, Zhou H, Qu L H, Chen Y Q. 2009. Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Letters, 583, 1723–1728.
Liu W, Kohlen W, Lillo A, Op den Camp R, Ivanov S, Hartog M, Limpens E, Jamil M, Smaczniak C, Kaufmann K, Yang W C, Hooiveld G J, Charnikhova T, Bouwmeester H J, Bisseling T, Geurts R. 2011. Strigolactone biosynthesis in Medicago truncatula and rice requires the symbiotic GRAS-type transcription factors NSP1 and NSP2. Plant Cell, 23, 3853–3865.
Liu Z, Kumari S, Zhang L, Zheng Y, Ware D. 2012. Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea mays. PLoS ONE, 7, e39786.
Lombardi-Crestana S, da Silva Azevedo M, Silva G F, Pino L E, Appezzato-da-Glória B, Figueira A, Nogueira F T, Peres L E. 2012. The tomato (Solanum lycopersicum cv. Micro-Tom) natural genetic variation Rg1 and the DELLA mutant procera control the competence necessary to form adventitious roots and shoots. Journal of Experimental Botany, 63, 5689–5703. 
Lucas M, Swarup R, Paponov I A, Swarup K, Casimiro I, Lake D, Peret B, Zappala S, Mairhofer S, Whitworth M, Wang J, Ljung K, Marchant A, Sandberg G, Holdsworth M J, Palme K, Pridmore T, Mooney S, Bennett M J. 2011. SHORT-ROOT regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiology, 155, 384–398.
Luo X, Chen Z, Gao J, Gong Z. 2014. Abscisic acid inhibits root growth in Arabidopsis through ethylene biosynthesis. Plant Journal, 79, 44–55.
Ma B, Yin C C, He S J, Lu X, Zhang W K, Lu T G, Chen S Y, Zhang J S. 2014. Ethylene-induced inhibition of root growth requires abscisic acid function in rice (Oryza sativa L.) seedlings. PLoS Genetics, 10, e1004701. 
Marin E, Jouannet V, Herz A, Lokerse A S, Weijers D, Vaucheret H, Nussaume L, Crespi M D, Maizel A. 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.
Mayzlish-Gati E, De-Cuyper C, Goormachtig S, Beeckman T, Vuylsteke M, Brewer P B, Beveridge C A, Yermiyahu U, Kaplan Y, Enzer Y, Wininger S, Resnick N, Cohen M, Kapulnik Y, Koltai H. 2012. Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiology, 160, 1329–1341.
Meng Y, Huang F, Shi Q, Cao J, Chen D, Zhang J, Ni J, Wu P, Chen M. 2009. Genome-wide survey of rice microRNAs and microRNA-target pairs in the root of a novel auxin-resistant mutant. Planta, 230, 883–898. 
Moriconi J I, Kotula L, Santa-María G E, Colmer T D. 2019. Root phenotypes of dwarf and “overgrowth” SLN1 barley mutants, and implications for hypoxic stress tolerance. Journal of Plant Physiology, 234, 60–70.
Morris E C, Griffiths M, Golebiowska A, Mairhofer S, Burr-Hersey J, Goh T, von Wangenheim D, Atkinson B, Sturrock C J, Lynch J P, Vissenberg K, Ritz K, Wells D M, Mooney S J, Bennett M J. 2017. Shaping 3D root architecture. Current Biology, 27, R919–R930.
Muraro D, Mellor N, Pound M P, Help H, Lucas M, Chopard J, Byrne H M, Godin C, Hodgman T C, King J R, Pridmore T P, Helariutta Y, Bennett M J, Bishopp A. 2014. Integration of hormonal signaling networks and mobile microRNAs is required for vascular patterning in Arabidopsis roots. Proceedings of the National Academy of Sciences of the United States of America, 111, 857–862.
Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones J D. 2006. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312, 436–439. 
Niu J, Wang J, Hu H, Chen Y, An J, Cai J, Sun R, Sheng Z, Liu X, Lin S. 2016. Cross-talk between freezing response and signaling for regulatory transcriptions of MIR475b and its targets by miR475b promoter in Populus suaveolens. Scientific Reports, 6, 20648.
Niu S, Li Z, Yuan H, Fang P, Chen X, Li W. 2013. Proper gibberellin localization in vascular tissue is required to regulate adventitious root development in tobacco. Journal of Experimental Botany, 64, 3411–3424.
Pacheco-Villalobos D, Sankar M, Ljung K, Hardtke C S. 2013. Disturbed local auxin homeostasis enhances cellular anisotropy and reveals alternative wiring of auxin-ethylene crosstalk in Brachypodium distachyon seminal roots. PLoS Genetics, 9, e1003564.
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 Journal, 62, 960–976.
Pekker I, Alvarez J P, Eshed Y. 2005. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell, 17, 2899–2910.
Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett M J. 2009. Arabidopsis lateral root development: An emerging story. Trends in Plant Science, 14, 399–408.
Petersson S V, Johansson A I, Kowalczyk M, Makoveychuk A, Wang J Y, Moritz T, Grebe M, Benfey P N, Sandberg G, Ljung K. 2009. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell, 21, 1659–1668.
Poethig R S. 1988. Heterochronic mutations affecting shoot development in maize. Genetics, 119, 959–973.
Qi Y, Wang S, Shen C, Zhang S, Chen Y, Xu Y, Liu Y, Wu Y, Jiang D. 2012. OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytologist, 193, 109–120. 
Rajagopalan R, Vaucheret H, Trejo J, Bartel D P. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Gene & Development, 20, 3407–3425.
Rasmussen A, Mason M G, De Cuyper C, Brewer P B, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, Beveridge C A. 2012. Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiology, 158, 1976–1987. 
Reyes J L, Chua N H. 2007. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant Journal, 49, 592–606.
Rodriguez R E, Ercoli M F, Debernardi J M, Breakfield N W, Mecchia M A, Sabatini M, Cools T, De Veylder L, Benfey P N, Palatnik J F. 2015. MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis roots. Plant Cell, 27, 3354–3366. 
Rogers K, Chen X. 2013. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell, 25, 2383–2399. 
Schoenaers S, Balcerowicz D, Breen G, Hill K, Zdanio M, Mouille G, Holman T J, Oh J, Wilson M H, Nikonorova N, Vu L D, De Smet I, Swarup R, De Vos W H, Pintelon I, Adriaensen D, Grierson C, Bennett M J, Vissenberg K. 2018. The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth. Current Biology, 28, 722–732.
El-Sharkawy I, El Kayal W, Prasath D, Fernandez H, Bouzayen M, Svircev A M, Jayasankar S. 2012. Identification and genetic characterization of a gibberellin 2-oxidase gene that controls tree stature and reproductive growth in plum. Journal of Experimental Botany, 63, 1225–1239.
Shen C, Wang S, Zhang S, Xu Y, Qian Q, Qi Y, Jiang D A. 2013. OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativa L.). Plant Cell & Environment, 36, 607–620.
Singh A, Roy S, Singh S, Das S S, Gautam V, Yadav S, Kumar A, Singh A, Samantha S, Sarkar A K. 2017. Phytohormonal crosstalk modulates the expression of miR166/165s, target Class III HD-ZIPs, and KANADI genes during root growth in Arabidopsis thaliana. Scientific Reports, 7, 3408–3420. 
Song Q X, Liu Y F, Hu X Y, Zhang W K, Ma B A, Chen S Y, Zhang J S. 2011. Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biology, 11, 5–20.
Sorin C, Declerck M, Christ A, Blein T, Ma L, Lelandais-Brière C, Njo M F, Beeckman T, Crespi M, Hartmann C. 2014. A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytologist, 202, 1197–1211. 
Sun H, Bi Y, Tao J, Huang S, Hou M, Xue R, Liang Z, Gu P, Yoneyama K, Xie X, Shen Q, Xu G, Zhang Y. 2016. Strigolactones are required for nitric oxide to induce root elongation in response to nitrogen and phosphate deficiencies in rice. Plant Cell & Environment, 39, 1473–1484.
Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G. 2014. Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. Journal of Experimental Botany, 65, 6735–6746. 
Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen J D, Palme K, Li C. 2009. Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell, 21, 1495–1511.
Vanstraelen M, Benkov E. 2012. Hormonal interactions in the regulation of plant development. Annual Review of Cell and Developmental Biology, 28, 463–487.
Veloccia A, Fattorini L, Della Rovere F, Sofo A, D’Angeli S, Betti C, Falasca G, Altamura M M. 2016. Ethylene and auxin interaction in the control of adventitious rooting in Arabidopsis thaliana. Journal of Experimental Botany, 67, 6445–6458. 
Vidal E A, Alvarez J M, Gutierrez R A. 2014. Nitrate regulation of AFB3 and NAC4 gene expression in Arabidopsis roots depends on NRT1.1 nitrate transport function. Plant Signaling & Behavior, 9, e28501.
Vidal E A, Araus V, Lu C, Parry G, Green P J, Coruzzi G M, Gutierrez R A. 2010. Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 107, 4477–4482.
Vidal E A, Moyano T C, Riveras E, Contreras-Lopez O, Gutierrez R A. 2013. Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proceedings of the National Academy of Sciences of the United States of America, 110, 12840–12845.
Vissenberg K, Claeijs N, Balcerowicz D, Schoenaers S. 2020. Hormonal regulation of root hair growth and responses to the environment in Arabidopsis thaliana. Journal of Experimental Botany, 71, 2412–2427.
Wang J J, Guo H S. 2015. Cleavage of INDOLE-3-ACETIC ACID INDUCIBLE28 mRNA by MicroRNA847 upregulates auxin signaling to modulate cell proliferation and lateral organ growth in Arabidopsis. Plant Cell, 27, 574–590. 
Wang J W, Wang L J, Mao Y B, Cai W J, Xue H W, Chen X Y. 2005. Control of root cap formation by MicroRNA-targeted auxin response factors in Arabidopsis. Plant Cell, 17, 2204–2216. 
Wang L, Mai Y X, Zhang Y C, Luo Q, Yang H Q. 2010. MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in Arabidopsis. Molecular Plant, 3, 794–806. 
Wang Y, Wang Z, Amyot L, Tian L, Xu Z, Gruber M Y, Hannoufa A. 2015. Ectopic expression of miR156 represses nodulation and causes morphological and developmental changes in Lotus japonicus. Molecular Genetics & Genomics, 290, 471–484.
Wei Z, Li J. 2016. Brassinosteroids regulate root growth, development, and symbiosis. Molecular Plant, 9, 86–100. 
Xia K, Ou X, Tang H, Wang R, Wu P, Jia Y, Wei X, Xu X, Kang S H, Kim S K, Zhang M. 2015. Rice microRNA osa-miR1848 targets the obtusifoliol 14α-demethylase gene OsCYP51G3 and mediates the biosynthesis of phytosterols and brassinosteroids during development and in response to stress. New Phytologist, 208, 790–802.
Xia R, Xu J, Arikit S, Meyers B. 2015. Extensive families of miRNAs and PHAS loci in Norway Spruce demonstrate the origins of complex phasiRNA networks in seed plants. Molecular Biology and Evolution, 32, 2905–2918.
Xia R, Zhu H, An Y Q, Beers E P, Liu Z R. 2012. Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biology, 13, R47
Xie Q, Frugis G, Colgan D, Chua N H. 2000. Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes & Development, 14, 3024–3036.
Xu M, Hu T, Zhao J, Park M Y, Earley K W, Wu G, Yang L, Poethig R S. 2016. Developmental functions of miR156-regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in Arabidopsis thaliana. PLoS Genetics, 12, e1006263.
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 Genomics, 11, 246–262.
Xu X Z, Li X, Hu X W, Wu T, Wang Y, Xu X, Zhang X Z, Han Z H. 2017. High miR156 expression is required for auxin-induced adventitious root formation via MxSPL26 independent of PINs and ARFs in Malus xiaojinensis. Frontiers in Plant Science, 8, 1059–1075.
Xue T, Liu Z, Dai X, Xiang F. 2017. Primary root growth in Arabidopsis thaliana is inhibited by the miR159 mediated repression of MYB33, MYB65 and MYB101. Plant Science, 262, 182–189.
Yan Y, Wang H, Hamera S, Chen X, Fang R. 2014. miR444a has multiple functions in the rice nitrate-signaling pathway. Plant Journal, 78, 44–55. 
Yang W, Zhu C H, Ma X L, Li G J, Gan L J, Ng D, Xia K. 2013. Hydrogen peroxide is a second messenger in the salicylic acid-triggered adventitious rooting process in mung bean seedlings. PLoS ONE, 8, 1–14. 
Yi K, Menand B, Bell E, Dolan L. 2010. A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nature Genetics, 42, 264–267. 
Yi X, Zhang Z, Ling Y, Xu W, Su Z. 2015. PNRD: A plant non-coding RNA database. Nucleic Acids Research, 43, 982–989.
Yoon E K, Yang J H, Lim J, Kim S H, Kim S K, Lee W S. 2010. Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Research, 38, 1382–1391.
Yu N, Niu Q W, Ng K H, Chua N H. 2015. The role of miR156/SPLs modules in Arabidopsis lateral root development. Plant Journal, 83, 673–685. 
Zhang B, Wang Q. 2015. MicroRNA-based biotechnology for plant improvement. Journal of Cellular Physiology, 230, 1–15.
Zhang F, Wang L, Lim J Y, Kim T, Pyo Y, Sung S, Shin C, Qiao H. 2016. Phosphorylation of CBP20 links microRNA to root growth in the ethylene response. PLoS Genetics, 12, e1006437. 
Zhang J F, Yuan L J, Shao Y, Du W, Yan D W, Lu Y T. 2008. The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis. Plant Cell & Environment, 31, 562–574. 
Zhang L, Yao L, Zhang N, Yang J, Zhu X, Tang X, Calderón-Urrea A, Si H. 2018. Lateral root development in potato is mediated by stu-mi164 regulation of NAC transcription factor. Frontiers in Plant Science, 9, 383–391. 
Zhang L F, Chia J M, Kumari S, Stein J C, Liu Z J, Narechania A, Maher C A, Guill K, McMullen M D, Ware D. 2009. A genome-side characterization of microRNA genes in maize. PLoS Genetics, 5, e1000716.
Zhao C Z, Xia H, Frazier T P, Yao Y Y, Bi Y P, Li A Q, Li M J, Li C S, Zhang B H, Wang X J. 2010. Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biology, 10, 3–14.
Zhao Y. 2012. Auxin biosynthesis: A simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Molecular Plant, 5, 334–338.
Zhao Y, Cheng S, Song Y, Huang Y, Zhou S, Liu X, Zhou D X. 2015. The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell, 27, 2469–2483.
Zheng C, Ye M, Sang M, Wu R. 2019. A regulatory network for miR156-SPL module in Arabidopsis thaliana. Internationnal Journal of Molecular Sciences, 20, 6166–6181.
Zhou Y, Liu X, Engstrom E M, Nimchuk Z L, Pruneda-Paz J L, Tarr P T, Yan A, Kay S A, Meyerowitz E M. 2015. Control of plant stem cell function by conserved interacting transcriptional regulators. Nature, 517, 377–380. 
Zhu Q H, Spriggs A, Matthew L, Fan L J, Kennedy G, Gubler F, Helliwell C. 2008. A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Research, 18, 1456–1465.
Zhu Y Y, Zeng H Q, Dong C X, Yin X M, Shen Q R, Yang Z M. 2010. microRNA expression profiles associated with phosphorus deficiency in white lupin (Lupinus albus L.). Plant Science, 178, 23–29.

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