Abstract
Abiotic stresses like drought, extreme temperature, and lack of sufficient water or nutrients adversely affect plant growth and productivity. The physiological responses of higher plants to the environmental stresses are largely influenced by the root system, which can quickly modulate its developmental pattern under changing water, nutrient, and temperature, as an adaptive response. Protein coding genes, phytohormones and microRNAs (miRNAs) are among the key players which imparts crucial intrinsic role in shaping the root development and its environment adaptive growth pattern. Among these factors, miRNAs belong to a class of small non-coding RNAs of 21–24 nucleotides in length, which regulates various aspects of plant growth and development by negatively regulating their target genes through either transcriptional cleavage or translational inhibition. Although many miRNAs have been identified to be differentially regulated under various abiotic stress conditions, only a limited number of them have been characterized, due to the complex nature of its regulation. However, some of the miRNAs, such as miR156, miR165/166, miR169 etc., have recently been shown to be involved in both abiotic stress response and root development, indicating the diverse role of miRNA mediated gene regulation. The field of miRNA mediated gene regulation is dynamically expanding and more miRNAs are being characterized for their function. Current review focuses on miRNAs that are differentially regulated by major abiotic stresses as well as are involved in root development in Arabidopsis thaliana. We highlight their role in regulation of multiple and diverse aspects of developmental and physiological processes in Arabidopsis.
Similar content being viewed by others
Abbreviations
- PR:
-
Primary root
- LR:
-
Lateral root
- AR:
-
Adventitious root
- SCN:
-
Stem cell niche
- QC:
-
Quiescent centre
- RSA:
-
Root system architecture
- miRNA:
-
microRNA
References
Aida M et al (2004) The PLETHORA genes mediate patterning of the ArabidopsisArabidopsis root stem cell niche. Cell 119(1):109–120. https://doi.org/10.1016/j.cell.2004.09.018
Alonso-Peral MM et al (2010) The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol 154(2):757–771. https://doi.org/10.1104/pp.110.160630
Aslam M, Sugita K, Qin Y, Rahman A (2020) Deciphering miRNAs involved in crosstalk between auxin and cold stress in Arabidopsis roots. https://doi.org/10.21203/rs.3.rs-29695/v1
Barik S et al (2014) Phylogenetic analysis reveals conservation and diversification of microRNA166 genes among diverse plant species. Genomics 103(1):114–121. https://doi.org/10.1016/j.ygeno.2013.11.004
Barik S et al (2015) Coevolution pattern and functional conservation or divergence of miR167s and their targets across diverse plant species. Sci. Rep.Sci. Rep. 5:14611. https://doi.org/10.1038/srep14611
Barrera-Rojas CH et al (2019) miR156-targeted SPL10 controls Arabidopsis root meristem activity and root-derived de novo shoot regeneration via cytokinin responses. J Exp Bot 71(3):934–950. https://doi.org/10.1093/jxb/erz475
Baumberger N, Baulcombe DC (2005) Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102(33):11928–11933. https://doi.org/10.1073/pnas.0505461102
Bellstaedt J et al (2019) A mobile auxin signal connects temperature sensing in cotyledons with growth responses in hypocotyls. Plant Physiol 180(2):757–766. https://doi.org/10.1104/pp.18.01377
Brodersen P et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320(5880):1185–1190. https://doi.org/10.1126/science.1159151
Cai X et al (2006) Mutant identification and characterization of the laccase gene family in Arabidopsis. J Exp Bot 57(11):2563–2569. https://doi.org/10.1093/jxb/erl022
Carlsbecker A et al (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465(7296):316–321. https://doi.org/10.1038/nature08977
Casadevall R, Rodriguez RE, Debernardi JM, Palatnik JF, Casati P (2013) Repression of growth regulating factors by the microRNA396 inhibits cell proliferation by UV-B radiation in Arabidopsis leaves. Plant Cell 25(9):3570–3583. https://doi.org/10.1105/tpc.113.117473
Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666):2022–2025. https://doi.org/10.1126/science.1088060
Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44. https://doi.org/10.1146/annurev.cellbio.042308.113417
Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2014) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J Cell Mol Biol 80:1108–1117
Deak KI, Malamy J (2005) Osmotic regulation of root system architecture. Plant J 43(1):17–28. https://doi.org/10.1111/j.1365-313X.2005.02425.x
Denver JB, Ullah H (2019) miR393s regulate salt stress response pathway in Arabidopsis thaliana through scaffold protein RACK1A mediated ABA signaling pathways. Plant Signal Behav 14(6):1600394. https://doi.org/10.1080/15592324.2019.1600394
Dolan L et al (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119(1):71–84
Dong Z, Han M-H, Fedoroff N (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc Natl Acad Sci 105(29):9970–9975 https://doi.org/10.1073/pnas.0803356105
Eysholdt-Derzsó E, Sauter M (2017) Root bending is antagonistically affected by hypoxia and ERF-mediated transcription via auxin signaling. Plant Physiol 175(1):412–423. https://doi.org/10.1104/pp.17.00555
Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037
Fukao T, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM (2019) Submergence and waterlogging stress in plants: a review highlighting research opportunities and understudied aspects. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00340
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 Cell Mol Biol 49(4):683–693. https://doi.org/10.1111/j.1365-313X.2006.02983.x
Gao P et al (2011) osa-MIR393: a salinity- and alkaline stress-related microRNA gene. Mol Biol Rep 38(1):237–242. https://doi.org/10.1007/s11033-010-0100-8
Gao R, Wang Y, Gruber MY, Hannoufa A (2018) miR156/SPL10 modulates lateral root development, branching and leaf morphology in Arabidopsis by silencing AGAMOUS-LIKE 79. Front Pl Sci 8:2226. https://doi.org/10.3389/fpls.2017.02226
Gautam V et al (2017) Role of miRNAs in root development of model plant Arabidopsis thaliana. Indian J Plant Physiol 22(4):382–392. https://doi.org/10.1007/s40502-017-0334-8
Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J Cell Mol Biol 74(5):840–851. https://doi.org/10.1111/tpj.12169
Gutierrez L, Bussell JD, Pacurar DI, 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(10):3119–3132. https://doi.org/10.1105/tpc.108.064758
Han M-H, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci USA 101(4):1093–1098. https://doi.org/10.1073/pnas.0307969100
Hardtke CS (2006) Root development—branching into novel spheres. Curr Opin Plant Biol 9(1):66–71. https://doi.org/10.1016/j.pbi.2005.11.004
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J Cell Mol Biol 61(6):1041–1052. https://doi.org/10.1111/j.1365-313X.2010.04124.x
Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. Annu Rev Plant Biol 53:225–245. https://doi.org/10.1146/annurev.arplant.53.100201.160729
Intergovernmental Panel Climate Change (IPCC) (2007) Climate change 2007: impacts, adaptation and vulnerability: contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. Intergovernmental Panel Climate Change (IPCC)
Josine TJ, Ji J, Wang G, Guan CF (2011) Advances in genetic engineering for plants abiotic stress control. Afr J Biotech 10:5402–5413
Jung JH, Park CM (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225(6):1327–1338. https://doi.org/10.1007/s00425-006-0439-1
Kinoshita N et al (2012) IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. Plant Cell 24(9):3590–3602. https://doi.org/10.1105/tpc.112.097006
Kumar A, Gautam V, Kumar P, Mukherjee S, Verma S, Sarkar AK (2019) Identification and co-evolution pattern of stem cell regulator miR394s and their targets among diverse plant species. BMC Evol Biol 19(1):55. https://doi.org/10.1186/s12862-019-1382-7
Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101(34):12753–12758. https://doi.org/10.1073/pnas.0403115101
Li W-X et al (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20(8):2238–2251. https://doi.org/10.1105/tpc.108.059444
Li S et al (2013) MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153(3):562–574. https://doi.org/10.1016/j.cell.2013.04.005
Licausi F, Perata P (2009) Chap. 4 low oxygen signaling and tolerance in plants. Adv Bot Res 50:139–198. https://doi.org/10.1016/S0065-2296(08)00804-5
Licausi F, Weits DA, Pant BD, Scheible WR, Geigenberger P, van Dongen JT (2011) Hypoxia responsive gene expression is mediated by various subsets of transcription factors and miRNAs that are determined by the actual oxygen availability. New Phytol 190(2):442–456. https://doi.org/10.1111/j.1469-8137.2010.03451.x
Liu J et al (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305(5689):1437–1441. https://doi.org/10.1126/science.1102513
Lin J-S et al (2018) MicroRNA160 modulates plant development and heat shock protein gene expression to mediate heat tolerance in Arabidopsis. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00068
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14(5):836–843. https://doi.org/10.1261/rna.895308
Malamy J (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77. https://doi.org/10.1111/j.1365-3040.2005.01306.x
Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17(5):1360–1375. https://doi.org/10.1105/tpc.105.031716
Marin E et al (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22(4):1104–1117. https://doi.org/10.1105/tpc.109.072553
Martins S et al (2017) Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature. Nat Commun 8(1):309. https://doi.org/10.1038/s41467-017-00355-4
McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411(6838):709–713. https://doi.org/10.1038/35079635
Megha S, Basu U, Kav NNV (2018) Regulation of low temperature stress in plants by microRNAs. Plant Cell Environ 41(1):1–15. https://doi.org/10.1111/pce.12956
Meng Y, Ma X, Chen D, Wu P, Chen M (2010) MicroRNA-mediated signaling involved in plant root development. Biochem Biophys Res Commun 393(3):345–349. https://doi.org/10.1016/j.bbrc.2010.01.129
Mira MM, El-Khateeb EA, Gaafar RM, Igamberdiev AU, Hill RD, Stasolla C (2019) Stem cell fate in hypoxic root apical meristems is influenced by phytoglobin expression. J Exp Bot 71(4):1350–1362. https://doi.org/10.1093/jxb/erz410
Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW (2009) Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61(1):165–177. https://doi.org/10.1093/jxb/erp296
Moldovan D, Spriggs A, Yang J, Pogson BJ, Dennis ES, Wilson IW (2010) Hypoxia-responsive microRNAs and trans-acting small interfering RNAs in Arabidopsis. J Exp Bot 61(1):165–177. https://doi.org/10.1093/jxb/erp296
Moreno AA, Orellana A (2011) The physiological role of the unfolded protein response in plants. Biol Res 44:75–80
Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20(12):1138–1143. https://doi.org/10.1016/j.cub.2010.05.035
Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2(6):a001537. https://doi.org/10.1101/cshperspect.a001537
Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12(17):1484–1495. https://doi.org/10.1016/s0960-9822(02)01017-5
Reichel M, Li Y, Li J, Millar AA (2015) Inhibiting plant microRNA activity: molecular SPONGEs, target MIMICs and STTMs all display variable efficacies against target microRNAs. Plant Biotechnol Jl 13:915–926
Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of Plant MicroRNA Targets. Cell 110:513–520. https://doi.org/10.1016/s0092-8674(02)00863-2
Rodriguez RE et al (2015) MicroRNA miR396 regulates the switch between stem cells and transit-amplifying cells in Arabidopsis roots. Plant Cell 27(12):3354–3366. https://doi.org/10.1105/tpc.15.00452
Sarkar AK et al (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446(7137):811–814. https://doi.org/10.1038/nature05703
Sarkar AK, Mayandi K, Gautam V, Barik S, Sarkar Das S (2013) Improving the plant root system architecture to combat abiotic stresses incurred as a result of global climate changes climate change and plant abiotic stress tolerance. Wiley-VCH Verlag GmbH & Co. KGaA, New York, pp 305–324
Scheres B, Benfey P, Dolan L (2002) Root development. Arabidopsis Book 1:e0101–e0101. https://doi.org/10.1199/tab.0101
Shaw B (2018) Salt stress tolerance in plants: the role of miRNAs. Adv Plants Agric Res. https://doi.org/10.15406/apar.2018.08.00360
Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21(12):3823–3838. https://doi.org/10.1105/tpc.109.069906
Singh A et al (2017) Phytohormonal crosstalk modulates the expression of miR166/165 s, target Class III HD-ZIPs, and KANADI genes during root growth in Arabidopsis thaliana. Sci Rep 7(1):3408. https://doi.org/10.1038/s41598-017-03632-w
Singh A et al (2018) Plant small RNAs: advancement in the understanding of biogenesis and role in plant development. Planta 248(3):545–558. https://doi.org/10.1007/s00425-018-2927-5
Singh S et al (2020a) Role of chromatin modification and remodeling in stem cell regulation and meristem maintenance in Arabidopsis. J Exp Bot 71(3):778–792. https://doi.org/10.1093/jxb/erz459
Singh S et al (2020b) Auxin signaling modulates LATERAL ROOT PRIMORDIUM1 (LRP1) expression during lateral root development in Arabidopsis. Plant J Cell Mol Biol 101(1):87–100. https://doi.org/10.1111/tpj.14520
Singh A, Singh S, Panigrahi KCS, Reski R, Sarkar AK (2014) 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 33(6):945–953. https://doi.org/10.1007/s00299-014-1573-z
Song JJ, Smith SK, Hannon GJ, Joshua-Tor L (2004) Crystal structure of argonaute and its implications for RISC slicer activity. Science 305(5689):1434–1437. https://doi.org/10.1126/science.1102514
Sorin C et al (2014) A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol 202(4):1197–1211. https://doi.org/10.1111/nph.12735
Spollen WG, Sharp RE (1991) Spatial distribution of turgor and root growth at low water potentials. Plant Physiol 96(2):438–443. https://doi.org/10.1104/pp.96.2.438
Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Bäurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26(4):1792–1807. https://doi.org/10.1105/tpc.114.123851
Sun F et al (2008) Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol 146(1):178–188. https://doi.org/10.1104/pp.107.109413
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(8):2051–2065. https://doi.org/10.1105/tpc.106.041673
Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17(4):196–203. https://doi.org/10.1016/j.tplants.2012.01.010
Sunkar R, Zhu J-K (2004) Novel and stress-regulated MicroRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019. https://doi.org/10.1105/tpc.104.022830
Takahashi N, Yamazaki Y, Kobayashi A, Higashitani A, Takahashi H (2003) Hydrotropism interacts with gravitropism by degrading amyloplasts in seedling roots of Arabidopsis and radish. Plant Physiol 132(2):805–810. https://doi.org/10.1104/pp.018853
Tang G, Yan J, Gu Y, Qiao M, Fan R, Mao Y, Tang X (2012) Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods 58:118–125
Vazquez F, Gasciolli V, Crété P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14(4):346–351. https://doi.org/10.1016/j.cub.2004.01.035
Wang CY et al (2014) MiR397b regulates both lignin content and seed number in Arabidopsis via modulating a laccase involved in lignin biosynthesis. Plant Biotechnol J 12(8):1132–1142. https://doi.org/10.1111/pbi.12222
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(8):2204–2216. https://doi.org/10.1105/tpc.105.033076
Wang R, Zhang Y, Kieffer M, Yu H, Kepinski S, Estelle M (2016) HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat Commun 7:10269. https://doi.org/10.1038/ncomms10269
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95(5):707–735. https://doi.org/10.1093/aob/mci083
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(4):750–759. https://doi.org/10.1016/j.cell.2009.06.031
Xie Z, Allen E, Wilken A, Carrington JC (2005) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102(36):12984–12989. https://doi.org/10.1073/pnas.0506426102
Yadav S, Sarkar Das S, Kumar P, Mishra V, Sarkar AK (2020) Chapter 3—tweaking microRNA-mediated gene regulation for crop improvement. In: Tuteja NR, Passricha N, Saifi SK (eds) Advancement in crop improvement techniques. Woodhead Publishing, Cambridge, pp 45–66
Yan J et al (2016) The miR165/166 mediated regulatory module plays critical roles in ABA homeostasis and response in Arabidopsis thaliana. PLoS Genet 12(11):e1006416–e1006416. https://doi.org/10.1371/journal.pgen.1006416
Yoon EK, Yang JH, Lim J, Kim SH, Kim S-K, Lee WS (2009) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucl Acids Res 38(4):1382–1391. https://doi.org/10.1093/nar/gkp1128
Yu N, Niu QW, Ng KH, Chua NH (2015) The role of miR156/SPLs modules in Arabidopsis lateral root development. Plant J Cell Mol Biol 83(4):673–685. https://doi.org/10.1111/tpj.12919
Acknowledgements
ArS thanks Department of Science and Technology-Science and Engineering Research Board (DST-SERB) for National-Postdoctoral Fellowship (N-PDF) (PDF/2017/000814), National Institute for Plant Biotechnology (NIPB) and National Institute of Plant Genome Research (NIPGR) for funding and support. SY, NG, and VM acknowledge NIPGR, University Grants Commission (UGC), Department of Biotechnology (DBT), New Delhi, India respectively, for fellowship. VR thanks NIPB for internal fundings and research facilities. AKS thanks NIPGR for internal funding and research facilities.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Singh, A., Gandhi, N., Mishra, V. et al. Role of abiotic stress responsive miRNAs in Arabidopsis root development. J. Plant Biochem. Biotechnol. 29, 733–742 (2020). https://doi.org/10.1007/s13562-020-00626-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13562-020-00626-0