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Simplifying the root dynamics: from complex hormone–environment interactions to specific root architectural modulation

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Abstract

The recent unveiling of the intriguing interactions among phytohormones and environmental cues in regulating root architecture for optimum plant acclimation has opened new avenues for research. Additional functions of transcriptional as well as protein-level regulators are being identified, uncovering novel interactions between hormonal and environmental signaling pathways, for shaping the root system architecture (RSA). Owing to the importance of root architectural dynamics under constantly encountered external factors, it is crucial to have a regular and comprehensive update of these interactions, affecting RSA, in order to improve crop performance. Moreover, it is equally important to identify and highlight, in crop species, the crucial regulators, which actively mediate hormonal as well as hormone–environment interactions, but have so far been characterized only in model plants such as Arabidopsis. Such updates will open up new research possibilities for plant biologists in extending the present knowledge on root system plasticity from Arabidopsis to economically important crop plants. Here, we provide a consolidated review of the recent findings on novel inter-hormonal and hormone–environment interactions with special emphasis on key downstream regulators and signaling pathways. We conclude by dissecting the gaps and challenges encountered at present, with an outline for future perspectives to channel the enormous information on hormone–environment regulation of RSA, towards a common output in the form of specific modulation of RSA components.

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References

  • Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S, Tsuchiya YN et al (2014) CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci USA 111:2029–2034

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Band LR, Wells DM, Larrieu A, Sun J, Middleton AM, French AP et al (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc Natl Acad Sci USA 109:4668–4673

    Article  PubMed  PubMed Central  Google Scholar 

  • Bao Y, Aggarwal P, Robbins NE, Sturrock CJ, Thompson MC, Tan HQ et al (2014) Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc Natl Acad Sci USA 111:9319–9324

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bunce JA (2014) Corn growth responses to elevated CO2 varies with the amount of nitrogen applied. Am J Plant Sci 5:306 – 12

    Article  CAS  Google Scholar 

  • Caffaro MM, Vivanco JM, Boem FHG, Rubio G (2011) The effect of root exudates on root architecture in Arabidopsis thaliana. Plant Growth Regul 64:241–249

    Article  CAS  Google Scholar 

  • Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T et al (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis. Plant Physiol 154:810–819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L et al (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng X, Ruyter-Spira C, Boumeester H (2013) The interaction between strigolactones and other plant hormones in the regulation of plant development. Front Plant Sci 4:199

    Article  PubMed  PubMed Central  Google Scholar 

  • Czyzewicz N, De Smet I (2016) The Arabidopsis thaliana CAVATA3/EMBRYO SURROUNDING REGION 26 (CLE 26) peptide is able to alter root architecture of Solanum lycopersicum and Brassica napus. Plant Signal Behav 11:e1118598

    Article  PubMed  CAS  Google Scholar 

  • Datta S, Kim CM, Pernas M, Pires ND, Proust H, Tam T et al (2011) Root hairs: development, growth and evolution at the plant-soil interface. Plant Soil 346:1–14

    Article  CAS  Google Scholar 

  • De Smet I, Signora L, Beeckman T, Inzé D, Foyer CH, Zhang H (2003) An abscisic acid checkpoint in lateral root development of Arabidopsis. Plant J 33:543–555

    Article  PubMed  Google Scholar 

  • De Smet I, Zhang H, Inźe D, Beeckman T (2006) A novel role for abscisic acid emerges from underground. Trends Plant Sci 11:434–439

    Article  PubMed  CAS  Google Scholar 

  • Dello Ioio R, Nakamura K, Moubayidin L, Perillim S, Taniguchi M, Morita MT et al (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    Article  PubMed  CAS  Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:365–373

    Article  CAS  Google Scholar 

  • Fridman Y, Elkouby L, Holland N, Vragovié K, Elbaum R (2014) Root growth is modulated by differential hormonal sensitivity in neighboring cells. Gene Dev 28:912–920

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gago J, Martínez-Núñez L, Landín M, Gallego PP (2010a) Artificial neural networks as an alternative to the traditional statistical methodology in plant research. J Plant Physiol 167:23–27

    Article  PubMed  CAS  Google Scholar 

  • Gago J, Landín M, Gallego PP (2010b) Strengths of artificial neuronal networks in modeling complex plant processes. Plant Signal Behav 5:743–745

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallego PP, Gago J, Landín M (2011). Artificial neural networks technology to model and predict plant biology process. In: Suzuki K (ed) Artificial neural networks—methodological advances and biomedical applications. Intech, Rijeka. ISBN: 978-953-307-243-2

    Google Scholar 

  • Geng Y, Wu R, Wee CW, Xie F, Wei X, Chan PMY, Tham C, Duan L, Dinneny JR (2013) A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25:2132–2154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giehl RFH, Gruber BD, Wirén NV (2014) Its time to make changes: modulation of root system architecture by nutrient signals. J Exp Bot 65:769–778

    Article  PubMed  CAS  Google Scholar 

  • Guan P, Wang R, Nacry P, Breton G, Kay SA, Pruneda-Paz JL et al (2014) Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proc Natl Acad Sci USA 111:15267–15272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo FQ, Wang R, Crawford NM (2002) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is regulated by auxin in both shoots and roots. J Exp Bot 53:835–844

    Article  PubMed  CAS  Google Scholar 

  • Guo D, Liang J, Li L (2009) Abscisic acid (ABA) inhibition of lateral root formation involves endogenous ABA biosynthesis in Arachis hypogaea L. Plant Growth Regul 58:173–179

    Article  CAS  Google Scholar 

  • Guo Q, Love J, Roche J, Song J, Turnbull MH, Jameson PE (2017) A RootNav analysis of morphological changes in Brassica napus L. roots in response to different nitrogen forms. Plant Growth Regul 83:83–92

    Article  CAS  Google Scholar 

  • Hachiya T, Sugiura D, Kojima M, Sato S, Yanagisawa S, Sakakibara H et al (2014) High CO2 triggers preferential root growth of Arabidopsis thaliana via two distinct systems under low pH and low N stresses. Plant Cell Physiol 55:269–280

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayashi K (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53:965–975

    Article  PubMed  CAS  Google Scholar 

  • Javaux M, Schröder T, Vanderborght J, Vereecken H (2008) Use of a three-dimensional detailed modeling approach for predicting root water uptake. Vadose Zone J 7:1079–1088

    Article  Google Scholar 

  • Ji H, Liu L, Li K, Xie Q, Wang Z, Zhao X et al (2014) PEG-mediated osmotic stress induces premature differentiation of the root apical meristem and outgrowth of lateral roots in wheat. J Exp Bot 65:4863–4872

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ji H, Wang S, Li K, Szakonyi D, Koncz C, Li X (2015) PRL1 modulates root stem cell niche activity and meristem size through WOX5 and PLTs in Arabidopsis. Plant J 81:399–412

    Article  PubMed  CAS  Google Scholar 

  • Jiang L, Matthys C, Marquez-Garcia L, De Cuyper C, Smet L, De Keyser A et al (2016) Strigolactones spatially influence lateral root development through the cytokinin signaling network. J Exp Bot 67:379–389

    Article  PubMed  CAS  Google Scholar 

  • Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM et al (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11:78–84

    Article  PubMed  CAS  Google Scholar 

  • Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31

    Article  PubMed  CAS  Google Scholar 

  • Lavenus J, Guyomarch S, Laplaze L (2016) PIN transcriptional regulation shapes root system architecture. Trends Plant Sci 21:175–177

    Article  PubMed  CAS  Google Scholar 

  • Lewis DR, Negi S, Sukumar P, Muday GK (2011) Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138:3485–3495

    Article  PubMed  CAS  Google Scholar 

  • Li X, Cai W, Liu Y, Li H, Fu L, Liu Z, Xu L, Liu H, Xu T, Xiong Y (2017) Differential TOR activation and cell proliferation in Arabidopsis root and shoot apexes. Proc Natl Acad Sci USA 114:2765–2770

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu JL, Mehdi S, Topping J, Friml J, Lindsey K (2013) Interaction of PLS and PIN and hormonal crosstalk in Arabidopsis root development. Front Plant Sci 4:75

    PubMed  PubMed Central  Google Scholar 

  • Liu J, Rowe J, Lindsey K (2014) Hormonal crosstalk for root development: a combined experimental and modeling perspective. Front Plant Sci 5:116

    PubMed  PubMed Central  Google Scholar 

  • Liu F, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 168:343–356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Y, Wang R, Zhang P, Chen Q, Luo Q, Zhu Y, Xu J (2016) The nitrification inhibitor methyl 3-(4-hydroxyphenyl) propionate modulates root development by interfering with auxin signaling via the NO/ROS Pathway. Plant Physiol 171:1686–1703

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lupini A, Araniti F, Sunseri F, Abenavoli MR (2014) Coumarin interacts with auxin polar transport to modify root system architecture in Arabidopsis thaliana. Plant Growth Regul 74:23–31

    Article  CAS  Google Scholar 

  • Marhavy P, Duclercq J, Weller B, Feraru E, Bielach A, Offringa R et al (2014) Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr Biol 24:1031–1037

    Article  PubMed  CAS  Google Scholar 

  • Marquez-Garcia B, Njo M, Beeckman T, Goormachtig S, Foyer CH (2014) A new role for glutathione in the regulation of root architecture linked to strigolactones. Plant Cell Environ 37:488–498

    Article  PubMed  CAS  Google Scholar 

  • Miguel A. Moreno-Risueno JM, Van Norman A, Moreno J, Zhang SE, Ahnert, Philip N, Benfey (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329(5997):1306–1311

    Article  CAS  Google Scholar 

  • Mishra BS, Singh M, Aggrawal P, Laxmi A (2009). Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS ONE 4:e4502

    Article  PubMed  PubMed Central  Google Scholar 

  • Monzón GC, Pinedo M, Lamattina L, de la Canal L (2012) Sunflower root growth regulation: the role of jasmonic acid and its relation with auxins. Plant Growth Regul 66:129–136

    Article  CAS  Google Scholar 

  • Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720

    Article  PubMed  CAS  Google Scholar 

  • Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195

    Article  PubMed  CAS  Google Scholar 

  • Nizampatnam NR, Schreier SJ, Domodaran S, Adhikari S, Subramnian S (2015) microRNA160 dictates stage-specific auxin and cytokinin sensitivities and directs soybean nodule development. Plant J 84:140–153

    Article  PubMed  CAS  Google Scholar 

  • Orman-Ligeza B, Civava R, de Dorlodot S, Draye X (2014) Root system architecture. In: Morte A, Varma A (eds) Root engineering, vol 40 of the series soil biology. Springer, New York, pp 39–56

    Google Scholar 

  • Paez-Garcia A, Motes CM, Scheible WR, Chen R, Blancaflor EB, Monteros MJ (2015) Root traits and phenotyping strategies for plant improvement. Plants 4:334–355

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandey A, Sharma M, Pandey GK (2016) Emerging roles of strigolactones in plant responses to stress and development. Front Plant Sci 7:434

    PubMed  PubMed Central  Google Scholar 

  • Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source ⁄sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol J 9:747–758

    Article  PubMed  CAS  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395 – 401

    Article  PubMed  CAS  Google Scholar 

  • Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290–294

    Article  PubMed  CAS  Google Scholar 

  • Reddy AR, Rasineni GK, Raghavendra AS (2010) The impact of global elevated CO2 concentration on photosynthesis and plant productivity. Current Sci 99:46–57

    CAS  Google Scholar 

  • Risk JM, Macknight RC, Day CL (2008) FCA does not bind abscisic acid. Nature 456:E5–E6

    Article  PubMed  CAS  Google Scholar 

  • Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M (2014) Shoot-derived cytokinins systemically regulate root nodulation. Nat Commun 5:4983

    Article  PubMed  CAS  Google Scholar 

  • Sengupta D, Kannan M, Reddy AR (2011) A root proteomics-based insight reveals dynamic regulation of root proteins under progressive drought stress and recovery in Vigna radiata (L.) Wilczek. Planta 233:1111–1127

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Park CM (2009) Auxin homeostasis during lateral root development under drought condition. Plant Signal Behav 4:1002–1004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shani E, Weinstain R, Zhang Y, Castillego C, Kaiserli E, Chory J et al (2013). Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc Natl Acad Sci USA 110:4834–4839

    Article  PubMed  PubMed Central  Google Scholar 

  • Shao A, Ma W, Zhao X, Mengyun H, He X, Teng W, Li H, Tong Y (2017) The auxin biosynthetic tryptophan aminotransferase related TaTAR2.1-3A increases grain yield of wheat. Plant Physiol 174:2274–2288

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sreeharsha RV, Sekhar KM, Reddy AR (2015) Delayed flowering is associated with lack of photosynthetic acclimation in pigeon pea (Cajanus cajan L.) grown under elevated CO2. Plant Sci 231:82–93

    Article  PubMed  CAS  Google Scholar 

  • Street IH, Aman S, Zubo Y, Ramzan A, Wang X, Shakeel SN et al (2015) Ethylene inhibits cell proliferation of the arabidopsis root meristem. Plant Physiol 169:338–350

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Su YH, Liu YB, Zhang XS (2011) Auxin-cytokinin interaction regulates meristem development. Mol Plant 4:616–625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun H, Tao J, Liu S, Huang S, Chen S, Xie X et al (2014) Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J Exp Bot 65:6735–6746

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N et al (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Gen 45:1097–1102

    Article  CAS  Google Scholar 

  • Valenzuela CE, Acevodo-Acevodo O, Miranda GS, Vergara-Barros P, Holuigue L, Figueroa CR et al (2016) Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root. J Exp Bot 67:4209–4220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vidal EA, Moyano TC, Riveras E, Contreras-López O, Gutiérrez RA (2013) Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. Proc Natl Acad Sci USA 110:12840–12845

    Article  PubMed  PubMed Central  Google Scholar 

  • Villordon AQ, Ginzberg I, Firon N (2014) Root architecture and root and tuber crop productivity. Trends Plant Sci 19:419–425

    Article  PubMed  CAS  Google Scholar 

  • Visentin I, Vitali M, Ferrero M, Zhang Y, Ruyter-Spira C, Novák O et al (2016) Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytol 212:954–963

    Article  PubMed  CAS  Google Scholar 

  • Wang YN, Zhang WS, Li KX, Sun FF, Han CK, Wang Y, Li X (2008) Salt-induced plasticity of root hair development is caused by ion disequilibrium in Arabidopsis thaliana. J Plant Res 121:87–96

    Article  PubMed  Google Scholar 

  • Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Li K, Chen L, Zou Y, Liu H, Tian Y et al (2015) MicroRNA167-directed regulation of the auxin response factors GmARF8a and GmARF8b Is required for soybean nodulation and lateral root development. Plant Physiol 168:101–116

    CAS  Google Scholar 

  • Wang J, Zhang Y, Jin J, Li Q, Zhao C, Nan W, Wang X, Ma R, Bi Y (2017) An intact cytokinin-signaling pathway is required for Bacillus sp.LZR216-promoted plant growth and root system architecture alteration in Arabidopsis thaliana seedlings. Plant Growth Regul. https://doi.org/10.1007/s10725-017-0357-1

    Article  Google Scholar 

  • Wu T, Zhang HT, Wang Y, Jia WS, Xu XF, Zhang XZ, Han ZH (2012) Induction of root Fe(lll) reductase activity and proton extrusion by iron deficiency is mediated by auxin-based systemic signalling in Malus xiaojinensis. J Exp Bot 63:859–870

    Article  PubMed  CAS  Google Scholar 

  • Xiong Y, Sheen J (2014) The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol 164:499–512

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J (2013) Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496:181–186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yong JWH, Wong YSC, Farquhar GD (2000) Effects of elevated CO2 and nitrogen nutrition on cytokinins in the xylem sap and leaves of cotton. Plant Physiol 124:767–779

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Huang L, Yan A, Liu Y, Liu B, Yu C et al (2016) Multiple phytohormones promote root hair elongation by regulating a similar set of genes in the root epidermis in Arabidopsis. J Exp Bot 67:6363–6372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao Y, Wang T, Zhang W, Li X (2011) SOS3 mediates lateral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. New Phytol 189:1122–1134

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Pan X, Deng Y, Wu H, Liu P, Li X (2016) AtOPR3 specifically inhibits primary root growth in Arabidopsis under phosphate deficiency. Sci Rep 6:24778

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu L, Zheng C, Liu R, Song A, Zhang Z, Xin J et al (2016) Chrysanthemum transcription factor CmLBD1 direct lateral root formation in Arabidopsis thaliana. Sci Rep 6:20009. https://doi.org/10.1038/srep20009

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zolla G, Heimer YM, Barak S (2010) Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J Exp Bot 61:211–224

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

Present work is supported by the Science and Engineering Research Board (Department of Science and Technology) Young Scientist Start Up Grant (YSS/2015/000635) to DS.

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Sengupta, D., Reddy, A.R. Simplifying the root dynamics: from complex hormone–environment interactions to specific root architectural modulation. Plant Growth Regul 85, 337–349 (2018). https://doi.org/10.1007/s10725-018-0397-1

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