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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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
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
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
Bunce JA (2014) Corn growth responses to elevated CO2 varies with the amount of nitrogen applied. Am J Plant Sci 5:306 – 12
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
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
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
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
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
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
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
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
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
Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:365–373
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
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
Gago J, Landín M, Gallego PP (2010b) Strengths of artificial neuronal networks in modeling complex plant processes. Plant Signal Behav 5:743–745
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
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
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
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
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
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
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
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
Hayashi K (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53:965–975
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
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
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
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
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
Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31
Lavenus J, Guyomarch S, Laplaze L (2016) PIN transcriptional regulation shapes root system architecture. Trends Plant Sci 21:175–177
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
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
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
Liu J, Rowe J, Lindsey K (2014) Hormonal crosstalk for root development: a combined experimental and modeling perspective. Front Plant Sci 5:116
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
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
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
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
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
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
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
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
Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720
Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195
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
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
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
Pandey A, Sharma M, Pandey GK (2016) Emerging roles of strigolactones in plant responses to stress and development. Front Plant Sci 7:434
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
Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395 – 401
Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290–294
Reddy AR, Rasineni GK, Raghavendra AS (2010) The impact of global elevated CO2 concentration on photosynthesis and plant productivity. Current Sci 99:46–57
Risk JM, Macknight RC, Day CL (2008) FCA does not bind abscisic acid. Nature 456:E5–E6
Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M (2014) Shoot-derived cytokinins systemically regulate root nodulation. Nat Commun 5:4983
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
Seo PJ, Park CM (2009) Auxin homeostasis during lateral root development under drought condition. Plant Signal Behav 4:1002–1004
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
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
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
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
Su YH, Liu YB, Zhang XS (2011) Auxin-cytokinin interaction regulates meristem development. Mol Plant 4:616–625
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
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
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
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
Villordon AQ, Ginzberg I, Firon N (2014) Root architecture and root and tuber crop productivity. Trends Plant Sci 19:419–425
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
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
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
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
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
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
Xiong Y, Sheen J (2014) The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol 164:499–512
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
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
Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279:407–409
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
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
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
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
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
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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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DOI: https://doi.org/10.1007/s10725-018-0397-1