Roots are sensors evolved to simultaneously respond to manifold signals, which allow the plant to survive. Root growth responses, including the modulation of directional root growth, were shown to be differently regulated when the root is exposed to a combination of exogenous stimuli compared to an individual stress trigger. Several studies pointed especially to the impact of the negative phototropic response of roots, which interferes with the adaptation of directional root growth upon additional gravitropic, halotropic or mechanical triggers. This review will provide a general overview of known cellular, molecular and signalling mechanisms involved in directional root growth regulation upon exogenous stimuli. Furthermore, we summarise recent experimental approaches to dissect which root growth responses are regulated upon which individual trigger. Finally, we provide a general overview of how to implement the knowledge gained to improve plant breeding.

Department of Functional and Evolutionary Ecology Faculty of Life Sciences Molecular Systems Biology University of Vienna Wien Austria

Laboratory of Hormonal Regulations in Plants Institute of Experimental Botany Czech Academy of Sciences Prague Czechia

Vienna Metabolomics Center University of Vienna Wien Austria

Zobrazit více v PubMed

Abas L., Benjamins R., Malenica N., Paciorek T., Wiśniewska J., Moulinier-Anzola J. C., et al. . (2006). Intracellular trafficking and proteolysis of the arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8 (3), 249–256. doi: 10.1038/ncb1369 PubMed DOI

Aronne G., Muthert L. W. F., Izzo L. G., Romano L. E., Iovane M., Capozzi F., et al. . (2022). Novel device to study altered gravity and light interactions in seedling tropisms. Life Sci. Sp Res. 32, 8–16. doi: 10.1016/j.lssr.2021.09.005 PubMed DOI

Atkinson J. A., Pound M. P., Bennett M. J., Wells D. M. (2019). Uncovering the hidden half of plants using new advances in root phenotyping. Curr. Opin. Biotechnol. 55, 1–8. doi: 10.1016/j.copbio.2018.06.002 PubMed DOI PMC

Baena-González E., Hanson J. (2017). Shaping plant development through the SnRK1–TOR metabolic regulators. Curr. Opin. Plant Biol. 35, 152–157. doi: 10.1016/j.pbi.2016.12.004 PubMed DOI

Baena-González E., Rolland F., Thevelein J. M., Sheen J. A. (2007). Central integrator of transcription networks in plant stress and energy signalling. Nature 448 (7156), 938–942. doi: 10.1038/nature06069 PubMed DOI

Barbez E., Dünser K., Gaidora A., Lendl T., Busch W. (2017). Auxin steers root cell expansion via apoplastic PH regulation in arabidopsis thaliana. Proc. Natl. Acad. Sci. U S A. 114 (24), E4884–E4893. doi: 10.1073/pnas.1613499114 PubMed DOI PMC

Barrada A., Montané M. H., Robaglia C., Menand B. (2015). Spatial regulation of root growth: Placing the plant TOR pathway in a developmental perspective. Int. J. Mol. Sci. 16 (8), 19671–19697. doi: 10.3390/ijms160819671 PubMed DOI PMC

Batoko H., Dagdas Y., Baluska F., Sirko A. (2017). Understanding and exploiting autophagy signaling in plants. Essays Biochem. 61 (6), 675–685. doi: 10.1042/EBC20170034 PubMed DOI PMC

Belda-Palazón B., Adamo M., Valerio C., Ferreira L. J., Confraria A., Reis-Barata D., et al. . (2020). Dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nat. Plants 6 (11), 1345–1353. doi: 10.1038/s41477-020-00778-w PubMed DOI

Belda-Palazón B., Costa M., Beeckman T., Rolland F., Baena-González E. (2022). ABA represses TOR and root meristem activity through nuclear exit of the SnRK1 kinase. Proc. Natl. Acad. Sci. U S A 119 (28), e2204862119. doi: 10.1073/pnas.2204862119 PubMed DOI PMC

Broeckx T., Hulsmans S., Rolland F. (2016). The plant energy sensor: Evolutionary conservation and divergence of SnRK1 structure, regulation, and function. J. Exp. botany. 67 (22), 6215–6252. doi: 10.1093/jxb/erw416 PubMed DOI

Cabrera J., Conesa C. M., Del Pozo J. C. (2022). May the dark be with roots: A perspective on how root illumination may bias in vitro research on plant-environment interactions. New Phytol. 233 (5), 1988–1997. doi: 10.1111/nph.17936 PubMed DOI

Calleja-Cabrera J., Boter M., Oñate-Sánchez L., Pernas M. (2020). Root growth adaptation to climate change in crops. Front. Plant Science. 11, 544. doi: 10.3389/fpls.2020.00544 PubMed DOI PMC

Cardarelli M., Rouphael Y., Kyriacou M. C., Colla G., Pane C. (2020). Augmenting the sustainability of vegetable cropping systems by configuring rootstock-dependent rhizomicrobiomes that support plant protection. Agronomy 10 (8). doi: 10.3390/agronomy10081185 DOI

Cassab G. I., Eapen D., Campos M. E. (2013). Root hydrotropism: An update. Am. J. Bot. 100 1, 14–24. doi: 10.3732/ajb.1200306 PubMed DOI

Chen Q., Hu T., Li X., Song C.-P., Zhu J.-K., Chen L., et al. . (2022). Phosphorylation of SWEET sucrose transporters regulates plant Root:Shoot ratio under drought. Nat. Plants 8 (1), 68–77. doi: 10.1038/s41477-021-01040-7 PubMed DOI

Chen Y., Weckwerth W. (2020). Mass spectrometry untangles plant membrane protein signaling networks. Trends Plant Sci. 25 (9), 930–944. doi: 10.1016/j.tplants.2020.03.013 PubMed DOI

Chin S., Blancaflor E. B. (2022). Plant gravitropism: From mechanistic insights into plant function on earth to plants colonizing other worlds. Methods Mol. Biol. 2368, 1–41. doi: 10.1007/978-1-0716-1677-2_1 PubMed DOI

Clark N. M., Nolan T. M., Wang P., Song G., Montes C., Valentine C. T., et al. . (2021). Integrated omics networks reveal the temporal signaling events of brassinosteroid response in arabidopsis. Nat. Commun. 12 (1), 5858. doi: 10.1038/s41467-021-26165-3 PubMed DOI PMC

Cole R. A., Fowler J. E. (2006). Polarized growth: Maintaining focus on the tip. Curr. Opin. Plant Biol. 9 (6), 579–588. doi: 10.1016/j.pbi.2006.09.014 PubMed DOI

Crepin N., Rolland F. (2019). SnRK1 activation, signaling, and networking for energy homeostasis. Curr. Opin. Plant Biol. 51, 29–36. doi: 10.1016/j.pbi.2019.03.006 PubMed DOI

D E Lima C. F. F., Kleine-Vehn J., De Smet I., Feraru E. (2021). Getting to the root of belowground high temperature responses in plants. J. Exp. Bot. doi: 10.1093/jxb/erab202 PubMed DOI

De Pessemier J., Chardon F., Juraniec M., Delaplace P., Hermans C. (2013). Natural variation of the root morphological response to nitrate supply in arabidopsis thaliana. Mech. Dev. 130 (1), 45–53. doi: 10.1016/j.mod.2012.05.010 PubMed DOI

Dietrich D., Pang L., Kobayashi A., Fozard J. A., Boudolf V., Bhosale R., et al. . (2017). Root hydrotropism is controlled via a cortex-specific growth mechanism. Nat. Plants 3, 17057. doi: 10.1038/nplants.2017.57 PubMed DOI

Dong Y., Aref R., Forieri I., Schiel D., Leemhuis W., Meyer C., et al. . (2022). The plant TOR kinase tunes autophagy and meristem activity for nutrient stress-induced developmental plasticity. Plant Cell 34 (10), 3814–3829. doi: 10.1093/plcell/koac201 PubMed DOI PMC

Dong Y., Silbermann M., Speiser A., Forieri I., Linster E., Poschet G., et al. . (2017). Sulfur availability regulates plant growth via glucose-TOR signaling. Nat. Commun. 8 (1), 1174. doi: 10.1038/s41467-017-01224-w PubMed DOI PMC

Doussan C. (2022). Putting plant roots at light: Temporal imaging of plant roots and soil water with a light transmission technique for linking water and root observations to soil-plant models. Methods Mol. Biol. 2395, 227–246. doi: 10.1007/978-1-0716-1816-5_11 PubMed DOI

Downie H., Holden N., Otten W., Spiers A. J., Valentine T. A., Dupuy L. X. (2012). Transparent soil for imaging the rhizosphere. PloS One 7 (9), 1–6. doi: 10.1371/journal.pone.0044276 PubMed DOI PMC

Dubey S. M., Serre N. B. C., Oulehlová D., Vittal P., Fendrych M. (2021). No time for transcription-rapid auxin responses in plants. Cold Spring Harb Perspect. Biol. 13 (8), a039891. doi: 10.1101/cshperspect.a039891 PubMed DOI PMC

Dyachok J., Zhu L., Liao F., He J., Huq E., Blancaflor E. B. (2011). SCAR mediates light-induced root elongation in arabidopsis through photoreceptors and proteasomes. Plant Cell 23 (10), 3610–3626. doi: 10.1105/tpc.111.088823 PubMed DOI PMC

Fendrych M., Akhmanova M., Merrin J., Glanc M., Hagihara S., Takahashi K., et al. . (2018). Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants. 4 (7), 453–459. doi: 10.1038/s41477-018-0190-1 PubMed DOI PMC

Fichtner F., Dissanayake I. M., Lacombe B., Barbier F. (2020). Sugar and nitrate sensing: A multi-Billion-Year story. Trends Plant Science. 26 (4), 352–374. doi: 10.1016/j.tplants.2020.11.006 PubMed DOI

Freschet G. T., Pagès L., Iversen C. M., Comas L. H., Rewald B., Roumet C., et al. . (2021). Starting guide to root ecology: Strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements. New Phytol. 232 (3), 973–1122. doi: 10.1111/nph.17572 PubMed DOI PMC

Friml J., Wiŝniewska J., Benková E., Mendgen K., Palme K. (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in arabidopsis. Nature. 415 (6873), 806–809. doi: 10.1038/415806a PubMed DOI

Fürtauer L., Weiszmann J., Weckwerth W., Nägele T. (2019). Dynamics of plant metabolism during cold acclimation. Int. J. Mol. Sci. 20 (21), 5411. doi: 10.3390/ijms20215411 PubMed DOI PMC

García-González J., Lacek J., Retzer K. (2021. a). Dissecting hierarchies between light, sugar and auxin action underpinning root and root hair growth. Plants. 10 (1), 111. doi: 10.3390/plants10010111 PubMed DOI PMC

García-González J., Lacek J., Weckwerth W., Retzer K. (2021. b). Exogenous carbon source supplementation counteracts root and hypocotyl growth limitations under increased cotyledon shading, with glucose and sucrose differentially modulating growth curves. Plant Signal. Behav. 16 (11), 1969818. doi: 10.1080/15592324.2021.1969818 PubMed DOI PMC

García-González J., Lacek J., Weckwerth W., Retzer K. (2022). Throttling growth speed: Evaluation of Aux1-7 root growth profile by combining d-root system and root penetration assay. Plants 11 (5), 650. doi: 10.3390/plants11050650 PubMed DOI PMC

García-González J., van Gelderen K. (2021). Bundling up the role of the actin cytoskeleton in primary root growth. Front. Plant Sci. 12, 777119. doi: 10.3389/fpls.2021.777119 PubMed DOI PMC

Ghatak A., Chaturvedi P., Bachmann G., Valledor L., Ramšak Ž., Bazargani M. M., et al. . (2020). Physiological and proteomic signatures reveal mechanisms of superior drought resilience in pearl millet compared to wheat. Front. Plant Sci. 11. doi: 10.3389/fpls.2020.600278 PubMed DOI PMC

Ghatak A., Chaturvedi P., Nagler M., Roustan V., Lyon D., Bachmann G., et al. . (2016). Comprehensive tissue-specific proteome analysis of drought stress responses in pennisetum glaucum (L.) r. br. (Pearl millet). J. Proteomics 143, 122–135. doi: 10.1016/j.jprot.2016.02.032 PubMed DOI

Ghatak A., Chaturvedi P., Waldherr S., Subbarao G. V., Weckwerth W. (2022. a). PANOMICS at the interface of root-soil microbiome and BNI. Trends Plant Sci. 28 (1), 106–122. doi: 10.1016/j.tplants.2022.08.016 PubMed DOI

Ghatak A., Chaturvedi P., Weckwerth W. (2017). Cereal crop proteomics: Systemic analysis of crop drought stress responses towards marker-assisted selection breeding. Front. Plant Sci. 8. doi: 10.3389/fpls.2017.00757 PubMed DOI PMC

Ghatak A., Schindler F., Bachmann G., Engelmeier D., Bajaj P., Brenner M., et al. . (2021). Root exudation of contrasting drought-stressed pearl millet genotypes conveys varying biological nitrification inhibition (BNI) activity. Biol. Fertil Soils. 58 (3), 291–306. doi: 10.1007/s00374-021-01578-w PubMed DOI PMC

Ghatak A., Schindler F., Bachmann G., Engelmeier D., Bajaj P., Brenner M., et al. . (2022. b). Root exudation of contrasting drought-stressed pearl millet genotypes conveys varying biological nitrification inhibition (BNI) activity. Biol. Fertil soils 58 (3), 291–306. doi: 10.1007/s00374-021-01578-w PubMed DOI PMC

González-García M. P., Conesa C. M., Lozano-Enguita A., Baca-González V., Simancas B., Navarro-Neila S., et al. . (2022). Temperature changes in the root ecosystem affect plant functionality. Plant Commun. 100514. doi: 10.1016/j.xplc.2022.100514 PubMed DOI PMC

Grierson C., Nielsen E., Ketelaarc T., Schiefelbein J. (2014). Root hairs. Arab B. 12, e0172–e0172. doi: 10.1199/tab.0172 PubMed DOI PMC

Gupta A., Rico-Medina A., Caño-Delgado A. I. (2020). The physiology of plant responses to drought. Science. 368 (6488), 266–269. doi: 10.1126/science.aaz7614 PubMed DOI

Handakumbura P. P., Rivas Ubach A., Battu A. K. (2021). Visualizing the hidden half: Plant-microbe interactions in the rhizosphere. mSystems 6 (5), e0076521. doi: 10.1128/mSystems.00765-21 PubMed DOI PMC

Henriques R., Bögre L., Horváth B., Magyar Z. (2014). Balancing act: Matching growth with environment by the TOR signalling pathway. J. Exp. Botany. 65 (10), 2691–2701. doi: 10.1093/jxb/eru049 PubMed DOI

Henriques R., Calderan-Rodrigues M. J., Luis Crespo J., Baena-González E., Caldana C. (2022). Growing of the TOR world. J. Exp. Bot. 73 (20), 6987–6992. doi: 10.1093/jxb/erac401 PubMed DOI PMC

Herranz R., Valbuena M. A., Manzano A., Kamal K. Y., Villacampa A., Ciska M., et al. . (2022). Use of reduced gravity simulators for plant biological studies. Methods Mol. Biol. 2368, 241–265. doi: 10.1007/978-1-0716-1677-2_16 PubMed DOI

Herranz R., Vandenbrink J. P., Villacampa A., Manzano A., Poehlman W. L., Feltus F. A., et al. . (2019). RNAseq analysis of the response of arabidopsis thaliana to fractional gravity under blue-light stimulation during spaceflight. Front. Plant Sci. 10. doi: 10.3389/fpls.2019.01529 PubMed DOI PMC

Hill K., Porco S., Lobet G., Zappala S., Mooney S., Draye X., et al. . (2013). Root systems biology: Integrative modeling across scales, from gene regulatory networks to the rhizosphere. Plant Physiol. 163 (4), 1487–1503. doi: 10.1104/pp.113.227215 PubMed DOI PMC

Huang L., Yu L.-J., Zhang X., Fan B., Wang F.-Z., Dai Y.-S., et al. . (2019). Autophagy regulates glucose-mediated root meristem activity by modulating ROS production in arabidopsis. Autophagy 15 (3), 407–422. doi: 10.1080/15548627.2018.1520547 PubMed DOI PMC

Iwata S., Miyazawa Y., Fujii N., Takahashi H. (2013). MIZ1-regulated hydrotropism functions in the growth and survival of arabidopsis thaliana under natural conditions. Ann. Bot. 112 (1), 103–114. doi: 10.1093/aob/mct098 PubMed DOI PMC

Jamsheer K. (2019). M.; jindal, s.; laxmi, a. evolution of TOR-SnRK dynamics in green plants and its integration with phytohormone signaling networks. J. Exp. Bot. 70 (8), 2239–2259. doi: 10.1093/jxb/erz107 PubMed DOI

Jamsheer K. ,. M., Kumar M., Srivastava V. (2021). SNF1-related protein kinase 1: The many-faced signaling hub regulating developmental plasticity in plants. J. Exp. Bot. 72 (17), 6042–6065. doi: 10.1093/jxb/erab079 PubMed DOI

Jonsson K., Ma Y., Routier-Kierzkowska A.-L., Bhalerao R. P. (2022). Multiple mechanisms behind plant bending. Nat. Plants. 9 (1), 13–21. doi: 10.1038/s41477-022-01310-y PubMed DOI

Karlova R., Boer D., Hayes S., Testerink C. (2021). Root plasticity under abiotic stress. Plant Physiol. 187 (3), 1057–1070. doi: 10.1093/plphys/kiab392 PubMed DOI PMC

Kashkan I., Garcia-González J., Lacek J., Müller K., Ružička K., Retzer K., et al. . (2022). RaPiD-chamber: Easy to self-assemble live-imaging chamber with adjustable LEDs allows to track small differences in dynamic plant movement adaptation on tissue level. bioRxiv. doi: 10.1101/2022.08.13.503848 DOI

Kawa D., Meyer A. J., Dekker H. L., Abd-El-Haliem A. M., Gevaert K., Van De Slijke E., et al. . (2020). SnRK2 protein kinases and MRNA decapping machinery control root development and response to salt. Plant Physiol. 182 (1), 361–377. doi: 10.1104/pp.19.00818 PubMed DOI PMC

Kim D., Yang J., Gu F., Park S., Combs J., Adams A., et al. . (2020). Temperature-sensitive FERONIA mutant allele that alters root hair growth. Plant Physiol. 185 (2), 405–423. doi: 10.1093/plphys/kiaa051 PubMed DOI PMC

Kolb E., Legué V., Bogeat-Triboulot M.-B. (2017). Physical root-soil interactions. Phys. Biol. 14 (6), 65004. doi: 10.1088/1478-3975/aa90dd PubMed DOI

Konstantinova N., Korbei B., Luschnig C. (2021). Auxin and root gravitropism: Addressing basic cellular processes by exploiting a defined growth response. Int. J. Mol. Sci. 22 (5), 2749. doi: 10.3390/ijms22052749 PubMed DOI PMC

Kulik A., Wawer I., Krzywińska E., Bucholc M., Dobrowolska G. (2011). SnRK2 protein kinases–key regulators of plant response to abiotic stresses. OMICS 15 (12), 859–872. doi: 10.1089/omi.2011.0091 PubMed DOI PMC

Lacek J., García-González J., Weckwerth W., Retzer K. (2021). Lessons learned from the studies of roots shaded from direct root illumination. Int. J. Mol. Sci. 22 (23), 12784. doi: 10.3390/ijms222312784 PubMed DOI PMC

Laxmi A., Pan J., Morsy M., Chen R. (2008). Light plays an essential role in intracellular distribution of auxin efflux carrier PIN2 in arabidopsis thaliana. PloS One. 3 (1), e1510. doi: 10.1371/journal.pone.0001510 PubMed DOI PMC

Leftley N., Banda J., Pandey B., Bennett M., Voß U. (2021). Uncovering how auxin optimizes root systems architecture in response to environmental stresses. Cold Spring Harb Perspect. Biol. 13 (11), a040014. doi: 10.1101/cshperspect.a040014 PubMed DOI PMC

Li X., Cai W., Liu Y., Li H., Fu L., Liu Z., et al. . (2017). Differential TOR activation and cell proliferation in arabidopsis root and shoot apexes. Proc. Natl. Acad. Sci. U S A. 114 (10), 2765–2770. doi: 10.1073/pnas.1618782114 PubMed DOI PMC

Li S., Tian Y., Wu K., Ye Y., Yu J., Zhang J., et al. . (2018). Modulating plant growth–metabolism coordination for sustainable agriculture. Nature 560 (7720), 595–600. doi: 10.1038/s41586-018-0415-5 PubMed DOI PMC

Li L., Verstraeten I., Roosjen M., Takahashi K., Rodriguez L., Merrin J., et al. . (2021). Cell surface and intracellular auxin signalling for h(+) fluxes in root growth. Nature 599 (7884), 273–277. doi: 10.1038/s41586-021-04037-6 PubMed DOI PMC

Li Y., Yuan W., Li L., Miao R., Dai H., Zhang J., et al. . (2020). Light-dark modulates root hydrotropism associated with gravitropism by involving amyloplast response in arabidopsis. Cell Rep. 32 13, 108198. doi: 10.1016/j.celrep.2020.108198 PubMed DOI

Lopez D., Tocquard K., Venisse J.-S., Legué V., Roeckel-Drevet P. (2014). Gravity sensing, a largely misunderstood trigger of plant orientated growth. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00610 PubMed DOI PMC

Luschnig C., Gaxiola R. A., Grisafi P., Fink G. R. (1998). EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in arabidopsis thaliana. Genes Dev. 12 (14), 2175–2187. doi: 10.1101/gad.12.14.2175 PubMed DOI PMC

Ma M., Lu Y., Di D., Kronzucker H. J., Dong G., Shi W. (2023). The nitrification inhibitor 1,9-decanediol from rice roots promotes root growth in arabidopsis through involvement of ABA and PIN2-mediated auxin signaling. J. Plant Physiol. 280, 153891. doi: 10.1016/j.jplph.2022.153891 PubMed DOI

Ma L., Shi Y., Siemianowski O., Yuan B., Egner T. K., Mirnezami S. V., et al. . (2019). Hydrogel-based transparent soils for root phenotyping in vivo. Proc. Natl. Acad. Sci. U S A 116 (22), 11063–11068. doi: 10.1073/pnas.1820334116 PubMed DOI PMC

Mair A., Pedrotti L., Wurzinger B., Anrather D., Simeunovic A., Weiste C., et al. . (2015). SnRK1-triggered switch of BZIP63 dimerization mediates the low-energy response in plants. Elife. 4, e05828. doi: 10.7554/eLife.05828 PubMed DOI PMC

Mairhofer S., Pridmore T., Johnson J., Wells D. M., Bennett M. J., Mooney S. J. (2017). Sturrock, c. j. X-ray computed tomography of crop plant root systems grown in soil. Curr. Protoc. Plant Biol. 2 (4), 270–286. doi: 10.1002/cppb.20049 PubMed DOI

Mairhofer S., Zappala S., Tracy S., Sturrock C., Bennett M. J., Mooney S. J., et al. . (2013). Recovering complete plant root system architectures from soil via X-ray μ-computed tomography. Plant Methods 9 (1), 8. doi: 10.1186/1746-4811-9-8 PubMed DOI PMC

Margalha L., Confraria A., Baena-González E. (2019). SnRK1 and TOR: Modulating growth–defense trade-offs in plant stress responses. J. Exp. Botany. 70 (8), 2261–2274. doi: 10.1093/jxb/erz066 PubMed DOI

Margalha L., Valerio C., Baena-González E. (2016). Plant SnRK1 kinases: Structure, regulation, and function. EXS. doi: 10.1007/978-3-319-43589-3_17 PubMed DOI

Massa G. D., Gilroy S. (2003). Touch modulates gravity sensing to regulate the growth of primary roots of arabidopsis thaliana. Plant J. 33 (3), 435–445. doi: 10.1046/j.1365-313x.2003.01637.x PubMed DOI

Mehra P., Pandey B. K., Melebari D., Banda J., Leftley N., Couvreur V., et al. . (2022). Hydraulic flux-responsive hormone redistribution determines root branching. Science 378 (6621), 762–768. doi: 10.1126/science.add3771 PubMed DOI

Migliaccio F., Fortunati A., Tassone P. (2009). Arabidopsis root growth movements and their symmetry: Progress and problems arising from recent work. Plant Signal. Behav. 4 (3), 183–190. doi: 10.4161/psb.4.3.7959 PubMed DOI PMC

Millar K. D. L., Kiss J. Z. (2013). Analyses of tropistic responses using metabolomics. Am. J. Bot. 100 (1), 79–90. doi: 10.3732/ajb.1200316 PubMed DOI

Miotto Y., Da Costa C. T., Offringa R., Kleine-Vehn J., Maraschin F. D. (2021). Effects of light intensity on root development in a d-root growth system. Front. Plant Sci. 12, 778382. doi: 10.3389/fpls.2021.778382 PubMed DOI PMC

Miyazawa Y., Yamazaki T., Moriwaki T., Takahashi H. (2011). “Chapter 10 - root tropism: Its mechanism and possible functions in drought avoidance,” in Plant responses to drought and salinity stress; turkan, i. b. t.-a. @ in b. r., Ed, vol. 57. (Academic Press; ), pp 349–pp 375. doi: 10.1016/B978-0-12-387692-8.00010-2 DOI

Mo M., Yokawa K., Wan Y., Baluska F. (2015). How and why do root apices sense light under the soil surface? Front. Plant Science. 6, 775. doi: 10.3389/fpls.2015.00775 PubMed DOI PMC

Montes C., Wang P., Liao C.-Y., Nolan T. M., Song G., Clark N. M., et al. . (2022). Integration of multi-omics data reveals interplay between brassinosteroid and target of rapamycin complex signaling in arabidopsis. New Phytol. 236 (3), 893–910. doi: 10.1111/nph.18404 PubMed DOI PMC

Muralidhara P., Weiste C., Collani S., Krischke M., Kreisz P., Draken J., et al. . (2021). Perturbations in plant energy homeostasis prime lateral root initiation via SnRK1-BZIP63-ARF19 signaling. Proc. Natl. Acad. Sci. U S A 118 (37), e2106961118. doi: 10.1073/pnas.2106961118 PubMed DOI PMC

Muramoto J., Parr D. M., Perez J., Wong D. G. (2022). Integrated soil health management for plant health and one health: Lessons from histories of soil-borne disease management in California strawberries and arthropod pest management. Front. Sustain. Food Syst. 6. doi: 10.3389/fsufs.2022.839648 DOI

Muthert L. W. F., Izzo L. G., van Zanten M., Aronne G. (2020). Root tropisms: Investigations on earth and in space to unravel plant growth direction. Front. Plant Sci. 10. doi: 10.3389/fpls.2019.01807 PubMed DOI PMC

Najrana T., Sanchez-Esteban J. (2016). Mechanotransduction as an adaptation to gravity. Front. Pediatr. 4. doi: 10.3389/fped.2016.00140 PubMed DOI PMC

Nukarinen E., Ngele T., Pedrotti L., Wurzinger B., Mair A., Landgraf R., et al. . (2016). Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation. Sci. Rep. 6, 31697. doi: 10.1038/srep31697 PubMed DOI PMC

Okada K., Shimura Y. (1990). Reversible root tip rotation in arabidopsis seedlings induced by obstacle-touching stimulus. Science 250 (4978), 274–276. doi: 10.1126/science.250.4978.274 PubMed DOI

Ottenschläger I., Wolff P., Wolverton C., Bhalerao R. P., Sandberg G., Ishikawa H., et al. . (2003). Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. U S A 100 (5), 2987–2991. doi: 10.1073/pnas.0437936100 PubMed DOI PMC

Pedrotti L., Weiste C., Nägele T., Wolf E., Lorenzin F., Dietrich K., et al. . (2018). Snf1-RELATED KINASE1-controlled C/S(1)-BZIP signaling activates alternative mitochondrial metabolic pathways to ensure plant survival in extended darkness. Plant Cell 30 (2), 495–509. doi: 10.1105/tpc.17.00414 PubMed DOI PMC

Peixoto B., Baena-González E. (2022). Management of plant central metabolism by SnRK1 protein kinases. J. Exp. Bot. 73 (20), 7068–7082. doi: 10.1093/jxb/erac261 PubMed DOI PMC

Pérez-Pérez M. E., Florencio F. J., Crespo J. L. (2010). Inhibition of target of rapamycin signaling and stress activate autophagy in chlamydomonas reinhardtii. Plant Physiol. 152 (4), 1874–1888. doi: 10.1104/pp.109.152520 PubMed DOI PMC

Pierik R., Fankhauser C., Strader L. C., Sinha N. (2021). Architecture and plasticity: Optimizing plant performance in dynamic environments. Plant Physiol. 187 (3), 1029–1032. doi: 10.1093/plphys/kiab402 PubMed DOI PMC

Pierik R., Testerink C. (2014). The art of being flexible: How to escape from shade, salt, and Drought1. Plant Physiol. 166 (1), 5–22. doi: 10.1104/pp.114.239160 PubMed DOI PMC

Piñeros M. A., Larson B. G., Shaff J. E., Schneider D. J., Falcão A. X., Yuan L., et al. . (2016). Evolving technologies for growing, imaging and analyzing 3D root system architecture of crop plants. J. Integr. Plant Biol. 58 (3), 230–241. doi: 10.1111/jipb.12456 PubMed DOI

Pu Y., Soto-Burgos J., Bassham D. C. (2017). Regulation of autophagy through SnRK1 and TOR signaling pathways. Plant Signal. Behav. 12 (12), e1395128. doi: 10.1080/15592324.2017.1395128 PubMed DOI PMC

Ramon M., Dang T. V. T., Broeckx T., Hulsmans S., Crepin N., Sheen J., et al. . (2019). Default activation and nuclear translocation of the plant cellular energy sensor SnRK1 regulate metabolic stress responses and development. Plant Cell. 31 (7), 1614–1632. doi: 10.1105/tpc.18.00500 PubMed DOI PMC

Retzer K., Akhmanova M., Konstantinova N., Malínská K., Leitner J., Petrášek J., et al. . (2019). Brassinosteroid signaling delimits root gravitropism via sorting of the arabidopsis PIN2 auxin transporter. Nat. Commun. 10 (1), 5516. doi: 10.1038/s41467-019-13543-1 PubMed DOI PMC

Retzer K., Korbei B., Luschnig C. (2014). “Auxin and tropisms,” in Auxin and its role in plant development. Springer, Vienna. doi: 10.1007/978-3-7091-1526-8_16 DOI

Retzer K., Lacek J., Skokan R., Del Genio C. I., Vosolsobě S., Laňková M., et al. . (2017). Evolutionary conserved cysteines function as cis-acting regulators of arabidopsis PIN-FORMED 2 distribution. Int. J. Mol. Sci. 18 (11), 2274. doi: 10.3390/ijms18112274 PubMed DOI PMC

Retzer K., Weckwerth W. (2021). The tor–auxin connection upstream of root hair growth. Plants. 10 (1), 150. doi: 10.3390/plants10010150 PubMed DOI PMC

Rogers E. D., Monaenkova D., Mijar M., Nori A., Goldman D. I. (2016). Benfey, p. n. X-ray computed tomography reveals the response of root system architecture to soil texture. Plant Physiol. 171 (3), 2028–2040. doi: 10.1104/pp.16.00397 PubMed DOI PMC

Roustan V., Jain A., Teige M., Ebersberger I., Weckwerth W. (2016). An evolutionary perspective of AMPK-TOR signaling in the three domains of life. J. Exp. Botany. 67 (13), 3897–3907. doi: 10.1093/jxb/erw211 PubMed DOI

Ryabova L. A., Robaglia C., Meyer C. (2019). Target of rapamycin kinase: Central regulatory hub for plant growth and metabolism. J. Exp. Botany. 70 (8), 2211–2216. doi: 10.1093/jxb/erz108 PubMed DOI PMC

Saleem M., Law A. D., Sahib M. R., Pervaiz Z. H., Zhang Q. (2018). Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere 6, 47–51. doi: 10.1016/j.rhisph.2018.02.003 DOI

Salem M. A., Li Y., Bajdzienko K., Fisahn J., Watanabe M., Hoefgen R., et al. . (2018). RAPTOR controls developmental growth transitions by altering the hormonal and metabolic balance. Plant Physiol. 177 (2), 565–593. doi: 10.1104/pp.17.01711 PubMed DOI PMC

Shymanovich T., Vandenbrink J. P., Herranz R., Medina F. J., Kiss J. Z. (2022). Spaceflight studies identify a gene encoding an intermediate filament involved in tropism pathways. Plant Physiol. Biochem. PPB 171, 191–200. doi: 10.1016/j.plaphy.2021.12.039 PubMed DOI

Signorelli S., Tarkowski Ł.P., Van den Ende W., Bassham D. C. (2019). Linking autophagy to abiotic and biotic stress responses. Trends Plant Sci. 24 (5), 413–430. doi: 10.1016/j.tplants.2019.02.001 PubMed DOI PMC

Silva-Navas J., Conesa C. M., Saez A., Navarro-Neila S., Garcia-Mina J. M., Zamarreño A. M., et al. . (2019). Role of cis-zeatin in root responses to phosphate starvation. New Phytol. 224 (1), 242–257. doi: 10.1111/nph.16020 PubMed DOI

Silva-Navas J., Moreno-Risueno M. A., Manzano C., Pallero-Baena M., Navarro-Neila S., Téllez-Robledo B., et al. . (2015). D-root: A system for cultivating plants with the roots in darkness or under different light conditions. Plant J. 84 (1), 244–255. doi: 10.1111/tpj.12998 PubMed DOI

Silva-Navas J., Moreno-Risueno M. A., Manzano C., Téllez-Robledo B., Navarro-Neila S., Carrasco V., et al. . (2016). Flavonols mediate root phototropism and growth through regulation of proliferation-to-Differentiation transition. Plant Cell. 28 (6), 1372–1387. doi: 10.1105/tpc.15.00857 PubMed DOI PMC

Son S., Im J. H., Ko J.-H., Han K.-H. (2023). SNF1-related protein kinase 1 represses arabidopsis growth through post-translational modification of E2Fa in response to energy stress. New Phytol. 237 (3), 823–839. doi: 10.1111/nph.18597 PubMed DOI PMC

Soto-Burgos J., Bassham D. C. (2017). SnRK1 activates autophagy via the TOR signaling pathway in arabidopsis thaliana. PloS One. 12 (8), e0182591. doi: 10.1371/journal.pone.0182591 PubMed DOI PMC

Sun D., Fang X., Xiao C., Ma Z., Huang X., Su J., et al. . (2021). Kinase SnRK1.1 regulates nitrate channel SLAH3 engaged in nitrate-dependent alleviation of ammonium toxicity. Plant Physiol. 186 (1), 731–749. doi: 10.1093/plphys/kiab057 PubMed DOI PMC

Swarup R., Bennett M. J. (2009). Root gravitropism; American cancer society. In Annual Plant Reviews: Root Development; Blackwell Publishing: Oxford, UK, 2009. doi: 10.1002/9781444310023.ch6 DOI

Swarup R., Kramer E. M., Perry P., Knox K., Leyser H. M. O., Haseloff J., et al. . (2005). Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7 (11), 1057–1065. doi: 10.1038/ncb1316 PubMed DOI

Taylor I., Lehner K., McCaskey E., Nirmal N., Ozkan-Aydin Y., Murray-Cooper M., et al. . (2021). Mechanism and function of root circumnutation. Proc. Natl. Acad. Sci. U S A 118 (8), e2018940118. doi: 10.1073/pnas.2018940118 PubMed DOI PMC

Thompson M. V., Holbrook N. M. (2004). Root-gel interactions and the root waving behavior of arabidopsis. Plant Physiol. 135 (3), 1822–1837. doi: 10.1104/pp.104.040881 PubMed DOI PMC

Tojo H., Nakamura A., Ferjani A., Kazama Y., Abe T., Iida H. A. (2021). Method enabling comprehensive isolation of arabidopsis mutants exhibiting unusual root mechanical behavior. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.646404 PubMed DOI PMC

Trewavas A., Knight M. (1994). Mechanical signalling, calcium and plant form. Plant Mol. Biol. 26 (5), 1329–1341. doi: 10.1007/BF00016478 PubMed DOI

Valbuena M. A., Manzano A., Vandenbrink J. P., Pereda-Loth V., Carnero-Diaz E., Edelmann R. E., et al. . (2018). The combined effects of real or simulated microgravity and red-light photoactivation on plant root meristematic cells. Planta 248 (3), 691–704. doi: 10.1007/s00425-018-2930-x PubMed DOI

Vandenbrink J. P., Kiss J. Z. (2019). Plant responses to gravity. Semin. Cell Dev. Biol. 92, 122–125. doi: 10.1016/j.semcdb.2019.03.011 PubMed DOI

Vandenbrink J. P., Kiss J. Z., Herranz R., Medina F. J. (2014). Light and gravity signals synergize in modulating plant development. Front. Plant Sci. 5. doi: 10.3389/fpls.2014.00563 PubMed DOI PMC

van Gelderen K., Kang C., Li P., Pierik R. (2021). Regulation of lateral root development by shoot-sensed far-red light via HY5 is nitrate-dependent and involves the NRT2.1 nitrate transporter. Front. Plant Sci. 12. doi: 10.3389/fpls.2021.660870 PubMed DOI PMC

Van Leene J., Eeckhout D., Gadeyne A., Matthijs C., Han C., De Winne N., et al. . (2022). Mapping of the plant SnRK1 kinase signalling network reveals a key regulatory role for the class II T6P synthase-like proteins. Nat. Plants 8 (11), 1245–1261. doi: 10.1038/s41477-022-01269-w PubMed DOI

Van Leene J., Han C., Gadeyne A., Eeckhout D., Matthijs C., Cannoot B., et al. . (2019). Capturing the phosphorylation and protein interaction landscape of the plant TOR kinase. Nat. Plants 5 (3), 316–327. doi: 10.1038/s41477-019-0378-z PubMed DOI

van Loon J. J. (2009). ~W. ~A. mechanomics and physicomics in gravisensing. Microgravity Sci. Technol. 21 (1–2), 159–167. doi: 10.1007/s12217-008-9065-9 DOI

Villacampa A., Fañanás-Pueyo I., Medina F. J., Ciska M. (2022). Root growth direction in simulated microgravity is modulated by a light avoidance mechanism mediated by flavonols. Physiol. Plant 174 (3), e13722. doi: 10.1111/ppl.13722 PubMed DOI PMC

Wan Y., Jasik J., Wang L., Hao H., Volkmann D., Menzel D., et al. . (2012). The signal transducer NPH3 integrates the Phototropin1 photosensor with PIN2-based polar auxin transport in arabidopsis root phototropism. Plant Cell 24 (2), 551–565. doi: 10.1105/tpc.111.094284 PubMed DOI PMC

Wan Y., Yokawa K., Baluška F. (2019). Arabidopsis roots and light: Complex interactions. Mol. Plant. 12 (11), 1428–1430. doi: 10.1016/j.molp.2019.10.001 PubMed DOI

Weckwerth W. (2003). Metabolomics in systems biology. Annu. Rev. Plant Biol. 54, 669–689. doi: 10.1146/annurev.arplant.54.031902.135014 PubMed DOI

Weckwerth W. (2008). Integration of metabolomics and proteomics in molecular plant physiology–coping with the complexity by data-dimensionality reduction. Physiol. Plant 132 (2), 176–189. doi: 10.1111/j.1399-3054.2007.01011.x PubMed DOI

Weckwerth W. (2011). Green systems biology - from single genomes, proteomes and metabolomes to ecosystems research and biotechnology. J. Proteomics 75 (1), 284–305. doi: 10.1016/j.jprot.2011.07.010 PubMed DOI

Weckwerth W., Ghatak A., Bellaire A., Chaturvedi P., Varshney R. K. (2020). PANOMICS meets germplasm. Plant Biotechnol. J. 18 (7), 1507–1525. doi: 10.1111/pbi.13372 PubMed DOI PMC

Weiste C., Pedrotti L., Selvanayagam J., Muralidhara P., Fröschel C., Novák O., et al. . (2017). The arabidopsis BZIP11 transcription factor links low-energy signalling to auxin-mediated control of primary root growth. PloS Genet. 13 (2), e1006607. doi: 10.1371/journal.pgen.1006607 PubMed DOI PMC

Wisniewska J., Xu J., Seifartová D., Brewer P. B., Růžička K., Blilou L., et al. . (2006). Polar PIN localization directs auxin flow in plants. Science 80-.). 312 (5775), 883. doi: 10.1126/science.1121356 PubMed DOI

Wu Y., Shi L., Li L., Fu L., Liu Y., Xiong Y., et al. . (2019). Integration of nutrient, energy, light, and hormone signalling via TOR in plants. J. Exp. Botany. 70 (8), 2227–2238. doi: 10.1093/jxb/erz028 PubMed DOI PMC

Wurzinger B., Mair A., Fischer-Schrader K., Nukarinen E., Roustan V., Weckwerth W., et al. . (2017). Redox state-dependent modulation of plant SnRK1 kinase activity differs from AMPK regulation in animals. FEBS Lett. 591 (21), 3625–3636. doi: 10.1002/1873-3468.12852 PubMed DOI PMC

Wurzinger B., Nukarinen E., Nägele T., Weckwerth W., Teige M. (2018). The SnRK1 kinase as central mediator of energy signaling between different organelles. Plant Physiol. 176 (2), 1085–1094. doi: 10.1104/pp.17.01404 PubMed DOI PMC

Wyatt S. E., Kiss J. Z. (2013). Plant tropisms: From Darwin to the international space station. American journal of botany . United States January, 100 (1), 1–3. doi: 10.3732/ajb.1200591 PubMed DOI

Xu W., Ding G., Yokawa K., Baluška F., Li Q. F., Liu Y., et al. . (2013). An improved agar-plate method for studying root growth and response of arabidopsis thaliana. Sci. Rep. 3, 1273. doi: 10.1038/srep01273 PubMed DOI PMC

Yan J., Wang B., Zhou Y., Hao S. (2018). Resistance from agar medium impacts the helical growth of arabidopsis primary roots. J. Mech. Behav. Biomed. Mater. 85, 43–50. doi: 10.1016/j.jmbbm.2018.05.018 PubMed DOI

Yang Y., Guo Y. (2018). Unraveling salt stress signaling in plants. J. Integr. Plant Biol. 60 (9), 796–804. doi: 10.1111/jipb.12689 PubMed DOI

Yang G., Yu Z., Gao L., Zheng C. (2019). SnRK2s at the crossroads of growth and stress responses. Trends Plant Sci. 24 (8), 672–676. doi: 10.1016/j.tplants.2019.05.010 PubMed DOI

Yokawa K., Baluška F. (2016). The TOR complex: An emergency switch for root behavior. Plant Cell Physiol. 57 (1), 14–18. doi: 10.1093/pcp/pcv191 PubMed DOI

Yokawa K., Fasano R., Kagenishi T., Baluška F. (2014. a). Light as stress factor to plant roots – case of root halotropism. Front. Plant Sci. 5, 718. doi: 10.3389/fpls.2014.00718 PubMed DOI PMC

Yokawa K., Kagenishi T., Baluška F. (2016). UV-B induced generation of reactive oxygen species promotes formation of BFA-induced compartments in cells of arabidopsis root apices. Front. Plant Sci. 6, 1162. doi: 10.3389/fpls.2015.01162 PubMed DOI PMC

Yokawa K., Koshiba T., Baluška F. (2014. b). Light-dependent control of redox balance and auxin biosynthesis in plants. Plant Signal. Behav. 9, e29522. doi: 10.4161/psb.29522 PubMed DOI PMC

Yu B., Zheng W., Xing L., Zhu J.-K., Persson S., Zhao Y. (2022). Root twisting drives halotropism via stress-induced microtubule reorientation. Dev. Cell 57 (20), 2412–2425.e6. doi: 10.1016/j.devcel.2022.09.012 PubMed DOI

Zhang Y., Friml J. (2020). Auxin guides roots to avoid obstacles during gravitropic growth. New Phytol. 225 (3), 1049–1052. doi: 10.1111/nph.16203 PubMed DOI PMC