Abstract
Plants cannot grow or develop properly without the support of their roots. Gravity plays an essential role in the formation of the root structure, but it is not clear how roots respond to gravity signals or how downward growth occurs. The two best-known models for root gravity sensing affirm the importance of starch. After the hyper-sensitive root crown perceives a gravity signal, starch granules within the rootlet cells settle to the endoplasmic reticulum in the direction of the signal, where they bind to specific receptors or open ion channels and release downstream signaling molecules. This triggers a series of signal transduction mechanisms, and this process involves signaling molecules such as indole-3‐acetic acid (IAA), reactive oxygen species, and calcium signaling, which ultimately induce groundward root growth. This review summarizes the mechanism of action underlying, and a research overview of, how plant roots sense and respond to gravity. The role of key signals such as starch, IAA, and calcium ions in root gravitropism is analyzed by integrating available information. The results provide a more complete theoretical basis for how roots grow toward gravity, which will contribute to our understanding of gravitropism and lay the foundation for discovering new directions of scientific research.
Graphical abstract
The graphics developed in this article are done by Microsoft Office PowerPoint 2010, Adobe Illustrator 2018 and ChemDraw 20.0.
Similar content being viewed by others
Data availability
Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.
References
Aubry-Hivet D, Nziengui H, Rapp K, Oliveira O, Paponov IA, Li Y, Hauslage J, Vagt N, Braun M, Ditengou FA, Dovzhenko A, Palme K (2014) Analysis of gene expression during parabolic flights revealsdistinct early gravity responses in Arabidopsis roots. Plant Biol (Stuttg) 1:129–141. https://doi.org/10.1111/plb.12130
Baldwin K, Strohm A, Masson P (2013) Gravity sensing and signal transduction in vascular plant primary roots. Am J Bot 100(1):126–142. https://doi.org/10.3732/ajb.1200318
Band LR, Wells DM, Larrieu A, Sun JY, Middleton AM, French AP, Brunoud G, Sato EM, Wilson MH, Péret B, Oliva M, Swarup R, Sairanen I, Parry G, Ljung K, Beeckman T, Garibaldi JM, Estelle M, Owen MR, Vissenberg K, Hodgman TC, Pridmore TP, King JR, Vernoux T, Bennett MJ (2012) Root gravitropism is regulated by a transient lateral auxin gradient controlled by a tipping-point mechanism. Proc Natl Acad Sci U S A 109(12):4668–4673. https://doi.org/10.1073/pnas.1201498109
Barlow PW (1974) Regeneration of the cap of primary roots of Zea mays. New Phytol 73:937–954
Barba-Espin G, Diaz-Vivancos P, Clemente-Moreno MJ, Albacete A, Faize L, Faize M, Pérez-Alfocea F, Hernández JA (2010) Interaction between hydrogen peroxide and plant hormones during germination and the early growth of pea seedlings. Plant Cell Environ 33(6):981–994. https://doi.org/10.1111/j.1365-3040.2010.02120.x
Batistic O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820(8):1283–1293. https://doi.org/10.1016/j.bbagen.2011.10.012
Belyavskaya NA (1992) The function of calcium in plant graviperception. Adv Space Res 12(1):83–91. https://doi.org/10.1016/0273-1177(92)90267-2
Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273(5277):948–950. https://doi.org/10.1126/science.273.5277.948
Blancaflor EB, Fasano JM, Gilroy S (1998) Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. Plant Physiol 116(1):213–222
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433(7021):39–44. https://doi.org/10.1038/nature03184
Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482(7383):103–106. https://doi.org/10.1038/nature10791
Caspar T, Pickard BG (1989) Gravitropism in a starchless mutant of Arabidopsis: implications for the starch-statolith hypothesis theory of gravity sensing. Planta 177:185–197. https://doi.org/10.1007/BF00392807
Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH (1998) The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc Natl Acad Sci U S A 95(25):15112–15117. https://doi.org/10.1073/pnas.95.25.15112
Chen YP, Xu SM, Tian L, Liu LR, Huang MC, Xu XL, Song GY, Wu PZ, Sato SS, Jiang HW, Wu GJ (2020) LAZY3 plays a pivotal role in positive root gravitropism in Lotus japonicus. J Exp Bot 71(1):168–177. https://doi.org/10.1093/jxb/erz429
Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129(2):469–485. https://doi.org/10.1104/pp.005645
DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signaling. Biochem J 425(1):27–40. https://doi.org/10.1042/BJ20091147
Edelmann HG (2018) Graviperception in maize plants: is amyloplast sedimentation a red herring? Protoplasma 255(6):1877–1881. https://doi.org/10.1007/s00709-018-1272-7
Evans ML, Moore R, Hasenstein KH (1986) How roots respond to gravity. Sci Am 255(6):112–119. https://doi.org/10.1038/scientificamerican1286-112
Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422(6930):442–446. https://doi.org/10.1038/nature01485
Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415(6873):806–809. https://doi.org/10.1038/415806a
Fuji N, Miyabayashi S, Sugita T, Kobayashi A, Yamazaki C, Miyazawa Y, Kamada M, Kasahara H, Osada I, Shimazu T, Fusejima Y, Higashibata A, Yamazaki T, Ishioka N, Takahashi H (2018) Root-tip-mediated inhibition of hydrotropism is accompanied with the suppression of asymmetric expression of auxin-inducible genes in response to moisture gradients in cucumber roots. PLoS ONE 13(1):e0189827. https://doi.org/10.1371/journal.pone.0189827
Furutani M, Hirano Y, Nishimura T, Nakamura M, Taniguchi M, Suzuki K, Oshida R, Kondo C, Sun S, Kato K, Fukao Y, Hakoshima T, Morita MT (2020) Polar recruitment of RLD by LAZY1-like protein during gravity signaling in root branch angle control. Nat Commun 11(1):76. https://doi.org/10.1038/s41467-019-13729-7
Ganguly A, Lee SH, Cho HT (2012) Functional identification of the phosphorylation sites of Arabidopsis PIN-FORMED3 for its subcellular localization and biological role. Plant J 71(5):810–823. https://doi.org/10.1111/j.1365-313X.2012.05030.x
Ge LF, Chen RJ (2016) Negative gravitropism in plant roots. Nat Plants 2(11):16155. https://doi.org/10.1038/nplants.2016.155
Ge LF, Chen RJ (2019) Negative gravitropic response of roots directs auxin flow to control root gravitropism. Plant Cell Environ 42(8):2372–2383. https://doi.org/10.1111/pce.13559
Grenzi M, Resentini F, Vanneste S, Zottini M, Bassi A, Costa A (2021) Illuminating the hidden world of calcium ions in plants with a universe of indicators. Plant Physiol 187:550–571. https://doi.org/10.1093/plphys/kiab339
Grones P, Abas P, Hajný J, Jones A, Waidmann S, Kleine-Vehn S, Friml J (2018) PID/WAG-mediated phosphorylation of the Arabidopsis PIN3 auxin transporter mediates polarity switches during gravitropism. Sci Rep 8(1):10279. https://doi.org/10.1038/s41598-018-28188-1
Haberlandt G (1900) Über die perzeption des geotropischen reizes. Ber Dtsch Bot Ges 18:261–272
Hager A (2003) Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects. J Plant Res 116(6):483–505. https://doi.org/10.1007/s10265-003-0110-x
Han HB, Adamowski M, Qi LL, Alotaibi SS, Friml J (2021) PIN-mediated polar auxin transport regulations in plant tropic responses. New Phytol 232(2):510–522. https://doi.org/10.1111/nph.17617
Harmon AC, Grisbov M, Harper JF (2000) CDPKs-a kinase for every Ca2+ signal? Trends Plant Sci 5(4):154–159. https://doi.org/10.1016/s1360-1385(00)01577-6
Hepler PK, Wayne RO (1985) Calcium and plant development. Ann Rev Plant Physiol 36:397–439
Ishikawa H, Evans ML (1990) Gravity-induced changes in intracellular potentials in elongation cortical cells of mung bean roots. Plant Cell Physiol 31(4):457–462
Ja´slan D, Dreyer I, Lu J, O’Malley R, Dindas J, Marten I, Hedrich R (2019) Voltage-dependent gating of SV channel TPC1 confers vacuole excitability. Nat Commun 10(1):2659. https://doi.org/10.1038/s41467-019-10599-x
Jiang GL, Su M, Wang LY, Jiao CJ, Sun ZX, Cheng W, Li FM, Wang CY (2012) Exogenous hydrogen peroxide reversibly inhibits root gravitropism and induces horizontal curvature of primary root during grass pea germination. Plant Physiol Biochem 53:84–93. https://doi.org/10.1016/j.plaphy.2012.01.017
Jiao ZC, Du H, Chen S, Huang W, Ge LF (2021) LAZY gene family in plant gravitropism. Front Plant Sci 11:606241. https://doi.org/10.3389/fpls.2020.606241
Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126(3):1055–1060. https://doi.org/10.1104/pp.126.3.1055
Kaneko M, Itoh H, Ueguchi-Tanaka M, Ashikari M, Matsuoka M (2002) The α-amylase induction in endosperm during rice seed germination is caused by gibberellin synthesized in epithelium. Plant Physiol 128(4):1264–1270. https://doi.org/10.1104/pp.010785
Kiss JZ, Hertel R, Sack FD (1989) Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 177(2):198–206. https://doi.org/10.1007/BF00392808
Kleine-Vehn J, Ding ZJ, Jones AR, Tasaka M, Morita MT, Friml J (2010) Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity sensing root cells. Proc Natl Acad Sci U S A 107(51):22344–22349. https://doi.org/10.1073/pnas.1013145107
Knight TA (1806) On the direction of the radicle and germen during the vegetation of seeds. Phil Trans R SOC 99:108–120
Kordyum EL (2003) Calcium signaling in plant cells in altered gravity. Adv Space Res 32(8):1621–1630. https://doi.org/10.1016/S0273-1177(03)90403-0
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. https://doi.org/10.3390/ijms22052749
Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14(10):2627–2641. https://doi.org/10.1105/tpc.005579
Lee JS, Mulkey TJ, Evans ML (1983) Gravity-induced polar transport of calcium across root tips of maize. Plant Physiol 73(4):874–876. https://doi.org/10.1104/pp.73.4.874
Lee JS, Mulkey TJ, Evans ML (1984) Inhibition of polar calcium movement and gravitropism in roots treated with auxin-transport inhibitors. Planta 160:536–543
Lee JS, Chang WK, Evans ML (1990) Effects of ethylene on the kinetics of curvature and auxin redistribution in gravistimulated roots of Zea mays. Plant Physiol 94(4):1770–1775. https://doi.org/10.1104/pp.94.4.1770
Li S, Xue L, Xu S, Feng H, An L (2007) Hydrogen peroxide involvement in formation and development of adventitious roots in cucumber. Plant Growth Regul 52:173–180. https://doi.org/10.1007/s10725-007-9188-9
Li S, Su LR, Ma SY, Shi ZZ, Yang XM (2015) Initial exploration of the mechanism underlying H2O2-induced root horizontal bending in pea. Sci Bull 60(14):1298–1300. https://doi.org/10.1007/s11434-015-0820-1
Li S, Su LR, Ma SY, Shi ZZ, Zhang Z, Liu HJ, Zhang JL, Yang XM, Sun ZW (2016) The impacts of exogenous H2O2 on primary root horizontal bending of pea (Pisum sativum). Plant Growth Regul 78:287–296. https://doi.org/10.1007/s10725-015-0092-4
Limbach C, Hauslage J, Schäfer C, Braun M (2005) How to activate a plant gravireceptor. Early mechanisms of gravity sensing studied in characean rhizoids during parabolic flights. Plant Physiol 139(2):1030–1040. https://doi.org/10.1104/pp.105.068106
Lin TS, Caspar T, Somerville CR, Preiss J (1988) A starch deficient mutant of Arabidopsis thaliana with low ADP glucose pyrophosphorylase activity lacks one of the two subunits of the enzyme’. Plant Physiol 88(4):1175–1181
Liu J, Rowe J, Lindsey K (2014) Hormonal crosstalk for root development: a combined experimental and modeling perspective. Front Plant Sci 5:116. https://doi.org/10.3389/fpls.2014.00116
Liu H, Liu B, Chen XL, Zhu H, Zou CX, Men SZ (2018) AUX1 acts upstream of PIN2 in regulating root gravitropism. Biochem Biophys Res Commun 507(1–4):433–436. https://doi.org/10.1016/j.bbrc.2018.11.056
Luo J, Zhou JJ, Zhang JZ (2018) Aux/IAA gene family in plants: molecular structure, regulation, and function. Int J Mol Sci 19(1):259. https://doi.org/10.3390/ijms19010259
Luschnig C, Gaxiola R, Grisafi P, Fink GR (1998) EIR1 a root specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12(14):2175–2187. https://doi.org/10.1101/gad.12.14.2175
Mancuso S, Barlow P, Volkmann D, Baluska F (2006) Actin turnover-mediated gravity response in maize root apices: gravitropism of de-capped roots implicates gravisensing outside of the root cap. Plant Signal Behav 1(2):52–58. https://doi.org/10.4161/psb.1.2.2432
Manian V, Orozco J, Gangapuram H, Janwa H, Agrinsoni C (2021) Network analysis of gene transcriptions of Arabidopsis thaliana in spaceflight microgravity. Genes (Basel) 12(3):337. https://doi.org/10.3390/genes12030337
Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18(8):2066–2073. https://doi.org/10.1093/emboj/18.8.2066
Masson PH (1995) Root gravitropism. BioEssays 17(2):119–127. https://doi.org/10.1002/bies.950170207
McQueen-Mason S, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4(11):1425–1433. https://doi.org/10.1105/tpc.4.11.1425
Meng Y, Chen F, Shuai H, Luo XF, Ding J, Tang SW, Xu SS, Liu JW, Liu WG, Du JB, Liu J, Yang F, Sun X, Yong TW, Wang XC, Feng Y, Shu K, Yang WY (2016) Karrikins delay soybean seed germination by mediating abscisic acid and gibberellin biogenesis under shaded conditions. Sci Rep 6:22073. https://doi.org/10.1038/srep22073
Mesland DA (1992) Mechanisms of gravity effects on cells: are there gravity-sensitive windows. Adv Space Biol Med 2:211–228. https://doi.org/10.1016/s1569-2574(08)60022-2
Miao ZQ, Zhao PX, Mao JL, Yu LH, Yuan Y, Tang H, Liu ZB, Xiang CB (2018) HOMEOBOX PROTEIN 52 mediates the crosstalk between ethylene and auxin signaling during primary root elongation by modulating auxin transport-related gene expression. Plant Cell 30(11):2761–2778. https://doi.org/10.1105/tpc.18.00584
Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem FV (2011) ROS signaling: the new wave? Trends Plant Sci 16(6):300–309. https://doi.org/10.1016/j.tplants.2011.03.007
Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–720. https://doi.org/10.1146/annurev.arplant.043008.092042
Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (2014) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17(23):6903–6911. https://doi.org/10.1093/emboj/17.23.6903
Muller L, Bennett M, French A, Wells DM, Swarup R (2018) Root gravitropism: quantification, challenges and solutions. Methods Mol Biol 1761:103–112. https://doi.org/10.1007/978-1-4939-7747-5_8
Nakamura M, Nishimura T, Morita MT (2019) Bridging the gap between amyloplasts and directional auxin transport in plant gravitropism. Curr Opin Plant Biol 52:54–60. https://doi.org/10.1016/j.pbi.2019.07.005
Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5(5):388–395. https://doi.org/10.1016/s1369-5266(02)00282-0
Němec B (1900) Über die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Ber Dtsch Bot Ges 18:241–245
Peer WA, Cheng Y, Murphy AS (2013) Evidence of oxidative attenuation of auxin signaling. J Exp Bot 64(9):2629–2639. https://doi.org/10.1093/jxb/ert152
Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406(6797):731–734. https://doi.org/10.1038/35021067
Perbal G (1999) Gravisensing in roots. Adv Space Res 24(6):723–729. https://doi.org/10.1016/s0273-1177(99)00405-6
Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119(3):849–858. https://doi.org/10.1104/pp.119.3.849
Richards DE, King KE, Tahar Aitali A, Harberd NP (2001) How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. Annu Rev Plant Physiol Plant Mol Biol 52:67–88. https://doi.org/10.1146/annurev.arplant.52.1.67
Richter P, Strauch SM, Lebert M (2019) Disproval of the starch-amyloplast hypothesis? Trends Plant Sci 24(4):291–293. https://doi.org/10.1016/j.tplants.2019.02.008
Sander D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:401–407. https://doi.org/10.1105/tpc.002899
Sato EM, Hijazi H, Bennett MJ, Vissenberg K, Swarup R (2015) New insights into root gravitropic signalling. J Exp Bot 66(8):2155–2165. https://doi.org/10.1093/jxb/eru515
Sengupta D, Reddy AR (2018) Simplifying the root dynamics: from complex hormone-environment interactions to specific root architectural modulation. Plant Growth Regul 85:337–349. https://doi.org/10.1007/s10725-018-0397-1
Sharma M, Singh D, Saksena HB, Sharma M, Tiwari A, Awasthi P, Botta HK, Shukla BN, Laxmi A (2021) Understanding the intricate web of phytohormone signaling in modulating root system architecture. Int J Mol Sci 22(11):5508. https://doi.org/10.3390/ijms22115508
Shu Y, Meng YJ, Shuai HW, Liu WG, Du GB, Liu J, Yang XY (2015) Dormancy and germination: how does the crop seed decide? Plant Biol (Stuttg) 17(6):1104–1112. https://doi.org/10.1111/plb.12356
Shu K, Zhou WG, Chen F, Luo XF, Yang WY (2018) Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Front Plant Sci 27(9):416
Šimášková M, O’Brien JA, Khan M, Noorden GV, Ötvös K, Vieten A, Clercq ID, Haperen GMAV, Cuesta C, Hoyerová K, Vanneste S, Marhavý P, Wabnik K, Breusegem FV, Nowack M, Murphy A, Friml J, Weijers D, Beeckman T, Benková E (2015) Cytokinin response factors regulate PIN-FORMED auxin transporters. Nat Commun 6:8717. https://doi.org/10.1038/ncomms9717
Su GX, Zhang WH, Liu YL (2006) Involvement of hydrogen peroxide generated by polyamine oxidative degradation in the development of lateral roots in soybean. J Integr Plant Biol 48(4):426–432
Su SH, Hijazi H, Gibbs NM, Jancewicz AL, Masson PH (2017) Molecular mechanisms of root gravitropism. Curr Biol 27(17):964–972. https://doi.org/10.1016/j.cub.2017.07.015
Swarup R, Bhosale R (2019) Developmental roles of AUX1/LAX auxin influx carriers in plants. Front Plant Sci 28(10):1306. https://doi.org/10.3389/fpls.2019.01306
Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15(20):2648–2653. https://doi.org/10.1101/gad.210501
Swarup R, Kargul J, Marchant A, Zadik D, Rahman A, Mills R, Yemm A, May S, Williams L, Millner P, Tsurumi S, Moore I, Napier R, Kerr ID, Bennett MJ (2004) Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1. Plant Cell 16(11):3069–3083. https://doi.org/10.1105/tpc.104.024737
Swarup R, Kramer EM, Perry P, Knox K, Leyser HMO, Haseloff J, Beemster GTS, Bhalerao R, Bennett MJ (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. https://doi.org/10.1038/ncb1316
Taylor I, Lehner K, McCaskey E, Nirmal N, Ozkan-Aydin Y, Murray-Cooper M, Jain R, Hawkes EW, Ronald PC, Goldman DI, Benfey PN (2021) Mechanism and function of root circumnutation. Proc Natl Acad Sci U S A 118(8):e2018940118. https://doi.org/10.1073/pnas.2018940118
Tian W, Wang C, Gao Q, Li L, Luan S (2020) Calcium spikes, waves and oscillations in plant development and biotic interactions. Nat Plants 6(7):750–759. https://doi.org/10.1038/s41477-020-0667-6
Toal TW, Ron M, Gibson D, Kajala K, Splitt B, Johnson LS, Miller ND, Slovak R, Gaudinier A, Patel R, Lucas MD, Provart NJ, Spalding EP, Busch W, Kliebenstein DJ, Brady SM (2018) Regulation of root angle and gravitropism. G3. (Bethesda) 8(12):3841–3855. https://doi.org/10.1534/g3.118.200540
Tong T, Li Q, Jiang W, Chen G, Xue DW, Deng FL, Zeng FR, Chen ZH (2021) Molecular evolution of calcium signaling and transport in plant adaptation to abiotic stress. Int J Mol Sci 22(22):12308. https://doi.org/10.3390/ijms222212308
Trevisan S, Forestan C, Brojanigo S, Quaggiotti S, Varotto S (2020) Brassinosteroid application affects the growth and gravitropic response of maize by regulating gene expression in the roots, shoots and leaves. Plant Growth Regul 92:117–130. https://doi.org/10.1007/s10725-020-00626-z
Utsuno K, Shikanai T, Yamada Y, Hashimoto T (1998) AGR, an agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol 39(10):1111–1118. https://doi.org/10.1093/oxfordjournals.pcp.a029310
Vitha S, Yang M, Sack F, Kiss JZ (2007) Gravitropism in starch-excess mutant of Arabidopsis thaliana. Am J Bot 94(4):590–598. https://doi.org/10.3732/ajb.94.4.590
Vivancos PD, Dong Y, Ziegler K, Markovic J, Pallardó FV, Pellny TK, Verrier PJ, Foyer CH (2010) Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J 64(5):825–838. https://doi.org/10.1111/j.1365-313X.2010.04371.x
Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345(6277):743–746. https://doi.org/10.1038/345743a0
Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (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 F, Chen ZH, Liu X, Colmer TD, Zhou M, Shabala S (2016) Tissue-specific root ion profiling reveals essential roles of the CAX and ACA calcium transport systems in response to hypoxia in Arabidopsis. J Exp Bot 67(12):3747–3762. https://doi.org/10.1093/jxb/erw034
Wang L, Sadeghnezhad E, Guan P, Gong P (2021) Review: microtubules monitor calcium and reactive oxygen species signatures in signal transduction. Plant Sci 304:110589. https://doi.org/10.1016/j.plantsci.2020.110589
Wang Y, Chen W, Ou Y, Zhu YY, Li J (2022a) Arabidopsis root elongation receptor kinases negatively regulate root growth putatively via altering cell wall remodeling gene expression. J Integr Plant Biol 64(8):1502–1513. https://doi.org/10.1111/jipb.13282
Wang HH, Ouyang QQ, Yang C, Zhang ZY, Hou DY, Liu H, Xu HW (2022b) Mutation of OsPIN1b by CRISPR/Cas9 reveals a role for auxin transport in modulating rice architecture and root gravitropism. Int J Mol Sci 23(16):8965. https://doi.org/10.3390/ijms23168965
Wayne R, Staves MP (1996) A down to earth model of gravisensing or Newton’s Law of Gravitation from the apple’s perspective. Physiol Plant 98(4):917–921
White PJ (2000) Calcium channels in higher plants. Biochim Biophys Acta 1465(1–2):171–189. https://doi.org/10.1016/s0005-2736(00)00137-1
White PJ, Bowen HC, Demidchik V, Nichols C, Davies JM (2002) Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochim Biophys Acta 1564(2):299–309. https://doi.org/10.1016/s0005-2736(02)00509-6
Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66(10):2839–2856. https://doi.org/10.1093/jxb/erv089
Yan ZQ, Wang DD, Cui HY, Sun YH, Yang XY, Jin H, Zhao YH, Li XZ, Xie M, Liu JK, Qin B (2018) Effects of artemisinin on root gravitropic response and root system development in Arabidopsis thaliana. Plant Growth Regul 85:211–220. https://doi.org/10.1007/s10725-018-0384-6
Yoshihara T, Spalding EP (2017) LAZY genes mediate the effects of gravity on auxin gradients and plant architecture. Plant Physiol 175(2):959–969. https://doi.org/10.1104/pp.17.00942
Yu ZP, Zhang F, Friml J, Ding ZJ (2022) Auxin signaling: research advances over the past 30 years. J Integr Plant Biol 64(2):371–392. https://doi.org/10.1111/jipb.13225
Zhang YZ, Friml J (2019a) Auxin guides roots to avoid obstacles during gravitropic growth. New Phytol 225(3):1049–1052. https://doi.org/10.1111/nph.16203
Zhang YZ, He P, Ma XF, Yang ZR, Pang CY, Yu JN, Wang JD, Friml J, Xiao GH (2019b) Auxin-mediated statolith production for root gravitropism. New Phytol 224(2):761–774. https://doi.org/10.1111/nph.15932
Zhang F, Li CL, Qu XZ, Liu JJ, Yu ZP, Wang JX, Zhu JY, Yu YQ, Ding ZJ (2022a) A feedback regulation between ARF7-mediated auxin signaling and auxin homeostasis involving MES17 affects plant gravitropism. J Integr Plant Biol 64(7):1339–1351. https://doi.org/10.1111/jipb.13268
Zhang H, Zhu JH, Gong ZZ, Zhu JK (2022b) Abiotic stress responses in plants. Nat Rev Genet 23(2):104–119. https://doi.org/10.1038/s41576-021-00413-0
Zhou L, Hou HZ, Yang T, Lian YK, Sun Y, Bian ZY, Wang CY (2018) Exogenous hydrogen peroxide inhibits primary root gravitropism by regulating auxin distribution during Arabidopsis seed germination. Plant Physiol Biochem 128:126–133. https://doi.org/10.1016/j.plaphy.2018.05.014
Funding
This study was financially supported by the Natural Science Fund Project of Gansu Province (21JR7RA822), Major special project in Gansu Province, (20ZD7NA007), National Green Fertilizer Industry Technology System (CARS-22-G-12), National Science Fund (31460382), China Agriculture Research System of MOF and MARA-Food Legumes (CARS-08), and the National Natural Science Foundation of China (32260483).
Author information
Authors and Affiliations
Contributions
SL, SM, QC and RW provided the study idea. RW completed the original draft of this paper. RW, LM, XL, LX, XF and YM performed the data collection. XZ and XY provided the idea reference. SL, SM, QC, LM and XL made the final revisions to the paper. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Communicated by Ben Zhang.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wei, R., Ma, L., Lu, X. et al. Research advances in plant root geotropism. Plant Growth Regul 102, 237–250 (2024). https://doi.org/10.1007/s10725-023-00992-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-023-00992-4