Abstract
Main conclusion
The review describes tissue-specific and non-cell autonomous molecular responses regulating the root system architecture and function in plants.
Abstract
Phenotypic plasticity of roots relies on specific molecular and tissue specific responses towards local and microscale heterogeneity in edaphic factors. Unlike gravitropism, hydrotropism in Arabidopsis is regulated by MIZU KUSSIE1 (MIZ1)-dependent asymmetric distribution of cytokinin and activation of Arabidopsis response regulators, ARR16 and ARR17 on the lower water potential side of the root leading to higher cell division and root bending. The cortex specific role of Abscisic acid (ABA)-activated SNF1-related protein kinase 2.2 (SnRK2.2) and MIZ1 in elongation zone is emerging for hydrotropic curvature. Halotropism involves clathrin-mediated internalization of PIN FORMED 2 (PIN2) proteins at the side facing higher salt concentration in the root tip, and ABA-activated SnRK2.6 mediated phosphorylation of cortical microtubule-associated protein Spiral2-like (SP2L) in the root transition zone, which results in anisotropic cell expansion and root bending away from higher salt. In hydropatterning, Indole-3-acetic acid 3 (IAA3) interacts with SUMOylated-ARF7 (Auxin response factor 7) and prevents expression of Lateral organ boundaries-domain 16 (LBD16) in air-side of the root, while on wet side of the root, IAA3 cannot repress the non-SUMOylated-ARF7 thereby leading to LBD16 expression and lateral root development. In root vasculature, ABA induces expression of microRNA165/microRNA166 in endodermis, which moves into the stele to target class III Homeodomain leucine zipper protein (HD-ZIP III) mRNA in non-cell autonomous manner. The bidirectional gradient of microRNA165/6 and HD-ZIP III mRNA regulates xylem patterning under stress. Understanding the tissue specific molecular mechanisms regulating the root responses under heterogeneous and stress environments will help in designing climate-resilient crops.
This is a preview of subscription content, log in via an institution to check access.
Data availability
Not applicable.
References
Antoni R, Gonzalez-Guzman M, Rodriguez L, Peirats-Llobet M, Pizzio GA, Fernandez MA, De Winne N, De Jaeger G, Dietrich D, Bennett MJ, Rodriguez PL (2013) PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiol 161(2):931–941. https://doi.org/10.1104/pp.112.208678
Ashraf MA, Rahman A (2019) Cold stress response in Arabidopsis thaliana is mediated by GNOM ARF-GEF. Plant J 97(3):500–516. https://doi.org/10.1111/tpj.14137
Ashraf MA, Umetsu K, Ponomarenko O, Saito M, Aslam M, Antipova O, Dolgova N, Kiani CD, Nehzati S, Tanoi K, Minegishi K, Nagatsu K, Kamiya T, Fujiwara T, Luschnig C, Tanino K, Pickering I, George GN, Rahman A (2020) PIN FORMED 2 modulates the transport of arsenite in Arabidopsis thaliana. Plant Commun 1(3):100009. https://doi.org/10.1016/j.xplc.2019.100009
Bao Y, Aggarwal P, Robbins NE, Sturrock CJ, Thompson MC, Tan HQ, Tham C, Duan L, Rodriguez PL, Vernoux T, Mooney SJ (2014) Plant roots use a patterning mechanism to position lateral root branches toward available water. Proc Natl Acad Sci USA 111(25):9319–9324. https://doi.org/10.1073/pnas.1400966111
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 114(24):E4884–E4893. https://doi.org/10.1073/pnas.1613499114
Bellstaedt J, Trenner J, Lippmann R, Poeschl Y, Zhang X, Friml J, Quint M, Delker C (2019) A mobile auxin signal connects temperature sensing in cotyledons with growth responses in hypocotyls. Plant Physiol 180(2):757–766. https://doi.org/10.1104/pp.18.01377
Bloch D, Puli MR, Mosquna A, Yalovsky S (2019) Abiotic stress modulates root patterning via ABA-regulated microRNA expression in the endodermis initials. Development 146(17):dev177097. https://doi.org/10.1242/dev.177097
Bradshaw AD (2006) Unravelling phenotypic plasticity–why should we bother? New Phytol 170(4):644–648. https://doi.org/10.1111/j.1469-8137.2006.01761.x
Brunetti P, Zanella L, De Paolis A, Di Litta D, Cecchetti V, Falasca G, Barbieri M, Altamura MM, Costantino P, Cardarelli M (2015) Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. J Exp Bot 66(13):3815–3829. https://doi.org/10.1093/jxb/erv185
Bruno L, Pacenza M, Forgione I, Lamerton LR, Greco M, Chiappetta A, Bitonti MB (2017) In Arabidopsis thaliana cadmium impact on the growth of primary root by altering SCR expression and auxin-cytokinin cross-talk. Front Plant Sci 8:1323. https://doi.org/10.3389/fpls.2017.01323
Burssens S, Himanen K, Van de Cotte B, Beeckman T, Van Montagu M, Inzé D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211(5):632–640. https://doi.org/10.1007/s004250000334
Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465(7296):316–321. https://doi.org/10.1038/nature08977
Casal JJ, Balasubramanian S (2019) Thermomorphogenesis. Ann Rev Plant Biol 70:321–346. https://doi.org/10.1146/annurev-arplant-050718-095919
Castrillo G, Sanchez-Bermejo E, de Lorenzo L, Crevillen P, Fraile-Escanciano A, Tc M, Mouriz A, Catarecha P, Sobrino-Plata J, Olsson S, Leo del Puerto Y, Mateos I, Rojo E, Hernandez LE, Jarillo JA, Pineiro M, Paz-Ares J, Leyva A (2013) WRKY6 transcription factor restricts arsenate uptake and transposon activation in Arabidopsis. Plant Cell 25(8):2944. https://doi.org/10.1105/tpc.113.114009
Chang J, Li X, Fu W, Wang J, Yong Y, Shi H, Ding Z, Kui H, Gou X, He K, Li J (2019) Asymmetric distribution of cytokinins determines root hydrotropism in Arabidopsis thaliana. Cell Res 29(12):984–993. https://doi.org/10.1038/s41422-019-0239-3
Chao D-Y, Chen Y, Chen J, Shi S, Chen Z, Wang C, Danku JM, Zhao F-J, Salt DE (2014) Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol 12:1002009. https://doi.org/10.1371/journal.pbio.1002009
Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45(2):437–448. https://doi.org/10.2135/cropsci2005.0437
Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12(10):444–451. https://doi.org/10.1016/j.tplants.2007.07.002
Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. Proc Natl Acad Sci USA 111(17):6497–6502. https://doi.org/10.1073/pnas.1319955111
Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512. https://doi.org/10.1146/annurev-arplant-043015-112301
Connolly EL, Fett JP, Guerinot ML (2002) Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14(6):1347–1357. https://doi.org/10.1105/tpc.001263
Conti L, Price G, O’Donnell E, Schwessinger B, Dominy P, Sadanandom A (2008) Small ubiquitin-like modifier proteases OVERLY TOLERANT TO SALT1 and -2 regulate salt stress responses in Arabidopsis. Plant Cell 20(8):2894–2908. https://doi.org/10.1105/tpc.108.058669
Dalal M, Sahu S, Tiwari S, Rao AR, Gaikwad K (2018) Transcriptome analysis reveals interplay between hormones, ROS metabolism and cell wall biosynthesis for drought-induced root growth in wheat. Plant Physiol Biochem 130:482–492. https://doi.org/10.1016/j.plaphy.2018.07.035
Dietrich D, Pang L, Kobayashi A, Fozard JA, Boudolf V, Bhosale R, Antoni R, Nguyen T, Hiratsuka S, Fujii N, Miyazawa Y (2017) Root hydrotropism is controlled via a cortex-specific growth mechanism. Nat Plants 3(6):17057. https://doi.org/10.1038/nplants.2017.57
Dowd TG, Braun DM, Sharp RE (2019) Maize lateral root developmental plasticity induced by mild water stress. I: genotypic variation across a high resolution series of water potentials. Plant Cell Environ 42(7):2259–2273. https://doi.org/10.1111/pce.13399
Dowd TG, Braun DM, Sharp RE (2020) Maize lateral root developmental plasticity induced by mild water stress. II: genotype-specific spatio-temporal effects on determinate development. Plant Cell Environ 43(10):2409–2427. https://doi.org/10.1111/pce.13840
Duan L, Dietrich D, Ng CH, Chan PM, Bhalerao R, Bennett MJ, Dinneny JR (2013) Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25(1):324–341. https://doi.org/10.1105/tpc.112.107227
Eapen D, Barroso ML, Campos ME, Ponce G, Corkidi G, Dubrovsky JG, Cassab GI (2003) A no hydrotropic response root mutant that responds positively to gravitropism in Arabidopsis. Plant Physiol 131(2):536–546. https://doi.org/10.1104/pp.011841
Fan JL, Wei XZ, Wan LC, Zhang LY, Zhao XQ, Liu WZ, Hao HQ, Zhang HY (2011) Disarrangement of actin filaments and Ca2+ gradient by CdCl2 alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking. J Plant Physiol 168(11):1157–1167. https://doi.org/10.1016/j.jplph.2011.01.031
Feng W, Lindner H, Robbins NE, Dinneny JR (2016) Growing out of stress: the role of cell-and organ-scale growth control in plant water-stress responses. Plant Cell 28(8):1769–1782. https://doi.org/10.1105/tpc.16.00182
Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu MC, Maman J, Steinhorst L, Schmitz-Thom I, Yvon R (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28(5):666–675. https://doi.org/10.1016/j.cub.2018.01.023
Feraru E, Feraru MI, Barbez E, Waidmann S, Sun L, Gaidora A, Kleine-Vehn J (2019) PILS6 is a temperature-sensitive regulator of nuclear auxin input and organ growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 116(9):3893–3898. https://doi.org/10.1073/pnas.1814015116
Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, Ye S, Yu P, Breen G, Cohen JD, Wigge PA (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108(50):20231–20235. https://doi.org/10.1073/pnas.1110682108
Fujii N, Miyabayashi S, Sugita T, Kobayashi A, Yamazaki C, Miyazawa Y, Kamada M, Kasahara H, Osada I, Shimazu T, Fusejima Y (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
Fusi R, Rosignoli S, Lou H, Sangiorgi G, Bovina R, Pattem JK, Borkar AN, Lombardi M, Forestan C, Milner SG, Davis JL (2022) Root angle is controlled by EGT1 in cereal crops employing an antigravitropic mechanism. Proc Natl Acad Sci USA 119(31):e2201350119. https://doi.org/10.1073/pnas.220135011
Galvan-Ampudia CS, Julkowska MM, Darwish E, Gandullo J, Korver RA, Brunoud G, Haring MA, Munnik T, Vernoux T, Testerink C (2013) Halotropism is a response of plant roots to avoid a saline environment. Curr Biol 23(20):2044–2050. https://doi.org/10.1016/j.cub.2013.08.042
Geng Y, Wu R, Wee CW, Xie F, Wei X, Chan PM, Tham C, Duan L, Dinneny JR (2013) A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25(6):2132–2154. https://doi.org/10.1105/tpc.113.112896
Geng D, Chen P, Shen X, Zhang Y, Li X, Jiang L, Xie Y, Niu C, Zhang J, Huang X, Ma F (2018) MdMYB88 and MdMYB124 enhance drought tolerance by modulating root vessels and cell walls in apple. Plant Physiol 178(3):1296–1309. https://doi.org/10.1104/pp.18.00502
Hanzawa T, Shibasaki K, Numata T, Kawamura Y, Gaude T, Rahman A (2013) Cellular auxin homeostasis under high temperature is regulated through a SORTING NEXIN1-dependent endosomal trafficking pathway. Plant Cell 25(9):3424–3433. https://doi.org/10.1105/tpc.113.115881
Haruta M, Gray WM, Sussman MR (2015) Regulation of the plasma membrane proton pump (H+-ATPase) by phosphorylation. Curr Opin Plant Biol 28:68–75. https://doi.org/10.1016/j.pbi.2015.09.005
Hong JH, Savina M, Du J, Devendran A, Ramakanth KK, Tian X, Sim WS, Mironova VV, Xu J (2017) A sacrifice-for-survival mechanism protects root stem cell niche from chilling stress. Cell 170(1):102–113. https://doi.org/10.1016/j.cell.2017.06.002
Huang BR, Taylor HM, McMichael BL (1991) Growth and development of seminal and crown roots of wheat seedlings as affected by temperature. Environ Exp Bot 31(4):471–477. https://doi.org/10.1016/0098-8472(91)90046-Q
Huang B, Rachmilevitch S, Xu J (2012) Root carbon and protein metabolism associated with heat tolerance. J Exp Bot 63(9):3455–3465. https://doi.org/10.1093/jxb/ers003
Huang G, Kilic A, Karady M, Zhang J, Mehra P, Song X, Sturrock CJ, Zhu W, Qin H, Hartman S, Schneider HM (2022) Ethylene inhibits rice root elongation in compacted soil via ABA-and auxin-mediated mechanisms. Proc Natl Acad Sci USA 119(30):e2201072119. https://doi.org/10.1073/pnas.2201072119
Hunter MC, Smith RG, Schipanski ME, Atwood LW, Mortensen DA (2017) Agriculture in 2050: recalibrating targets for sustainable intensification. Bioscience 67(4):386–391. https://doi.org/10.1093/biosci/bix010
Illston BG, Fiebrich CA (2017) Horizontal and vertical variability of observed soil temperatures. Geosci Data J 4(1):40–46. https://doi.org/10.1002/gdj3.47
Iwata S, Miyazawa Y, Takahashi H (2012) MIZU-KUSSEI1 plays an essential role in the hydrotropism of lateral roots in Arabidopsis thaliana. Environ Exp Bot 75:167–172. https://doi.org/10.1016/j.envexpbot.2011.09.007
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. https://doi.org/10.1093/aob/mct098
Jaffe MJ, Takahashi H, Biro RL (1985) A pea mutant for the study of hydrotropism in roots. Science 230(4724):445–447. https://doi.org/10.1126/science.230.4724.445
Ji R, Zhou L, Liu J, Wang Y, Yang L, Zheng Q, Zhang C, Zhang B, Ge H, Yang Y, Zhao F (2017) Calcium-dependent protein kinase CPK31 interacts with arsenic transporter AtNIP1; 1 and regulates arsenite uptake in Arabidopsis thaliana. PLoS One 12(3):e0173681. https://doi.org/10.1371/journal.pone.0173681
Jobe TO, Yu Q, Hauser F, Xie Q, Meng Y, Maassen T, Kopriva S, Schroeder JI (2021) The SLIM1 transcription factor is required for arsenic resistance in Arabidopsis thaliana. FEBS Lett 595(12):1696–1707. https://doi.org/10.1002/1873-3468.14096
Jones VA, Dolan L (2012) The evolution of root hairs and rhizoids. Ann Bot 110(2):205–212. https://doi.org/10.1093/aob/mcs136
Jupp AP, Newman EI (1987) Morphological and anatomical effects of severe drought on the roots of Lolium perenne L. New Phytol 105:393–402. https://doi.org/10.1111/j.1469-8137.1987.tb00876.x
Kamiya T, Islam R, Duan G, Uraguchi S, Fujiwara T (2013) Phosphate deficiency signaling pathway is a target of arsenate and phosphate transporter OsPT1 is involved in As accumulation in shoots of rice. Soil Sci Plant Nutr 59(4):580–590. https://doi.org/10.1080/00380768.2013.804390
Kaneyasu T, Kobayashi A, Nakayama M, Fujii N, Takahashi H, Miyazawa Y (2007) Auxin response, but not its polar transport, plays a role in hydrotropism of Arabidopsis roots. J Exp Bot 58(5):1143–1150. https://doi.org/10.1093/jxb/erl274
Kenrick P, Strullu-Derrien C (2014) The origin and early evolution of roots. Plant Physiol 166(2):570–580. https://doi.org/10.1104/pp.114.244517
Kirschner GK, Rosignoli S, Guo L, Vardanega I, Imani J, Altmüller J, Milner SG, Balzano R, Nagel KA, Pflugfelder D, Forestan C (2021) ENHANCED GRAVITROPISM 2 encodes a STERILE ALPHA MOTIF-containing protein that controls root growth angle in barley and wheat. Proc Natl Acad Sci USA 118(35):e2101526118. https://doi.org/10.1073/pnas.2101526118
Kitomi Y, Hanzawa E, Kuya N, Inoue H, Hara N, Kawai S, Kanno N, Endo M, Sugimoto K, Yamazaki T, Sakamoto S (2020) Root angle modifications by the DRO1 homolog improve rice yields in saline paddy fields. Proc Natl Acad Sci USA 117(35):21242–21250. https://doi.org/10.1073/pnas.2005911117
Kobayashi A, Takahashi A, Kakimoto Y, Miyazawa Y, Fujii N, Higashitani A, Takahashi H (2007) A gene essential for hydrotropism in roots. Proc Natl Acad Sci USA 104(11):4724–4729. https://doi.org/10.1073/pnas.0609929104
Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture requires the bHLH transcription factor PIF4. Curr Biol 19(5):408–413. https://doi.org/10.1016/j.cub.2009.01.046
Korenkov V, Park S, Cheng NH, Sreevidya C, Lachmansingh J, Morris J, Hirschi K, Wagner GJ (2007) Enhanced Cd 2+-selective root-tonoplast-transport in tobaccos expressing Arabidopsis cation exchangers. Planta 225:403–411. https://doi.org/10.1007/s00425-006-0352-7
Korver RA, van den Berg T, Meyer AJ, Galvan-Ampudia CS, Ten Tusscher KH, Testerink C (2020) Halotropism requires phospholipase Dζ1-mediated modulation of cellular polarity of auxin transport carriers. Plant Cell Environ 43(1):143–158. https://doi.org/10.1111/pce.13646
Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130(4):2129–2141. https://doi.org/10.1104/pp.008532
Krieger G, Shkolnik D, Miller G, Fromm H (2016) Reactive oxygen species tune root tropic responses. Plant Physiol 172(2):1209–1220. https://doi.org/10.1104/pp.16.00660
Lee S, Wang W, Huq E (2021) Spatial regulation of thermomorphogenesis by HY5 and PIF4 in Arabidopsis. Nat Commun 12(1):3656. https://doi.org/10.1038/s41467-021-24018-7
Li X, Chen L, Forde BG, Davies WJ (2017) The biphasic root growth response to abscisic acid in Arabidopsis involves interaction with ethylene and auxin signalling pathways. Front Plant Sci 8:1493. https://doi.org/10.3389/fpls.2017.01493
Li Y, Yuan W, Li L, Dai H, Dang X, Miao R, Baluška F, Kronzucker HJ, Lu C, Zhang J, Xu W (2020a) Comparative analysis reveals gravity is involved in the MIZ1-regulated root hydrotropism. J Exp Bot 71(22):7316–7330. https://doi.org/10.1093/jxb/eraa409
Li Y, Yuan W, Li L, Miao R, Dai H, Zhang J, Xu W (2020b) Light-dark modulates root hydrotropism associated with gravitropism by involving amyloplast response in Arabidopsis. Cell Rep 32(13):108198. https://doi.org/10.1016/j.celrep.2020.108198
Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez L, Merrin J, Chen J, Shabala L, Smet W, Ren H, Vanneste S, Shabala S, Rybel BD, Weijers D, Kinoshita T, Gray WM, Friml J (2021) Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature 599(7884):273–277. https://doi.org/10.1038/s41586-021-04037-6
Li L, Chen H, Alotaibi SS, Pěnčík A, Adamowski M, Novak O, Friml J (2022) RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis. Proc Natl Acad Sci USA 119(31):e2121058119. https://doi.org/10.1073/pnas.2121058119
Liu Y, Zhang Y, Wang Z, Guo S, Fang Y, Zhang Z, Gao H, Ren H, Wang C (2023) Plasma membrane-associated calcium signaling regulates arsenate tolerance in Arabidopsis. Plant Physiol 192(2):910–926. https://doi.org/10.1093/plphys/kiad171
Luo X, Chen Z, Gao J, Gong Z (2014) Abscisic acid inhibits root growth in Arabidopsis through ethylene biosynthesis. Plant J 79(1):44–55. https://doi.org/10.1111/tpj.12534
Luo JS, Huang J, Zeng DL, Peng JS, Zhang GB, Ma HL, Guan Y, Yi HY, Fu YL, Han B, Lin HX, Qian Q, Gong J-M (2018) A defensin-like protein drives cadmium efflux and allocation in rice. Nat Commun 9(1):645. https://doi.org/10.1038/s41467-018-03088-0
Luo H, Xu H, Chu C, He F, Fang S (2020) High temperature can change root system architecture and intensify root interactions of plant seedlings. Front Plant Sci 11:160. https://doi.org/10.3389/fpls.2020.00160
Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann Bot 112(2):347–357. https://doi.org/10.1093/aob/mcs293
Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S, Fujiwara T, Katsuhara M, Yano M (2007) An efflux transporter of silicon in rice. Nature 448:209–212. https://doi.org/10.1038/nature05964
Ma JF, Yamaji N, Mitani N, Xu X-Y, Su Y-H, Su Y-H, McGrath SP, Zhao F-J (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105:9931–9935. https://doi.org/10.1073/pnas.08023611
Martins S, Montiel-Jorda A, Cayrel A, Huguet S, Paysant-Le Roux C, Ljung K, Vert G (2017) Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature. Nat Commun 8(1):1–1. https://doi.org/10.1038/s41467-017-00355-4
Mbow C, Rosenzweig C, Barioni LG, Benton TG, Herrero M, Krishnapillai M et al (2019) Food security. In: Shukla PR, Skea J, Calvo BE, Masson-Delmotte V, Portner H-O, Roberts DC, Zhai P, Slade R, Connors S, van Diemen R, Ferrat M, Haughey E, Luz S, Neogi S, Pathak M, Petzold J, Portugal Pereira J, Vyas P, Huntley E, Kissick K, Malley BM, J, (eds) Climate change and land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems. IPCC, Geneva
McMichael BL, Burke JJ (1998) Soil Temperature and Root Growth. HortScience 33(6):947–951
Miao R, Wang M, Yuan W, Ren Y, Li Y, Zhang N, Zhang J, Kronzucker HJ, Xu W (2018) Comparative analysis of Arabidopsis ecotypes reveals a role for brassinosteroids in root hydrotropism. Plant Physiol 176(4):2720–2736. https://doi.org/10.1104/pp.17.01563
Miao R, Yuan W, Wang Y, Garcia-Maquilon I, Dang X, Li Y, Zhang J, Zhu Y, Rodriguez PL, Xu W (2021) Low ABA concentration promotes root growth and hydrotropism through relief of ABA INSENSITIVE 1-mediated inhibition of plasma membrane H+-ATPase 2. Sci Adv 7(12):eabd4113. https://doi.org/10.1126/sciadv.abd4113
Miyashima S, Koi S, Hashimoto T, Nakajima K (2011) Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138(11):2303–2313. https://doi.org/10.1242/dev.060491
Miyazawa Y, Takahashi A, Kobayashi A, Kaneyasu T, Fujii N, Takahashi H (2009) GNOM-mediated vesicular trafficking plays an essential role in hydrotropism of Arabidopsis roots. Plant Physiol 149(2):835–840. https://doi.org/10.1104/pp.108.131003
Miyazawa Y, Moriwaki T, Uchida M, Kobayashi A, Fujii N, Takahashi H (2012) Overexpression of MIZU-KUSSEI1 enhances the root hydrotropic response by retaining cell viability under hydrostimulated conditions in Arabidopsis thaliana. Plant Cell Physiol 53(11):1926–1933. https://doi.org/10.1093/pcp/pcs129
Morel M, Crouzet J, Gravot A, Auroy P, Leonhardt N, Vavasseur A, Richaud P (2009) AtHMA3, a P1B-ATPase allowing Cd/Zn/Co/Pb vacuolar storage in Arabidopsis. Plant Physiol 149(2):894–904. https://doi.org/10.1104/pp.108.130294
Moriwaki T, Miyazawa Y, Fujii N, Takahashi H (2012) Light and abscisic acid signalling are integrated by MIZ1 gene expression and regulate hydrotropic response in roots of Arabidopsis thaliana. Plant Cell Environ 35(8):1359–1368. https://doi.org/10.1111/j.1365-3040.2012.02493.x
Morohashi K, Okamoto M, Yamazaki C, Fujii N, Miyazawa Y, Kamada M, Kasahara H, Osada I, Shimazu T, Fusejima Y, Higashibata A (2017) Gravitropism interferes with hydrotropism via counteracting auxin dynamics in cucumber roots: clinorotation and spaceflight experiments. New Phytol 215(4):1476–1489. https://doi.org/10.1111/nph.14689
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167(3):645–663. https://doi.org/10.1111/j.1469-8137.2005.01487.x
Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413(6853):307–311. https://doi.org/10.1038/35095061
Nakajima Y, Nara Y, Kobayashi A, Sugita T, Miyazawa Y, Fujii N, Takahashi H (2017) Auxin transport and response requirements for root hydrotropism differ between plant species. J Exp Bot 68(13):3441–3456. https://doi.org/10.1093/jxb/erx193
Nakanishi H, Ogawa I, Ishimaru Y, Mori S, Nishizawa NK (2006) Iron deficiency enhances cadmium uptake and translocation mediated by the Fe 2+ transporters OsIRT1 and OsIRT2 in rice. Soil Sci Plant Nutr 52(4):464–469. https://doi.org/10.1111/j.1747-0765.2006.00055.x
Navarro C, Mateo-Elizalde C, Mohan TC, Sanchez-Bermejo E, Urrutia O, Fernandez-Muniz MN, Garcia-Mina JM, Munoz R, Paz-Ares J, Castrillo G, Leyva A (2021) Arsenite provides a selective signal that coordinates arsenate uptake and detoxification through the regulation of PHR1 stability in Arabidopsis. Mol Plant 14(9):1489–1507. https://doi.org/10.1016/j.molp.2021.05.020
Nishida S, Duan G, Ohkama-Ohtsu N, Uraguchi S, Fujiwara T (2016) Enhanced arsenic sensitivity with excess phytochelatin accumulation in shoots of a SULTR1; 2 knockout mutant of Arabidopsis thaliana (L.) Heynh. Soil Sci Plant Nutr 62(4):367–372. https://doi.org/10.1080/00380768.2016.1150790
Ogura T, Goeschl C, Filiault D, Mirea M, Slovak R, Wolhrab B, Satbhai SB, Busch W (2019) Root system depth in Arabidopsis is shaped by EXOCYST70A3 via the dynamic modulation of auxin transport. Cell 178(2):400–412. https://doi.org/10.1016/j.cell.2019.06.021
Okumura T, Nomoto Y, Kobayashi K, Suzuki T, Takatsuka H, Ito M (2021) MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana. J Plant Res 134(2):261–277. https://doi.org/10.1007/s10265-020-01250-8
Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19(1):118–130. https://doi.org/10.1105/tpc.106.047761
Orman-Ligeza B, Morris EC, Parizot B, Lavigne T, Babé A, Ligeza A, Klein S, Sturrock C, Xuan W, Novák O, Ljung K (2018) The xerobranching response represses lateral root formation when roots are not in contact with water. Curr Biol 28(19):3165–3173. https://doi.org/10.1016/j.cub.2018.07.074
Orosa-Puente B, Leftley N, von Wangenheim D, Banda J, Srivastava AK, Hill K, Truskina J, Bhosale R, Morris E, Srivastava M, Kümpers B (2018) Root branching toward water involves posttranslational modification of transcription factor ARF7. Science 362(6421):1407–1410. https://doi.org/10.1126/science.aau3956
Oyanagi A, Takahashi H, Suge H (1995) Interactions between hydrotropism and gravitropism in the primary seminal roots of Triticum eastivum L. Ann Bot 75(3):229–35. http://www.jstor.org/stable/42761706.
Pandey BK, Huang G, Bhosale R, Hartman S, Sturrock CJ, Jose L, Martin OC, Karady M, Voesenek LA, Ljung K, Lynch JP, Brown KM, Whalley WR, Mooney SJ, Zhang D, Bennett MJ (2021) Plant roots sense soil compaction through restricted ethylene diffusion. Science 371(6526):276–280. https://doi.org/10.1126/science.abf3013
Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y (2012) The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J 69(2):278–288. https://doi.org/10.1111/j.1365-313X.2011.04789.x
Pena LB, Barcia RA, Azpilicueta CE, Mendez AA, Gallego SM (2012) Oxidative post translational modifications of proteins related to cell cycle are involved in cadmium toxicity in wheat seedlings. Plant Sci 196:1–7. https://doi.org/10.1016/j.plantsci.2012.07.008
Ramachandran P, Wang G, Augstein F, de Vries J, Carlsbecker A (2018) Continuous root xylem formation and vascular acclimation to water deficit involves endodermal ABA signalling via miR165. Development 145(3):dev159202. https://doi.org/10.1242/dev.159202
Ramachandran P, Augstein F, Mazumdar S, Van Nguyen T, Minina EA, Melnyk CW, Carlsbecker A (2021) Abscisic acid signaling activates distinct VND transcription factors to promote xylem differentiation in Arabidopsis. Curr Biol 31(14):3153–3161. https://doi.org/10.1016/j.cub.2021.04.057
Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. J Exp Bot 52:381–401. https://doi.org/10.1093/jexbot/52.suppl_1.381
Rellan-Alvarez R, Lobet G, Lindner H, Pradier PL, Sebastian J, Yee MC, Geng Y, Trontin C, LaRue T, Schrager-Lavelle A, Haney CH (2015) GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems. Elife 4:e07597. https://doi.org/10.7554/eLife.07597
Robbins NE, Dinneny JR (2018) Growth is required for perception of water availability to pattern root branches in plants. Proc Natl Acad Sci 115(4):E822–E831. https://doi.org/10.1073/pnas.1710709115
Ronzan M, Piacentini D, Fattorini L, Della Rovere F, Eiche E, Riemann M, Altamura MM, Falasca G (2018) Cadmium and arsenic affect root development in Oryza sativa L. negatively interacting with auxin. Environ Exp Bot 151:64–75. https://doi.org/10.1016/j.envexpbot.2018.04.008
Rosales MA, Maurel C, Nacry P (2019) Abscisic acid coordinates dose-dependent developmental and hydraulic responses of roots to water deficit. Plant Physiol 180(4):2198–2211. https://doi.org/10.1104/pp.18.01546
Rosquete MR, Von Wangenheim D, Marhavý P, Barbez E, Stelzer EH, Benková E, Maizel A, Kleine-Vehn J (2013) An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Curr Biol 23(9):817–822. https://doi.org/10.1016/j.cub.2013.03.064
Roychoudhry S, Del Bianco M, Kieffer M, Kepinski S (2013) Auxin controls gravitropic setpoint angle in higher plant lateral branches. Curr Biol 23(15):1497–1504. https://doi.org/10.1016/j.cub.2013.06.034
Saab IN, Sharp RE, Pritchard J, Voetberg GS (1990) Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol 93(4):1329–1336. https://doi.org/10.1104/pp.93.4.1329
Sanchez-Bermejo E, Castrillo G, del Llano B, Navarro C, Zarco-Fern S (2014) Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. Nat Commun 5:4617. https://doi.org/10.1038/ncomms5617
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24(5):2155–2167. https://doi.org/10.1105/tpc.112.096925
Satoh-Nagasawa N, Mori M, Nakazawa N, Kawamoto T, Nagato Y, Sakurai K, Takahashi H, Watanabe A, Akagi H (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53:213–224. https://doi.org/10.1093/pcp/pcr166
Saucedo M, Ponce G, Campos ME, Eapen D, García E, Luján R, Sánchez Y, Cassab GI (2012) An altered hydrotropic response (ahr1) mutant of Arabidopsis recovers root hydrotropism with cytokinin. J Exp Bot 63(10):3587–3601. https://doi.org/10.1093/jxb/ers025
Schneider HM, Lynch JP (2020) Should root plasticity be a crop breeding target? Front Plant Sci 11:546. https://doi.org/10.3389/fpls.2020.00546
Seiler GJ (1998) Influence of temperature on primary and lateral root growth of sunflower seedlings. Environ Exp Bot 40(2):135–146. https://doi.org/10.1016/S0098-8472(98)00027-6
Seregin IV, Kozhevnikova AD (2023) Phytochelatins: sulfur-containing metal (loid)-chelating ligands in plants. Int J Mol Sci 24(3):2430. https://doi.org/10.3390/ijms24032430
Sharp RE, Silk WK, Hsiao TC (1988) Growth of the maize primary root at low water potentials: I. Spatial distribution of expansive growth. Plant Physiol 87(1):50–57. https://doi.org/10.1104/pp.87.1.50
Sharp RE, Wu Y, Voetberg GS, Saab IN, LeNoble ME (1994) Confirmation that abscisic acid accumulation is required for maize primary root elongation at low water potentials. J Exp Bot. https://doi.org/10.1093/jxb/45.Special_Issue.1743
Shelef O, Lazarovitch N, Rewald B, Golan-Goldhirsh A, Rachmilevitch S (2010) Root halotropism: salinity effects on Bassia indica root. Plant Biosyst 144(2):471–478. https://doi.org/10.1080/11263501003732001
Shi S, Wang T, Chen Z, Tang Z, Wu Z, Salt DE, Chao DY, Zhao FJ (2016) OsHAC1; 1 and OsHAC1; 2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiol 172(3):1708–1719. https://doi.org/10.1104/pp.16.01332
Shi Y, Ding Y, Yang S (2018) Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 23(7):623–637. https://doi.org/10.1016/j.tplants.2018.04.002
Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21(12):3823–3838. https://doi.org/10.1105/tpc.109.069906
Shin H, Shin H-S, Dewbre GR, Harrison MJ (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39:629–642. https://doi.org/10.1111/j.1365-313X.2004.02161.x
Shkolnik D, Krieger G, Nuriel R, Fromm H (2016) Hydrotropism: root bending does not require auxin redistribution. Mol Plant 9(5):757–759. https://doi.org/10.1016/j.molp.2016.02.001
Shkolnik D, Nuriel R, Bonza MC, Costa A, Fromm H (2018) MIZ1 regulates ECA1 to generate a slow, long-distance phloem-transmitted Ca 2+ signal essential for root water tracking in Arabidopsis. Proc Natl Acad Sci USA 115(31):8031–8036. https://doi.org/10.1073/pnas.1804130115
Song W-Y, Park J, Mendoza-Cozatl DG, Suter-Grotemeyer M, Shim D, Hortensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, Schroeder JI, Lee Y, Martinoia E (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci USA 107:21187–21192. https://doi.org/10.1073/pnas.1013964107
Song WY, Yamaki T, Yamaji N, Ko D, Jung K-H, Fujii-Kashino M, An G, Martinoia E, Lee Y, Ma JF (2014) A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci USA 111:15699–15704. https://doi.org/10.1073/pnas.1414968111
Spollen WG, LeNoble ME, Samuels TD, Bernstein N, Sharp RE (2000) Abscisic acid accumulation maintains maize primary root elongation at low water potentials by restricting ethylene production. Plant Physiol 122(3):967–976. https://doi.org/10.1104/pp.122.3.967
Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170(2):603–617. https://doi.org/10.1104/pp.15.01360
Stevenson JR, Villoria N, Byerlee D, Kelley T, Maredia M (2013) Green Revolution research saved an estimated 18 to 27 million hectares from being brought into agricultural production. Proc Natl Acad Sci USA 110(21):8363–8368. https://doi.org/10.1073/pnas.1208065110
Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5(12):537–542. https://doi.org/10.1016/S1360-1385(00)01797-0
Sun F, Zhang W, Hu H, Li B, Wang Y, Zhao Y, Li K, Liu M, Li X (2008) Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol 146(1):178–188. https://doi.org/10.1104/pp.107.109413
Sun L, Feraru E, Feraru MI, Waidmann S, Wang W, Passaia G, Wang ZY, Wabnik K, Kleine-Vehn J (2020) PIN-LIKES coordinate brassinosteroid signaling with nuclear auxin input in Arabidopsis thaliana. Curr Biol 30(9):1579-1588.e6. https://doi.org/10.1016/j.cub.2020.02.002
Suralta RR, Inukai Y, Yamauchi A (2008) Genotypic variations in responses of lateral root development to transient moisture stresses in rice cultivars. Plant Prod Sci 11(3):324–335. https://doi.org/10.1626/pps.11.324
Takahashi N, Goto N, Okada K, Takahashi H (2002) Hydrotropism in abscisic acid, wavy, and gravitropic mutants of Arabidopsis thaliana. Planta 216(2):203–211. https://doi.org/10.1007/s00425-002-0840-3
Takahashi R, Ishimaru Y, Senoura T, Shimo H, Ishikawa S, Arao T, Nakanishi H, Nishizawa NK (2011) The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J Exp Bot 62(14):4843–4850. https://doi.org/10.1093/jxb/err136
Takahashi N, Ogita N, Takahashi T, Taniguchi S, Tanaka M, Seki M, Umeda M (2019) A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis. Elife 8:e43944. https://doi.org/10.7554/eLife.43944
Tanaka-Takada N, Kobayashi A, Takahashi H, Kamiya T, Kinoshita T, Maeshima M (2019) Plasma membrane-associated Ca2+-binding protein PCaP1 is involved in root hydrotropism of Arabidopsis thaliana. Plant Cell Physiol 60(6):1331–1341. https://doi.org/10.1093/pcp/pcz042
Tang N, Shahzad Z, Lonjon F, Loudet O, Vailleau F, Maurel C (2018) Natural variation at XND1 impacts root hydraulics and trade-off for stress responses in Arabidopsis. Nat Commun 9(1):1–2. https://doi.org/10.1038/s41467-018-06430-8
Taniguchi YY, Taniguchi M, Tsuge T, Oka A, Aoyama T (2010) Involvement of Arabidopsis thaliana phospholipase Dζ2 in root hydrotropism through the suppression of root gravitropism. Planta 231(2):491. https://doi.org/10.1007/s00425-009-1052-x
Ueno D, Yamaji N, Kono I, Huang CF, Ando T, Yano M, Ma JF (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci 107(38):16500–16505. https://doi.org/10.1073/pnas.1005396107
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Kitomi Y, Inukai Y, Ono K, Kanno N, Inoue H (2013) Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet 45(9):1097–1102. https://doi.org/10.1038/ng.2725
van den Berg T, Korver RA, Testerink C, Ten Tusscher KH (2016) Modeling halotropism: a key role for root tip architecture and reflux loop remodeling in redistributing auxin. Development 143(18):3350–3362. https://doi.org/10.1242/dev.135111
Van der Weele CM, Spollen WG, Sharp RE, Baskin TI (2000) Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. J Exp Bot 51(350):1555–1562. https://doi.org/10.1093/jexbot/51.350.1555
Von Sachs J (1887) Lectures on the physiology of plants. H. M. Ward, Transl. Clarendon Press, Oxford
Voothuluru P, Sharp RE (2013) Apoplastic hydrogen peroxide in the growth zone of the maize primary root under water stress. I. Increased levels are specific to the apical region of growth maintenance. J Exp Bot 64(5):1223–1233. https://doi.org/10.1093/jxb/ers277
Voothuluru P, Makela P, Zhu J, Yamaguchi M, Cho IJ, Oliver MJ, Simmonds J, Sharp RE (2020) Apoplastic hydrogen peroxide in the growth zone of the maize primary root. Increased levels differentially modulate root elongation under well-watered and water-stressed conditions. Front Plant Sci 11:392. https://doi.org/10.3389/fpls.2020.00392
Wang P, Zhang W, Mao C, Xu G, Zhao FJ (2016a) The role of OsPT8 in arsenate uptake and varietal difference in arsenate tolerance in rice. J Exp Bot 67(21):6051–6059. https://doi.org/10.1093/jxb/erw362
Wang R, Zhang Y, Kieffer M, Yu H, Kepinski S, Estelle M (2016b) HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat Commun 7(1):1–1. https://doi.org/10.1038/ncomms10269
Wang FZ, Chen MX, Yu LJ, Xie LJ, Yuan LB, Qi H, Xiao M, Guo W, Chen Z, Yi K, Zhang J, Qiu R, Shu W, Xiao S, Chen Q-F (2017) OsARM1, an R2R3 MYB transcription factor, is involved in regulation of the response to arsenic stress in rice. Front Plant Sci 8:1868. https://doi.org/10.3389/fpls.2017.01868
Wang Y, Afeworki Y, Geng S, Kanchupati P, Gu M, Martins C, Rude B, Tefera H, Kim Y, Ge X, Auger D (2020) Hydrotropism in the primary roots of maize. New Phytol 226(6):1796–1808. https://doi.org/10.1111/nph.16472
Wang HQ, Xuan W, Huang XY, Mao C, Zhao FJ (2021) Cadmium inhibits lateral root emergence in rice by disrupting OsPIN-mediated auxin distribution and the protective effect of OsHMA3. Plant Cell Physiol 62(1):166–177. https://doi.org/10.1093/pcp/pcaa150
Wasson AP, Richards RA, Chatrath R, Misra SC, Prasad SS, Rebetzke GJ, Kirkegaard JA, Christopher J, Watt M (2012) Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J Exp Bot 63(9):3485–3498. https://doi.org/10.1093/jxb/ers111
West G, Inzé D, Beemster GT (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135(2):1050–1058. https://doi.org/10.1104/pp.104.040022
Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78. https://doi.org/10.1111/j.1469-8137.2008.02638.x
Wu Y, Cosgrove DJ (2000) Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins. J Exp Bot 51(350):1543–1553. https://doi.org/10.1093/jexbot/51.350.1543
Xu W, Jia L, Shi W, Liang J, Zhou F, Li Q, Zhang J (2013) Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. New Phytol 197(1):139–150. https://doi.org/10.1111/nph.12004
Xue Q, Zhu Z, Musick JT, Stewart BA, Dusek DA (2003) Root growth and water uptake in winter wheat under deficit irrigation. Plant Soil 257(1):151–161. https://doi.org/10.1023/A:1026230527597
Yamaguchi M, Valliyodan B, Zhang J, Lenoble ME, Yu O, Rogers EE, Nguyen HT, Sharp RE (2010) Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region-specific regulation of phenylpropanoid metabolism and control of free iron in the elongation zone. Plant Cell Environ 33(2):223–243. https://doi.org/10.1111/j.1365-3040.2009.02073.x
Yamazaki T, Miyazawa Y, Kobayashi A, Moriwaki T, Fujii N, Takahashi H (2012) MIZ1, an essential protein for root hydrotropism, is associated with the cytoplasmic face of the endoplasmic reticulum membrane in Arabidopsis root cells. FEBS Lett 586(4):398–402. https://doi.org/10.1016/j.febslet.2012.01.008
Yan H, Xu W, Xie J, Gao Y, Wu L, Sun L, Feng L, Chen X, Zhang T, Dai C, Li T, Lin X, Zhang Z, Wang X, Li F, Zhu X, Li J, Li Z, Chen C, Ma M, Zhang H, He Z (2019) Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat Commun 10(1):2562. https://doi.org/10.1038/s41467-019-10544-y
Yang G, Fu S, Huang J, Li L, Long Y, Wei Q, Wang Z, Chen Z, Xia J (2021) The tonoplast-localized transporter OsABCC9 is involved in cadmium tolerance and accumulation in rice. Plant Sci 307:110894. https://doi.org/10.1016/j.plantsci.2021.110894
Ye Y, Li P, Xu T, Zeng L, Cheng D, Yang M, Luo J, Lian X (2017) OsPT4 contributes to arsenate uptake and transport in rice. Front Plant Sci 8:2197. https://doi.org/10.3389/fpls.2017.02197
Yu B, Zheng W, Xing L, Zhu JK, Persson S, Zhao Y (2022) Root twisting drives halotropism via stress-induced microtubule reorientation. Dev Cell 57(20):2412–2425. https://doi.org/10.1016/j.devcel.2022.09.012
Zhang P, Wang R, Ju Q, Li W, Tran LS, Xu J (2019) The R2R3-MYB transcription factor MYB49 regulates cadmium accumulation. Plant Physiol 180(1):529–542. https://doi.org/10.1104/pp.18.01380
Zhao FJ, Ago Y, Mitani N, Li RY, Su YH, Yamaji N, McGrath SP, Ma JF (2010) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186(2):392–399. https://doi.org/10.1111/j.1469-8137.2010.03192.x
Zhao L, Wang P, Hou H, Zhang H, Wang Y, Yan S, Huang Y, Li H, Tan J, Hu A, Gao F (2014) Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS One 9(8):e106070. https://doi.org/10.1371/journal.pone.0106070
Zhu J, Zhang KX, Wang WS, Gong W, Liu WC, Chen HG, Xu HH, Lu YT (2015) Low temperature inhibits root growth by reducing auxin accumulation via ARR1/12. Plant Cell Physiol 56(4):727–736. https://doi.org/10.1093/pcp/pcu217
Acknowledgements
MD acknowledges funding support from Indian Council of Agricultural Research-National Institute for Plant Biotechnology (ICAR-NIPB) and Science and Engineering Research Board (SERB)-project (grant No: EMR/2016/007645), New Delhi.
Author information
Authors and Affiliations
Contributions
MD conceived the idea and prepared the outline, M and KM contributed primary draft for one section each, MD wrote rest of the sections, edited and revised the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Gerhard Leubner.
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
Dalal, M., Mansi & Mayandi, K. Zoom-in to molecular mechanisms underlying root growth and function under heterogeneous soil environment and abiotic stresses. Planta 258, 108 (2023). https://doi.org/10.1007/s00425-023-04262-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04262-5