Arabidopsis thaliana; camalexin; iron deficiency; laser ablation ICP‐MS; metal transporter; root apical meristem; specialized metabolism; zinc
Abstract :
[en] Zinc (Zn) excess negatively impacts primary root growth in Arabidopsis thaliana. Yet, the effects of Zn excess on specific growth processes in the root tip (RT) remain largely unexplored. Transcriptomics, ionomics, and metabolomics were used to examine the specific impact of Zn excess on the RT compared with the remaining root (RR). Zn excess exposure resulted in a shortened root apical meristem and elongation zone, with differentiation initiating closer to the tip of the root. Zn accumulated at a lower concentration in the RT than in the RR. This pattern was associated with lower expression of Zn homeostasis and iron (Fe) deficiency response genes. A distinct distribution of Zn and Fe in RT and RR was highlighted by laser ablation inductively coupled plasma-mass spectrometry analysis. Specialized tryptophan (Trp)-derived metabolism genes, typically associated with redox and biotic stress responses, were specifically upregulated in the RT upon Zn excess, among those Phytoalexin Deficient 3 (PAD3) encoding the last enzyme of camalexin synthesis. In the roots of wild-type seedlings, camalexin concentration increased by sixfold upon Zn excess, and a pad3 mutant displayed increased Zn sensitivity and an altered ionome. Our results indicate that distinct redox and iron homeostasis mechanisms are key elements of the response to Zn excess in the RT.
Thiébaut, Noémie ✱; Université de Liège - ULiège > Département des sciences de la vie > Biologie végétale translationnelle ; Laboratory of Plant Physiology and Molecular Genetics, Université Libre de Bruxelles, B-1050, Brussels, Belgium ; Department of Plant and Environmental Sciences, University of Copenhagen, 1871, Frederiksberg, Denmark
Richtmann, Ludwig ✱; Laboratory of Plant Physiology and Molecular Genetics, Université Libre de Bruxelles, B-1050, Brussels, Belgium ; Department of Plant Physiology and Faculty of Life Sciences: Food, Nutrition and Health, University of Bayreuth, 95440, Bayreuth, Germany
Pergament Persson, Daniel ; Department of Plant and Environmental Sciences, University of Copenhagen, 1871, Frederiksberg, Denmark
Ranjan, Alok ; Laboratory of Plant Physiology and Molecular Genetics, Université Libre de Bruxelles, B-1050, Brussels, Belgium
Schloesser, Marie ; Université de Liège - ULiège > Département des sciences de la vie
Boutet, Stéphanie ; INRAE, AgroParisTech, Institute Jean-Pierre Bourgin for Plant Sciences (IJPB), Université Paris-Saclay, 78000, Versailles, France
Rezende, Lucas ; Hedera-22 SA, Boulevard du Rectorat 27b, B-4000, Liège, Belgium
Clemens, Stephan ; Department of Plant Physiology and Faculty of Life Sciences: Food, Nutrition and Health, University of Bayreuth, 95440, Bayreuth, Germany
Verbruggen, Nathalie ✱; Laboratory of Plant Physiology and Molecular Genetics, Université Libre de Bruxelles, B-1050, Brussels, Belgium
Hanikenne, Marc ✱; Université de Liège - ULiège > Integrative Biological Sciences (InBioS)
✱ These authors have contributed equally to this work.
Language :
English
Title :
Specific redox and iron homeostasis responses in the root tip of Arabidopsis upon zinc excess
Ahuja I, Kissen R, Bones AM. 2012. Phytoalexins in defense against pathogens. Trends in Plant Science 17: 73–90.
Amini S, Arsova B, Hanikenne M. 2022. The molecular basis of zinc homeostasis in cereals. Plant, Cell & Environment 45: 1339–1361.
Arrivault S, Senger T, Krämer U. 2006. The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. The Plant Journal 46: 861–879.
Assunção AGL, Herrero E, Lin YF, Huettel B, Talukdar S, Smaczniak C, Immink RGH, Van Eldik M, Fiers M, Schat H et al. 2010. Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency. Proceedings of the National Academy of Sciences of the United States of America 107: 10296–10301.
Barberon M. 2017. The endodermis as a checkpoint for nutrients. New Phytologist 213: 1604–1610.
Barberon M, Vermeer JEM, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE et al. 2016. Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164: 447–459.
Barco B, Kim Y, Clay NK. 2019. Expansion of a core regulon by transposable elements promotes Arabidopsis chemical diversity and pathogen defense. Nature Communications 10: 1–12.
Bechtold U, Field B. 2018. Molecular mechanisms controlling plant growth during abiotic stress. Journal of Experimental Botany 69: 2753–2758.
Boutet S, Barreda L, Perreau F, Totozafy JC, Mauve C, Gakière B, Delannoy E, Martin-Magniette ML, Monti A, Lepiniec L et al. 2022. Untargeted metabolomic analyses reveal the diversity and plasticity of the specialized metabolome in seeds of different Camelina sativa genotypes. The Plant Journal 110: 147–165.
Briat JF, Duc C, Ravet K, Gaymard F. 2010. Ferritins and iron storage in plants. Biochimica et Biophysica Acta – General Subjects 1800: 806–814.
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. Frontiers in Plant Science 8: 1–13.
Bruno L, Talarico E, Madeo Maria L, Muto A, Minervino M, Araniti F, Bitonti Maria B, Chiappetta A. 2021. Cadmium affects cell niches maintenance in Arabidopsis thaliana post-embryonic shoot and root apical meristem by altering the expression of WUS/WOX homolog genes and cytokinin accumulation. Plant Physiology and Biochemistry 167: 785–794.
Cabot C, Martos S, Llugany M, Gallego B, Tolrà R, Poschenrieder C. 2019. A role for zinc in plant defense against pathogens and herbivores. Frontiers in Plant Science 10: 1–15.
Cai G, Ahmed MA. 2022. The role of root hairs in water uptake: recent advances and future perspectives. Journal of Experimental Botany 73: 3330–3338.
Carrera D, Oddsson S, Grossmann J, Trachsel C, Streb S. 2018. Comparative proteomic analysis of plant acclimation to six different long-term environmental changes. Plant and Cell Physiology 59: 510–526.
Castaings L, Caquot A, Loubet S, Curie C. 2016. The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient metal provision. Scientific Reports 6: 1–11.
Castro B, Citterico M, Kimura S, Stevens DM, Wrzaczek M, Coaker G. 2021. Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nature Plants 7: 403–412.
Charlier JB, Polese C, Nouet C, Carnol M, Bosman B, Krämer U, Motte P, Hanikenne M. 2015. Zinc triggers a complex transcriptional and post-transcriptional regulation of the metal homeostasis gene FRD3 in Arabidopsis relatives. Journal of Experimental Botany 66: 3865–3878.
Chen Y, Zhang J. 2024. Multiple functions and regulatory networks of WRKY33 and its orthologs. Gene 931: 148899.
Clemens S. 2019. Metal ligands in micronutrient acquisition and homeostasis. Plant, Cell & Environment 42: 2902–2912.
Clemens S. 2022. The cell biology of zinc. Journal of Experimental Botany 73: 1688–1698.
Clemens S, Deinlein U, Ahmadi H, Höreth S, Uraguchi S. 2013. Nicotianamine is a major player in plant Zn homeostasis. Biometals 26: 623–632.
Clemens S, Weber M. 2016. The essential role of coumarin secretion for Fe acquisition from alkaline soil. Plant Signaling & Behavior 11: 1–6.
Colangelo EP, Lou GM. 2004. The essential basic helix–loop–helix protein FIT1 is required for the iron deficiency response. Plant Cell 16: 3400–3412.
Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P. 1999. Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. The Plant Journal 20: 503–508.
Cools T, Iantcheva A, Maes S, Van den Daele H, De Veylder L. 2010. A replication stress-induced synchronization method for Arabidopsis thaliana root meristems. The Plant Journal 64: 705–714.
Corso M, Schvartzman MS, Guzzo F, Souard F, Malkowski E, Hanikenne M, Verbruggen N. 2018. Contrasting cadmium resistance strategies in two metallicolous populations of Arabidopsis halleri. New Phytologist 218: 283–297.
Cui Y, Cao W, He Y, Zhao Q, Wakazaki M, Zhuang X, Gao J, Zeng Y, Gao C, Ding Y et al. 2019. A whole-cell electron tomography model of vacuole biogenesis in Arabidopsis root cells. Nature Plants 5: 95–105.
Cuypers A, Hendrix S, dos Reis RA, De Smet S, Deckers J, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J et al. 2016. Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Frontiers in Plant Science 7: 470.
De A, Hoang CV, Escudero V, Armas AM, Echavarri-Erasun C, González-Guerrero M, Jordá L. 2025. Combating plant diseases through transition metal allocation. New Phytologist 245: 1833–1842.
De Smet S, Cuypers A, Vangronsveld J, Remans T. 2015. Gene networks involved in hormonal control of root development in Arabidopsis thaliana: a framework for studying its disturbance by metal stress. International Journal of Molecular Sciences 16: 19195–19224.
Desbrosses-Fonrouge AG, Voigt K, Schröder A, Arrivault S, Thomine S, Krämer U. 2005. Arabidopsis thaliana MTP1 is a Zn transporter in the vacuolar membrane which mediates Zn detoxification and drives leaf Zn accumulation. FEBS Letters 579: 4165–4174.
van Dijk JR, Kranchev M, Blust R, Cuypers A, Vissenberg K. 2022. Arabidopsis root growth and development under metal exposure presented in an adverse outcome pathway framework. Plant, Cell & Environment 45: 737–750.
Fukao Y, Ferjani A, Tomioka R, Nagasaki N, Kurata R, Nishimori Y, Fujiwara M, Maeshima M. 2011. iTRAQ analysis reveals mechanisms of growth defects due to excess zinc in Arabidopsis. Plant Physiology 155: 1893–1907.
García-García JD, Girard L, Hernández G, Saavedra E, Pardo JP, Rodríguez-Zavala JS, Encalada R, Reyes-Prieto A, Mendoza-Cózatl DG, Moreno-Sánchez R. 2014. Zn-bis-glutathionate is the best co-substrate of the monomeric phytochelatin synthase from the photosynthetic heavy metal-hyperaccumulator Euglena gracilis. Metallomics 6: 604–616.
Genschik P, Marrocco K, Bach L, Noir S, Criqui MC. 2014. Selective protein degradation: a rheostat to modulate cell-cycle phase transitions. Journal of Experimental Botany 65: 2603–2615.
Giehl RFH, Flis P, Fuchs J, Gao Y, Salt DE, von Wirén N. 2023. Cell type-specific mapping of ion distribution in Arabidopsis thaliana roots. Nature Communications 14: 1–12.
Glawischnig E. 2007. Camalexin. Phytochemistry 68: 401–406.
Gollhofer J, Timofeev R, Lan P, Schmidt W, Buckhout TJ. 2014. Vacuolar-iron-transporter1-like proteins mediate iron homeostasis in Arabidopsis. PLoS ONE 9: e110468.
Gruber BD, Giehl RFH, Friedel S, von Wirén N. 2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163: 161–179.
Hanikenne M, Esteves SM, Fanara S, Rouached H. 2021. Coordinated homeostasis of essential mineral nutrients: a focus on iron. Journal of Experimental Botany 72: 2136–2153.
Haydon MJ, Kawachi M, Wirtz M, Hillmer S, Hell R, Krämer U. 2012. Vacuolar nicotianamine has critical and distinct roles under iron deficiency and for zinc sequestration in Arabidopsis. Plant Cell 24: 724–737.
He Y, Xu J, Wang X, He X, Wang Y, Zhou J, Zhang S, Meng X. 2019. The Arabidopsis pleiotropic drug resistance transporters PEN3 and PDR12 mediate camalexin secretion for resistance to Botrytis cinerea. Plant Cell 31: 2206–2222.
Henriques R, Jásik J, Klein M, Martinoia E, Feller U, Schell J, Pais MS, Koncz C. 2002. Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects. Plant Molecular Biology 50: 587–597.
Horák V, Tròka I, Stefl M. 1976. The influence of Zn2+ ions on the tryptophan biosynthesis in plants V. Biologia Plantarum 18: 393–396.
Inzé D, De Veylder L. 2006. Cell cycle regulation in plant development. Annual Review of Genetics 40: 77–105.
Kaiser S, Scheuring D. 2020. To lead or to follow: contribution of the plant vacuole to cell growth. Frontiers in Plant Science 11: 8–13.
Kaur H, Garg N. 2021. Zinc toxicity in plants: a review. Planta 253: 1–28.
Khare D, Choi H, Huh SU, Bassin B, Kim J, Martinoia E, Sohn KH, Paek KH, Lee Y, Chrispeels MJ. 2017. Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin. Proceedings of the National Academy of Sciences, USA 114: E5712–E5720.
Kimura S, Vaattovaara A, Ohshita T, Yokoyama K, Yoshida K, Hui A, Kaya H, Ozawa A, Kobayashi M, Mori IC et al. 2023. Zinc deficiency-induced defensin-like proteins are involved in the inhibition of root growth in Arabidopsis. The Plant Journal 115: 1071–1083.
Kobayashi T, Nozoye T, Nishizawa NK. 2019. Iron transport and its regulation in plants. Free Radical Biology and Medicine 133: 11–20.
Kondo Y, Tamaki T, Fukuda H. 2014. Regulation of xylem cell fate. Frontiers in Plant Science 5: 1–6.
Kumpf R, Thorstensen T, Rahman MA, Heyman J, Zeynep Nenseth H, Lammens T, Herrmann U, Swarup R, Veiseth SV, Emberland G et al. 2014. The ASH1-RELATED3 SET-domain protein controls cell division competence of the meristem and the quiescent center of the Arabidopsis primary root. Plant Physiology 166: 632–643.
Lee S, Lee J, Ricachenevsky FK, Punshon T, Tappero R, Salt DE, Lou GM. 2021. Redundant roles of four ZIP family members in zinc homeostasis and seed development in Arabidopsis thaliana. The Plant Journal 108: 1162–1173.
Leitner D, Klepsch S, Ptashnyk M, Marchant A, Kirk GJD, Schnepf A, Roose T. 2010. A dynamic model of nutrient uptake by root hairs. New Phytologist 185: 792–802.
Lešková A, Giehl RFH, Hartmann A, Fargašová A, von Wirén N. 2017. Heavy metals induce iron deficiency responses at different hierarchic and regulatory levels. Plant Physiology 174: 1648–1668.
Li B, Sun L, Huang J, Göschl C, Shi W, Chory J, Busch W. 2019. GSNOR provides plant tolerance to iron toxicity via preventing iron-dependent nitrosative and oxidative cytotoxicity. Nature Communications 10: 1–13.
Lilay GH, Thiébaut N, du Mee D, Assunção AGL, Schjoerring JK, Husted S, Persson DP. 2024. Linking the key physiological functions of essential micronutrients to their deficiency symptoms in plants. New Phytologist 242: 881–902.
Lin YF, Liang HM, Yang SY, Boch A, Clemens S, Chen CC, Wu JF, Huang JL, Yeh KC. 2009. Arabidopsis IRT3 is a zinc-regulated and plasma membrane localized zinc/iron transporter. New Phytologist 182: 392–404.
Loo DT, Rillema JR. 1998. Measurement of cell death. In: Mather JP, Barnes D, eds. Methods in cell biology, 251–264. Cambridge, MA, USA: Academic Press.
Malka SK, Cheng Y. 2017. Possible interactions between the biosynthetic pathways of indole glucosinolate and Auxin. Frontiers in Plant Science 8: 1–14.
Manasa K, Chitra V. 2020. Evaluation of in-vitro antioxidant activity of camalexin-a novel anti-Parkinson's agent. Research Journal of Pharmacy and Technology 13: 578–582.
Martos S, Gallego B, Cabot C, Llugany M, Barceló J, Poschenrieder C. 2016. Zinc triggers signaling mechanisms and defense responses promoting resistance to Alternaria brassicicola in Arabidopsis thaliana. Plant Science 249: 13–24.
Mase K, Tsukagoshi H. 2021. Reactive oxygen species link gene regulatory networks during Arabidopsis root development. Frontiers in Plant Science 12: 1–15.
Merlot S, Sanchez Garcia de LaTorre V, Hanikenne M. 2021. Physiology and molecular biology of trace element hyperaccumulation. In: van der Ent A, Baker AJM, Echevarria G, Simonnot M-O, and Morel JL, eds. Agromining: farming for metals, 155–182. Switzerland AG: Springer Nature.
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 Physiology 149: 894–904.
Mucha S, Heinzlmeir S, Kriechbaumer V, Strickland B, Kirchhelle C, Choudhary M, Kowalski N, Eichmann R, Hückelhoven R, Grill E et al. 2019. The formation of a camalexin biosynthetic metabolon. Plant Cell 31: 2697–2710.
Murgia I, Tarantino D, Soave C, Morandini P. 2011. Arabidopsis CYP82C4 expression is dependent on Fe availability and circadian rhythm, and correlates with genes involved in the early Fe deficiency response. Journal of Plant Physiology 168: 894–902.
Nguyen NN, Lamotte O, Alsulaiman M, Ruffel S, Krouk G, Berger N, Demolombe V, Nespoulous C, Dang TMN, Aimé S et al. 2023. Reduction in PLANT DEFENSIN 1 expression in Arabidopsis thaliana results in increased resistance to pathogens and zinc toxicity. Journal of Experimental Botany 74: 5374–5393.
Paffrath V, Tandron Moya YA, Weber G, von Wirén N, Giehl RFH. 2024. A major role of coumarin-dependent ferric iron reduction in strategy I-type iron acquisition in Arabidopsis. Plant Cell 36: 642–664.
Pastorczyk M, Kosaka A, Piślewska-Bednarek M, López G, Frerigmann H, Kułak K, Glawischnig E, Molina A, Takano Y, Bednarek P. 2020. The role of CYP71A12 monooxygenase in pathogen-triggered tryptophan metabolism and Arabidopsis immunity. New Phytologist 225: 400–412.
Perilli S, Sabatini S. 2010. Analysis of root meristem size development. Plant Developmental Biology: Methods and Protocols 655: 177–187.
Persson DP, Chen A, Aarts MGM, Salt DE, Schjoerring JK, Husted S. 2016. Multi-element bioimaging of Arabidopsis thaliana roots. Plant Physiology 172: 835–847.
Petersen K, Fiil BK, Mundy J, Petersen M. 2008. Downstream targets of WRKY33. Plant Signaling & Behavior 3: 1033–1034.
Rajniak J, Giehl RFH, Chang E, Murgia I, Von Wirén N, Sattely ES. 2018. Biosynthesis of redox-active metabolites in response to iron deficiency in plants. Nature Chemical Biology 14: 442–450.
Ravet K, Touraine B, Kim SA, Cellier F, Thomine S, Lou GM, Briat JF, Gaymard F. 2009. Post-translational regulation of AtFER2 ferritin in response to intracellular iron trafficking during fruit development in Arabidopsis. Molecular Plant 2: 1095–1106.
Remans T, Opdenakker K, Guisez Y, Carleer R, Schat H, Vangronsveld J, Cuypers A. 2012. Exposure of Arabidopsis thaliana to excess Zn reveals a Zn-specific oxidative stress signature. Environmental and Experimental Botany 84: 61–71.
Reyt G, Boudouf S, Boucherez J, Gaymard F, Briat JF. 2015. Iron- and ferritin-dependent reactive oxygen species distribution: impact on arabidopsis root system architecture. Molecular Plant 8: 439–453.
Riaz N, Lou GM. 2021. All together now: regulation of the iron deficiency response. Journal of Experimental Botany 72: 2045–2055.
Ricachenevsky FK, Menguer PK, Sperotto RA, Fett JP. 2015. Got to hide your Zn away: molecular control of Zn accumulation and biotechnological applications. Plant Science 236: 1–17.
Richtmann L, Thiebaut N, Sarthou M, Ranjan A, Boutet S, Hanikenne M, Verbruggen N, Clemens S. 2024. A multi-omics analysis of Arabidopsis thaliana root tips under Cd exposure: a role of HY5 in limiting accumulation. bioRxiv. doi: 10.1101/2024.08.29.609871.
Schaller GE, Bishopp A, Kieber JJ. 2015. The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27: 44–63.
Scheepers M, Spielmann J, Boulanger M, Carnol M, Bosman B, De Pauw E, Goormaghtigh E, Motte P, Hanikenne M. 2020. Intertwined metal homeostasis, oxidative and biotic stress responses in the Arabidopsis frd3 mutant. The Plant Journal 102: 34–52.
Schwarz B, Bauer P. 2020. FIT, a regulatory hub for iron deficiency and stress signaling in roots, and FIT-dependent and -independent gene signatures. Journal of Experimental Botany 71: 1694–1705.
Shahan R, Hsu CW, Nolan TM, Cole BJ, Taylor IW, Greenstreet L, Zhang S, Afanassiev A, Vlot AHC, Schiebinger G et al. 2022. A single-cell Arabidopsis root atlas reveals developmental trajectories in wild-type and cell identity mutants. Developmental Cell 57: 543–560.
Shanmugam V, Lo JC, Wu CL, Wang SL, Lai CC, Connolly EL, Huang JL, Yeh KC. 2011. Differential expression and regulation of iron-regulated metal transporters in Arabidopsis halleri and Arabidopsis thaliana – the role in zinc tolerance. New Phytologist 190: 125–137.
Sinclair SA, Krämer U. 2012. The zinc homeostasis network of land plants. BBA – Molecular Cell Research 1823: 1553–1567.
Sinclair SA, Senger T, Talke IN, Cobbett CS, Haydon MJ, Krämer U. 2018. Systemic upregulation of mtp2-and hma2-mediated Zn partitioning to the shoot supplements local Zn deficiency responses. Plant Cell 30: 2463–2479.
Sinclair SA, Sherson SM, Jarvis R, Camakaris J, Cobbett CS. 2007. The use of the zinc-fluorophore, Zinpyr-1, in the study of zinc homeostasis in Arabidopsis roots. New Phytologist 174: 39–45.
Sofo A, Bochicchio R, Amato M, Rendina N, Vitti A, Nuzzaci M, Altamura MM, Falasca G, Della Rovere F, Scopa A. 2017. Plant architecture, auxin homeostasis and phenol content in Arabidopsis thaliana grown in cadmium- and zinc-enriched media. Journal of Plant Physiology 216: 174–180.
Sofo A, Vitti A, Nuzzaci M, Tataranni G, Scopa A, Vangronsveld J, Remans T, Falasca G, Altamura MM, Degola F et al. 2013. Correlation between hormonal homeostasis and morphogenic responses in Arabidopsis thaliana seedlings growing in a Cd/Cu/Zn multi-pollution context. Physiologia Plantarum 149: 487–498.
Somssich M, Khan GA, Persson S. 2016. Cell wall heterogeneity in root development of Arabidopsis. Frontiers in Plant Science 7: 1–11.
Spielmann J, Cointry V, Devime F, Ravanel S, Neveu J, Vert G. 2022. Differential metal sensing and metal-dependent degradation of the broad spectrum root metal transporter IRT1. The Plant Journal 112: 1252–1265.
Spielmann J, Schloesser M, Hanikenne M. 2024. Reduced expression of bZIP19 and bZIP23 increases zinc and cadmium accumulation in Arabidopsis halleri. Plant, Cell & Environment 47: 2093–2108.
Spielmann J, Vert G. 2021. The many facets of protein ubiquitination and degradation in plant root iron-deficiency responses. Journal of Experimental Botany 72: 2071–2082.
Stanton C, Rodríguez-Celma J, Krämer U, Sanders D, Balk J. 2023. BRUTUS-LIKE (BTSL) E3 ligase-mediated fine-tuning of Fe regulation negatively affects Zn tolerance of Arabidopsis. Journal of Experimental Botany 74: 5767–5782.
Stanton C, Sanders D, Krämer U, Podar D. 2022. Zinc in plants: integrating homeostasis and biofortification. Molecular Plant 15: 65–85.
Stortenbeker N, Bemer M. 2019. The SAUR gene family: the plant's toolbox for adaptation of growth and development. Journal of Experimental Botany 70: 17–27.
Talke IN, Hanikenne M, Krämer U. 2006. Zinc-dependent global transcriptional control, transcriptional deregulation, and higher gene copy number for genes in metal homeostasis of the hyperaccumulator Arabidopsis halleri. Plant Physiology 142: 148–167.
Tennstedt P, Peisker D, Böttcher C, Trampczynska A, Clemens S. 2009. Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiology 149: 938–948.
Tewes LJ, Stolpe C, Kerim A, Krämer U, Müller C. 2018. Metal hyperaccumulation in the Brassicaceae species Arabidopsis halleri reduces camalexin induction after fungal pathogen attack. Environmental and Experimental Botany 153: 120–126.
Thiébaut N, Hanikenne M. 2022. Zinc deficiency responses: bridging the gap between Arabidopsis and dicotyledonous crops. Journal of Experimental Botany 73: 1699–1716.
Tsai HH, Rodríguez-Celma J, Lan P, Wu YC, Vélez-Bermúdez IC, Schmidt W. 2018. Scopoletin 8-hydroxylase-mediated fraxetin production is crucial for iron mobilization. Plant Physiology 177: 194–207.
Tsuji J, Jackson EP, Gage DA, Hammerschmidt R, Somerville SC. 1992. Phytoalexin accumulation in Arabidopsis thaliana during the hypersensitive reaction to Pseudomonas syringae pv syringae. Plant Physiology 98: 1304–1309.
Tsukagoshi H, Busch W, Benfey PN. 2010. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606–616.
Van De Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Van Themaat EVL, Koornneef M, Aarts MGM. 2006. Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiology 142: 1127–1147.
Vélez-Bermúdez IC, Schmidt W. 2023. Iron sensing in plants. Frontiers in Plant Science 14: 1–7.
Vert G, Barberon M, Zelazny E, Séguéla M, Briat JF, Curie C. 2009. Arabidopsis IRT2 cooperates with the high-affinity iron uptake system to maintain iron homeostasis in root epidermal cells. Planta 229: 1171–1179.
Vestenaa MW, Husted S, Minutello F, Persson DP. 2024. Endodermal suberin restricts root leakage of cesium: a suitable tracer for potassium. Physiologia Plantarum 176: 1–14.
Vik D, Mitarai N, Wulff N, Halkier BA, Burow M. 2018. Dynamic modeling of indole glucosinolate hydrolysis and its impact on auxin signaling. Frontiers in Plant Science 9: 1–16.
Wang J, Moeen-ud-din M, Yang S. 2021. Dose-dependent responses of Arabidopsis thaliana to zinc are mediated by auxin homeostasis and transport. Environmental and Experimental Botany 189: 104554.
Won SK, Lee YJ, Lee HY, Heo YK, Cho M, Cho HT. 2009. cis-element- and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. Plant Physiology 150: 1459–1473.
Yang W, Wightman R, Meyerowitz EM. 2017. Cell cycle control by nuclear sequestration of CDC20 and CDH1 mRNA in plant stem cells. Molecular Cell 68: 1108–1119.e3.
Yuan HM, Huang X. 2016. Inhibition of root meristem growth by cadmium involves nitric oxide-mediated repression of auxin accumulation and signalling in Arabidopsis. Plant, Cell & Environment 39: 120–135.
Zamioudis C, Korteland J, Van Pelt JA, Van Hamersveld M, Dombrowski N, Bai Y, Hanson J, Van Verk MC, Ling HQ, Schulze-Lefert P et al. 2015. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. The Plant Journal 84: 309–322.
Zhang P, Sun L, Qin J, Wan J, Wang R, Li S, Xu J. 2018. cGMP is involved in Zn tolerance through the modulation of auxin redistribution in root tips. Environmental and Experimental Botany 147: 22–30.
Zhong K, Zhang P, Wei X, Platre MP, He W, Zhang L, Małolepszy A, Cao M, Hu S, Tang S et al. 2024. Natural variation of TBR confers plant zinc toxicity tolerance through root cell wall pectin methylesterification. Nature Communications 15: 1–14.
Zluhan-Martínez E, López-Ruíz BA, García-Gómez ML, García-Ponce B, de la Paz Sánchez M, Álvarez-Buylla ER, Garay-Arroyo A. 2021. Integrative roles of phytohormones on cell proliferation, elongation and differentiation in the Arabidopsis thaliana primary root. Frontiers in Plant Science 12: 1–20.
