Adaptation of Arabidopsis halleri to extreme metal pollution through limited metal accumulation involves changes in cell wall composition and metal homeostasis.
Corso, Massimiliano; An, Xinhui; Jones, Catherine Yvonneet al.
Arabidopsis; Cd exclusion; cell wall; ion transport; ionomic; metal homeostasis; transcriptomic
Abstract :
[en] Metallophytes constitute powerful models to study metal homeostasis, adaptation to extreme environments and the evolution of naturally-selected traits. Arabidopsis halleri is a pseudometallophyte which shows constitutive Zn/Cd tolerance and Zn hyperaccumulation but high intraspecific variability in Cd accumulation. To examine the molecular basis of the variation in metal tolerance and accumulation, ionome, transcriptome and cell-wall glycan array profiles were compared in two genetically close A. halleri populations from metalliferous and non-metalliferous sites in Northern Italy. The metallicolous population displayed increased tolerance to, reduced hyperaccumulation of Zn and limited accumulation of Cd, as well as altered metal homeostasis, compared to the non-metallicolous population. This correlated well with the differential expression of transporter genes involved in trace metal entry and in Cd/Zn vacuolar sequestration in roots. Many cell wall-related genes were also more expressed in roots of the metallicolous population. Glycan array and histological staining analyses supported major differences between the two populations in the accumulation of specific root pectins and hemicelluloses epitopes. Our results supported a role for specific cell wall components and regulation of transporter genes of Arabidopsis halleri in limiting accumulation of metals on contaminated sites.
Schvartzman Echenique, Maria Sol ; Université de Liège - ULiège > Département des sciences de la vie > Génomique fonctionnelle et imagerie moléculaire végétale
Malkowski, Eugeniusz; Plant Ecophysiology Team, Institute of Biology, Biotechnology and Environmental Protection ; Faculty of Natural Sciences, University of Silesia in Katowice, 40-032 Katowice, Poland
Willats, William G. T.; School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
Hanikenne, Marc ; Université de Liège - ULiège > Département des sciences de la vie > Génomique fonctionnelle et imagerie moléculaire végétale
Verbruggen, Nathalie; Laboratory of Plant Physiology and Molecular Genetics, Université Libre de Bruxelles, 1050 Brussels, Belgium
Language :
English
Title :
Adaptation of Arabidopsis halleri to extreme metal pollution through limited metal accumulation involves changes in cell wall composition and metal homeostasis.
Publication date :
2021
Journal title :
New Phytologist
ISSN :
0028-646X
eISSN :
1469-8137
Publisher :
Wiley, Oxford, United Kingdom
Volume :
230
Pages :
669-682
Peer reviewed :
Peer Reviewed verified by ORBi
Commentary :
This article is protected by copyright. All rights reserved.
Arnold PA, Kruuk LEB, Nicotra AB. 2019. How to analyse plant phenotypic plasticity in response to a changing climate. New Phytologist 222: 1235–1241.
Atmodjo MA, Hao Z, Mohnen D. 2013. Evolving views of pectin biosynthesis. Annual Review of Plant Biology 64: 747–779.
Babst-Kostecka A, Schat H, Saumitou-Laprade P, Grodzińska K, Bourceaux A, Pauwels M, Frérot H. 2018. Evolutionary dynamics of quantitative variation in an adaptive trait at the regional scale: the case of zinc hyperaccumulation in Arabidopsis halleri. Molecular Ecology 27: 3257–3273.
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.
Becher M, Talke IN, Krall L, Krämer U. 2004. Cross-species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. The Plant Journal 37: 251–268.
Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pagès F, Trajanoski Z, Galon J. 2009. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25: 1091–1093.
Blumenkrantz N, Asboe-Hansen G. 1973. New method for quantitative determination of uronic acids. Analytical Biochemistry 54: 484–489.
Broadley MR, White PJ, Hammond JP, Zelko I, Lux A. 2007. Zinc in plants. New Phytologist 173: 677–702.
Clemens S. 2006. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707–1719.
Clemens S. 2019. Metal ligands in micronutrient acquisition and homeostasis. Plant, Cell & Environment 42: 2902–2912.
Clemens S, Aarts MGM, Thomine S, Verbruggen N. 2013. Plant science: the key to preventing slow cadmium poisoning. Trends in Plant Science 18: 92–99.
Clemens S, Ma JF. 2016. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annual Review of Plant Biology 67: 489–512.
Cornu J-Y, Deinlein U, Hoereth S, Braun M, Schmidt H, Weber M, Persson DP, Husted S, Schjoerring JK, Clemens S. 2015. Contrasting effects of nicotianamine synthase knockdown on zinc and nickel tolerance and accumulation in the zinc/cadmium hyperaccumulator Arabidopsis halleri. New Phytologist 206: 738–750.
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.
Deinlein WU, Weber M, Schmidt H, Rensch S, Trampczynska A, Hansen TH, Husted S, Schjoerring JK, Talke IN, Krämer U et al. 2012. Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. The Plant Cell 24: 708–723.
Doblas VG, Geldner N, Barberon M. 2017. The endodermis, a tightly controlled barrier for nutrients. Current Opinion in Plant Biology 39: 136–143.
Dubeaux G, Neveu J, Zelazny E, Vert G. 2018. Metal sensing by the IRT1 transporter-receptor orchestrates its own degradation and plant metal nutrition. Molecular Cell 69: 953–964.e5.
Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F. 1951. A colorimetric method for the determination of sugars. Nature 168: 167.
Eren E, Argüello JM. 2004. Arabidopsis HMA2, a divalent heavy metal transporting PIB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiology 136: 3712–3723.
Fang X, Gui Z, Lei J, Jiang T, Liu Y, Li GX, Zheng SJ. 2012. Cell wall polysaccharides are involved in P-deficiency-induced Cd exclusion in Arabidopsis thaliana. Planta 236: 989–997.
Fasani E, DalCorso G, Varotto C, Li M, Visioli G, Mattarozzi M, Furini A. 2017. The MTP1 promoters from Arabidopsis halleri reveal cis-regulating elements for the evolution of metal tolerance. New Phytologist 214: 1614–1630.
Frérot H, Hautekèete N-C, Decombeix I, Bouchet M-H, Créach A, Saumitou-Laprade P, Piquot Y, Pauwels M. 2017. Habitat heterogeneity in the pseudometallophyte Arabidopsis halleri and its structuring effect on natural variation of zinc and cadmium hyperaccumulation. Plant and Soil 423: 157–174.
Gao F, Robe K, Gaymard F, Izquierdo E, Dubos C. 2019. The transcriptional control of iron homeostasis in plants: a tale of bHLH transcription factors? Frontiers in Plant Science 10: 6.
Gollhofer J, Timofeev R, Lan P, Schmidt W, Buckhout TJ, Kosman D, Eide D, Broderius M, Fett J, Guerinot M et al. 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.
Halimaa P, Blande D, Baltzi E, Aarts MGM, Granlund L, Keinänen M, Kärenlampi SO, Kozhevnikova AD, Peräniemi S, Schat H et al. 2019. Transcriptional effects of cadmium on iron homeostasis differ in calamine accessions of Noccaea caerulescens. The Plant Journal 97: 306–320.
Hanikenne M, Nouet C. 2011. Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Current Opinion in Plant Biology 14: 252–259.
Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Krämer U. 2008. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453: 391–395.
Hassinen V, Tervahauta A, Halimaa P, Plessl M, Peräniemi S, Schat H, Aarts M, Servomaa K, Kärenlampi S. 2007. Isolation of Zn-responsive genes from two accessions of the hyperaccumulator plant Thlaspi caerulescens. Planta 225: 977–989.
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. The Plant Cell 24: 724–737.
Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette M-LM, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J et al. 2006. Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88: 1751–1765.
Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, Salt DE. 2013. Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proceedings of the National Academy of Sciences, USA 110: 14498–14503.
Jan A, Azam M, Siddiqui K, Ali A, Choi I, Haq Q. 2015. Heavy metals and human health: mechanistic insight into toxicity and counter defense system of antioxidants. International Journal of Molecular Sciences 16: 29592–29630.
Karam MJ, Souleman D, Schvartzman MS, Gallina S, Spielmann J, Poncet C, Bouchez O, Pauwels M, Hanikenne M, Frérot H. 2019. Genetic architecture of a plant adaptive trait: QTL mapping of intraspecific variation for tolerance to metal pollution in Arabidopsis halleri. Heredity 122: 877–892.
Konlechner C, Türktaş M, Langer I, Vaculík M, Wenzel WW, Puschenreiter M, Hauser MT. 2013. Expression of zinc and cadmium responsive genes in leaves of willow (Salix caprea L.) genotypes with different accumulation characteristics. Environmental Pollution 178: 121–127.
Krämer U. 2010. Metal hyperaccumulation in plants. Annual Review of Plant Biology 61: 517–534.
Krzesłowska M. 2011. The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiologiae Plantarum 33: 35–51.
Lanquar V, Lelièvre F, Bolte S, Hamès C, Alcon C, Neumann D, Vansuyt G, Curie C, Schröder A, Krämer U et al. 2005. Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO Journal 24: 4041–4051.
Lee G, Quintana J, Ahmadi H, Syllwasschy L, Anderson JE, Pietzenuk B, Krämer U. 2019. Enhanced genome integrity maintenance and few large stress-mitigating changes in Arabidopsis halleri extreme-habitat local adaptation. bioRxiv: doi: 10.1101/859249.
Leskova A, Zvarĺk M, Araya T, Giehl RFH. 2019. Nickel toxicity targets cell wall-related processes and PIN2-mediated auxin transport to inhibit root elongation and gravitropic responses in Arabidopsis. Plant and Cell Physiology 61: 519–535.
Li T, Tao Q, Shohag MJI, Yang X, Sparks DL, Liang Y. 2015. Root cell wall polysaccharides are involved in cadmium hyperaccumulation in Sedum alfredii. Plant and Soil 389: 387–399.
Liu H, Zhao H, Wu L, Liu A, Zhao F-J, Xu W. 2017. Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytologist 215: 687–698.
Loix C, Huybrechts M, Vangronsveld J, Gielen M, Keunen E, Cuypers A. 2017. Reciprocal interactions between cadmium-induced cell wall responses and oxidative stress in plants. Frontiers in Plant Science 8: 1867.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 550.
Martinka M, Vaculık M, Lux A. 2014. Plant cell responses to cadmium and zinc. In: Nick P, Opatrny Z eds. Applied plant cell biology, plant cell monographs 22. Berlin/Heidelberg, Germany: Springer-Verlag, 209–246.
McCarthy DJ, Chen Y, Smyth GK. 2012. Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Research 40: 4288–4297.
Mei H, Cheng NH, Zhao J, Park S, Escareno RA, Pittman JK, Hirschi KD. 2009. Root development under metal stress in Arabidopsis thaliana requires the H+/cation antiporter CAX4. New Phytologist 183: 95–105.
Merlot S, de la Torre V, Hanikenne M. 2018. Physiology and molecular biology of trace element hyperaccumulation. In: der Ent A, Echevarria G, Baker AJM, Morel JL, eds. Agromining: farming for metals: extracting unconventional resources using plants. Cham: Springer International Publishing, 93–116.
Meyer CL, Juraniec M, Huguet S, Chaves-Rodriguez E, Salis P, Isaure M-P, Goormaghtigh E, Verbruggen N. 2015. Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. Journal of Experimental Botany 66: 3215–3227.
Meyer C-L, Pauwels M, Briset L, Godé C, Salis P, Bourceaux A, Souleman D, Frérot H, Verbruggen N. 2016. Potential preadaptation to anthropogenic pollution: evidence from a common quantitative trait locus for zinc and cadmium tolerance in metallicolous and nonmetallicolous accessions of Arabidopsis halleri. New Phytologist 212: 934–943.
Molins H, Mchelet L, Lanquar V, Agorio A, Giraudat J, Roach T, Krieger-Liszkay A, Thomine S. 2013. Mutants impaired in vacuolar metal mobilization identify chloroplasts as a target for cadmium hypersensitivity in Arabidopsis thaliana. Plant, Cell & Environment 36: 804–817.
Moller I, Marcus SE, Haeger A, Verhertbruggen Y, Verhoef R, Schols H, Ulvskov P, Dalgaard Mikkelsen J, Paul Knox J, Willats W. 2008. High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchical clustering of their carbohydrate microarray binding profiles. Glycoconjugate Journal 25: 37–48.
Moller I, Sørensen I, Bernal AJ, Blaukopf C, Lee K, Øbro J, Pettolino F, Roberts A, Mikkelsen JD, Knox JP et al. 2007. High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. The Plant Journal 50: 1118–1128.
Parrotta L, Guerriero G, Sergeant K, Cai G, Hausman J-F. 2015. Target or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity: differences in the response mechanisms. Frontiers in Plant Science 6: 133.
Pauwels M, Vekemans X, Godé C, Frérot H, Castric V, Saumitou-Laprade P. 2012. Nuclear and chloroplast DNA phylogeography reveals vicariance among European populations of the model species for the study of metal tolerance, Arabidopsis halleri (Brassicaceae). New Phytologist 193: 916–928.
Pellerin P, O’Neill MA. 1998. The interaction of the pectic polysaccharide Rhamnogalacturonan II with heavy metals and lanthanides in wines and fruit juices. Analusis Magazine 26: 32–36.
Peng J-S, Wang Y-J, Ma GDH-L, Zhang Y-J, Gong J-M. 2016. A pivotal role of cell wall in cadmium accumulation in the Crassulaceae hyperaccumulator Sedum plumbizincicola. Molecular Plant 10: 771–774.
Rabęda I, Bilski H, Mellerowicz EJ, Napieralska A, Suski S, Woźny A, Krzesłowska M. 2015. Colocalization of low-methylesterified pectins and Pb deposits in the apoplast of aspen roots exposed to lead. Environmental Pollution 205: 315–326.
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.
Robe K, Gao F, Lefebvre-legendre L, Sylvestre- E, Hem S, Rouhier N, Barberon M, Hecker A, Izquierdo E, Dubos C. 2021. Coumarin accumulation and trafficking in Arabidopsis thaliana: a complex and dynamic process. New Phytologist. 229: 2062–2079.
Roschzttardtz H, Séguéla-Arnaud M, Briat J-F, Vert G, Curie C. 2011. The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development. The Plant Cell 23: 2725–2737.
Satbhai SB, Setzer C, Freynschlag F, Slovak R, Kerdaffrec E, Busch W. 2017. Natural allelic variation of FRO2 modulates Arabidopsis root growth under iron deficiency. Nature Communications 8: 15603.
Schat H, Llugany M, Vooijs R, Hartley-Whitaker J, Bleeker PM. 2002. The role of phytochelatins in constitutive and adaptive heavy metal tolerances in hyperaccumulator and non-hyperaccumulator metallophytes. Journal of Experimental Botany 53: 2381–2392.
Schvartzman MS, Corso M, Fataftah N, Scheepers M, Nouet C, Bosman B, Carnol M, Motte P, Verbruggen N, Hanikenne M. 2018. Adaptation to high zinc depends on distinct mechanisms in metallicolous populations of Arabidopsis halleri. New Phytologist 218: 269–282.
Shi YZ, Zhu XF, Wan JX, Li GX, Zheng SJ. 2015. Glucose alleviates cadmium toxicity by increasing cadmium fixation in root cell wall and sequestration into vacuole in Arabidopsis. Journal of Integrative Plant Biology 57: 830–837.
Stein RJ, Stephan H, Rom J, De MF, Syllwasschy L, Lee G, Garbin L, Clemens S, Kr U. 2016. Relationships between soil and leaf mineral composition are element-specific, environment-dependent and geographically structured in the emerging model Arabidopsis halleri. New Phytologist 213: 1274–1286.
Stringlis IA, Yu K, Feussner K, de Jonge R, Van Bentum S, Van Verk MC, Berendsen RL, Bakker PAHM, Feussner I, Pieterse CMJ. 2018. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proceedings of the National Academy of Sciences, USA 115: E5213–E5222.
Su C, Jiang L, Zhang W. 2014. A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environmental Skeptics and Critics 3: 24–38.
Tao Q, Jupa R, Luo J, Lux A, Kováč J, Wen Y, Zhou Y, Jan J, Liang Y, Li T. 2017. The apoplasmic pathway via the root apex and lateral roots contributes to Cd hyperaccumulation in the hyperaccumulator Sedum alfredii. Journal of Experimental Botany 68: 739–751.
Tóth G, Hermann T, Da Silva MR, Montanarella L. 2016. Heavy metals in agricultural soils of the European Union with implications for food safety. Environment International 88: 299–309.
Tsednee M, Yang S-C, Lee D-C, Yeh K-C. 2014. Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability. Plant Physiology 166: 839–852.
Ursache R, Andersen TG, Marhavý P, Geldner N. 2018. A protocol for combining fluorescent proteins with histological stains for diverse cell wall components. The Plant Journal 93: 399–412.
Van De Mortel JE, Schat H, Moerland PD, Van Themaat EVL, Van Der Ent S, Blankestijn H, Ghandilyan A, Tsiatsiani S, Aarts MGM. 2008. Expression differences for genes involved in lignin, glutathione and sulphate metabolism in response to cadmium in Arabidopsis thaliana and the related Zn/Cd-hyperaccumulator Thlaspi caerulescens. Plant, Cell & Environment 31: 301–324.
Van De Mortel JE, Villanueva LA, Schat H, Kwekkeboom J, Coughlan S, Moerland PD, Ver E, Van Themaat L, 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.
Verbruggen N, Hermans C, Schat H. 2009. Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist 181: 759–776.
Verbruggen N, Juraniec M, Baliardini C, Meyer C-L. 2013. Tolerance to cadmium in plants: the special case of hyperaccumulators. BioMetals 26: 633–638.
Verhertbruggen Y, Marcus SE, Chen J, Knox JP. 2013. Cell wall pectic arabinans influence the mechanical properties of Arabidopsis thaliana inflorescence stems and their response to mechanical stress. Plant Cell Physiology 54: 1278–1288.
Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Lou GM, Briat J-F, Curie C. 2002. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. The Plant Cell 14: 1223–1233.
Wasowicz P, Pauwels M, Pasierbinski A, Przedpelska-Wasowicz EM, Babst-Kostecka AA, Saumitou-Laprade P, Rostanski A. 2016. Phylogeography of Arabidopsis halleri (Brassicaceae) in mountain regions of Central Europe inferred from cpDNA variation and ecological niche modelling. PeerJ 4: e1645.
Waters BM, Chu H-H, Didonato RJ, Roberts LA, Eisley RB, Lahner B, Salt DE, Walker EL. 2006. Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiology 141: 1446–1458.
Yapo BM. 2011. Pectin Rhamnogalacturonan II: on the ‘small stem with four branches’ in the primary cell walls of plants. International Journal of Carbohydrate Chemistry 2011: 1–11.
Zhong H, Lauchli A. 1993. Changes of cell wall composition and polymer size in primary roots of cotton seedlings under high salinity. Journal of Experimental Botany 44: 773–778.