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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

The barrier function of plant roots: biological bases for selective uptake and avoidance of soil compounds

Ramces De-Jesús-García A , Ulises Rosas https://orcid.org/0000-0001-5088-2679 B and Joseph G. Dubrovsky https://orcid.org/0000-0002-2072-4650 A C
+ Author Affiliations
- Author Affiliations

A Departamento de Biología Molecular de Plantas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenuenida Universidad 2001, Colonia Chamilpa, Cuernavaca, Morelos 62210, Mexico.

B Jardín Botánico, Instituto de Biología, Universidad Nacional Autónoma de México, 04510, CDMX, Mexico.

C Corresponding author. Email: jdubrov@ibt.unam.mx

Functional Plant Biology 47(5) 383-397 https://doi.org/10.1071/FP19144
Submitted: 24 May 2019  Accepted: 16 December 2019   Published: 26 March 2020

Abstract

The root is the main organ through which water and mineral nutrients enter the plant organism. In addition, root fulfils several other functions. Here, we propose that the root also performs the barrier function, which is essential not only for plant survival but for plant acclimation and adaptation to a constantly changing and heterogeneous soil environment. This function is related to selective uptake and avoidance of some soil compounds at the whole plant level. We review the toolkit of morpho-anatomical, structural, and other components that support this view. The components of the root structure involved in selectivity, permeability or barrier at a cellular, tissue, and organ level and their properties are discussed. In consideration of the arguments supporting barrier function of plant roots, evolutionary aspects of this function are also reviewed. Additionally, natural variation in selective root permeability is discussed which suggests that the barrier function is constantly evolving and is subject of natural selection.

Additional keywords: metal ions, natural variation, rhizosphere, root evolution, root function, selectivity.


References

Alassimone J, Naseer S, Geldner N (2010) A developmental framework for endodermal differentiation and polarity. Proceedings of the National Academy of Sciences of the United States of America 107, 5214–5219.
A developmental framework for endodermal differentiation and polarity.Crossref | GoogleScholarGoogle Scholar | 20142472PubMed |

Alassimone J, Fujita S, Doblas VG, van Dop M, Barberon M, Kalmbach L, Vermeer JE, Rojas-Murcia N, Santuari L, Hardtke CS (2016) Polarly localized kinase SGN1 is required for Casparian strip integrity and positioning. Nature Plants 2, 16113
Polarly localized kinase SGN1 is required for Casparian strip integrity and positioning.Crossref | GoogleScholarGoogle Scholar | 27455051PubMed |

Aleamotu’a M, Tai Y-T, McCurdy D, Collings D (2018) Developmental biology and induction of Phi thickenings by abiotic stress in roots of the Brassicaceae. Plants 7, 47
Developmental biology and induction of Phi thickenings by abiotic stress in roots of the Brassicaceae.Crossref | GoogleScholarGoogle Scholar |

Allan DL, Jarrell WM (1989) Proton and copper adsorption to maize and soybean root cell walls. Plant Physiology 89, 823–832.
Proton and copper adsorption to maize and soybean root cell walls.Crossref | GoogleScholarGoogle Scholar | 16666628PubMed |

Almeida P, Katschnig D, de Boer A (2013) HKT transporters – state of the art. International Journal of Molecular Sciences 14, 20359–20385.
HKT transporters – state of the art.Crossref | GoogleScholarGoogle Scholar | 24129173PubMed |

An D, Chen J-G, Gao Y-Q, Li X, Chao Z-F, Chen Z-R, Li Q-Q, Han M-L, Wang Y-L, Wang Y-F, Chao D-Y (2017) AtHKT1drives adaptation of Arabidopsis thaliana to salinity by reducing floral sodium content. PLOS Genetics 13, e1007086
AtHKT1drives adaptation of Arabidopsis thaliana to salinity by reducing floral sodium content.Crossref | GoogleScholarGoogle Scholar | 29084222PubMed |

Arnaud C, Bonnot C, Desnos T, Nussaume L (2010) The root cap at the forefront. Comptes Rendus Biologies 333, 335–343.
The root cap at the forefront.Crossref | GoogleScholarGoogle Scholar | 20371108PubMed |

Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant, Cell & Environment 32, 666–681.
Regulation and function of root exudates.Crossref | GoogleScholarGoogle Scholar |

Bailey PH, Currey JD, Fitter AH (2002) The role of root system architecture and root hairs in promoting anchorage against uprooting forces in Allium cepa and root mutants of Arabidopsis thaliana. Journal of Experimental Botany 53, 333–340.
The role of root system architecture and root hairs in promoting anchorage against uprooting forces in Allium cepa and root mutants of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 11807137PubMed |

Barber S, Walker J, Vasey EH (1963) Mechanisms for movement of plant nutrients from soil and fertilizer to plant root. Journal of Agricultural and Food Chemistry 11, 204–207.
Mechanisms for movement of plant nutrients from soil and fertilizer to plant root.Crossref | GoogleScholarGoogle Scholar |

Barberon M, Geldner N (2014) Radial transport of nutrients: the plant root as a polarized epithelium. Plant Physiology 166, 528–537.
Radial transport of nutrients: the plant root as a polarized epithelium.Crossref | GoogleScholarGoogle Scholar | 25136061PubMed |

Barberon M, Vermeer JEM, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164, 447–459.
Adaptation of root function by nutrient-induced plasticity of endodermal differentiation.Crossref | GoogleScholarGoogle Scholar | 26777403PubMed |

Barnabas AD, Peterson CA (1992) Development of Casparian bands and suberine lamellae in the endodermis of onion roots. Canadian Journal of Botany 70, 2233–2237.
Development of Casparian bands and suberine lamellae in the endodermis of onion roots.Crossref | GoogleScholarGoogle Scholar |

Baskin TI (2000) On the constancy of cell division rate in the root meristem. Plant Molecular Biology 43, 545–554.
On the constancy of cell division rate in the root meristem.Crossref | GoogleScholarGoogle Scholar | 11089859PubMed |

Baxter I, Hosmani PS, Rus A, Lahner B, Borevitz JO, Muthukumar B, Mickelbart MV, Schreiber L, Franke RB, Salt DE (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLOS Genetics 5, e1000492
Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19461889PubMed |

Baxter I, Brazelton JN, Yu D, Huang YS, Lahner B, Yakubova E, Li Y, Bergelson J, Borevitz JO, Nordborg M (2010) A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1; 1. PLOS Genetics 6, e1001193
A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1; 1.Crossref | GoogleScholarGoogle Scholar | 21085628PubMed |

Bell TL, Ojeda F (1999) Underground starch storage in Erica species of the Cape Floristic Region – differences between seeders and resprouters. New Phytologist 144, 143–152.
Underground starch storage in Erica species of the Cape Floristic Region – differences between seeders and resprouters.Crossref | GoogleScholarGoogle Scholar |

Bergelson J, Mittelstrass J, Horton MW (2019) Characterizing both bacteria and fungi improves understanding of the Arabidopsis root microbiome. Scientific Reports 9, 24
Characterizing both bacteria and fungi improves understanding of the Arabidopsis root microbiome.Crossref | GoogleScholarGoogle Scholar | 30631088PubMed |

Berger F, Hung CY, Dolan L, Schifelbein J (1998) Control of cell division in the root epidermis of Arabidopsis thaliana Developmental Biology 194, 235–245.
Control of cell division in the root epidermis of Arabidopsis thalianaCrossref | GoogleScholarGoogle Scholar | 9501025PubMed |

Berhin A, de Bellis D, Franke RB, Buono RA, Nowack MK, Nawrath C (2019) The root cap cuticle: a cell wall structure for seedling establishment and lateral root formation. Cell 176, 1367–1378.e8.
The root cap cuticle: a cell wall structure for seedling establishment and lateral root formation.Crossref | GoogleScholarGoogle Scholar | 30773319PubMed |

Blancaflor EB, Masson PH (2003) Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiology 133, 1677–1690.
Plant gravitropism. Unraveling the ups and downs of a complex process.Crossref | GoogleScholarGoogle Scholar | 14681531PubMed |

Brown JT (1975) Equisetum clarnoi, a new species based on petrifactions from the Eocene of Oregon. American Journal of Botany 62, 410–415.
Equisetum clarnoi, a new species based on petrifactions from the Eocene of Oregon.Crossref | GoogleScholarGoogle Scholar |

Campbell M, Bandillo N, Al Shiblawi FRA, Sharma S, Liu K, Du Q, Schmitz AJ, Zhang C, Véry AA, Lorenz AJ, Walia H (2017) Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content. PLoS Genetics 13, e1006823
Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content.Crossref | GoogleScholarGoogle Scholar | 28582424PubMed |

Canarini A, Wanek W, Merchant A, Richter A, Kaiser C (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Frontiers in Plant Science 10, 157
Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli.Crossref | GoogleScholarGoogle Scholar | 30881364PubMed |

Cardoso FB, Cambraia J, de Oliveira JA, Ribeiro C, de Souza LT, Braun H, DaMatta FM (2016) Aluminum-induced citric acid secretion is not the sole mechanism of Al-resistance in maize. Acta Physiologiae Plantarum 38, 279
Aluminum-induced citric acid secretion is not the sole mechanism of Al-resistance in maize.Crossref | GoogleScholarGoogle Scholar |

Cassab GI, Eapen D, Campos ME (2013) Root hydrotropism: an update. American Journal of Botany 100, 14–24.
Root hydrotropism: an update.Crossref | GoogleScholarGoogle Scholar | 23258371PubMed |

Channing A, Zamuner A, Edwards D, Guido D (2011) Equisetum thermale sp. nov.(Equisetales) from the Jurassic San Agustín hot spring deposit, Patagonia: anatomy, paleoecology, and inferred paleoecophysiology. American Journal of Botany 98, 680–697.
Equisetum thermale sp. nov.(Equisetales) from the Jurassic San Agustín hot spring deposit, Patagonia: anatomy, paleoecology, and inferred paleoecophysiology.Crossref | GoogleScholarGoogle Scholar | 21613167PubMed |

Chen Y-T, Wang Y, Yeh K-C (2017) Role of root exudates in metal acquisition and tolerance. Current Opinion in Plant Biology 39, 66–72.
Role of root exudates in metal acquisition and tolerance.Crossref | GoogleScholarGoogle Scholar | 28654805PubMed |

Clarkson D, Robards A, Stephens J, Stark M (1987) Suberin lamellae in the hypodermis of maize (Zea mays) roots; development and factors affecting the permeability of hypodermal layers. Plant, Cell & Environment 10, 83–93.
Suberin lamellae in the hypodermis of maize (Zea mays) roots; development and factors affecting the permeability of hypodermal layers.Crossref | GoogleScholarGoogle Scholar |

Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88, 1707–1719.
Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants.Crossref | GoogleScholarGoogle Scholar | 16914250PubMed |

Clowes FAL (2000) Pattern in root meristem development in angiosperms. New Phytologist 146, 83–94.
Pattern in root meristem development in angiosperms.Crossref | GoogleScholarGoogle Scholar |

Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiology 123, 825–832.
Phytochelatins and their roles in heavy metal detoxification.Crossref | GoogleScholarGoogle Scholar | 10889232PubMed |

Cointry V, Vert G (2019) The bifunctional transporter‐receptor IRT 1 at the heart of metal sensing and signaling. New Phytologist 223, 1173–1178.
The bifunctional transporter‐receptor IRT 1 at the heart of metal sensing and signaling.Crossref | GoogleScholarGoogle Scholar | 30929276PubMed |

Damus M, Peterson R, Enstone DE, Peterson CA (1997) Modifications of cortical cell walls in roots of seedless vascular plants. Botanica Acta 110, 190–195.
Modifications of cortical cell walls in roots of seedless vascular plants.Crossref | GoogleScholarGoogle Scholar |

Datta S, Kim CM, Pernas M, Pires ND, Proust H, Tam T, Vijayakumar P, Dolan L (2011) Root hairs: development, growth and evolution at the plant–soil interface. Plant and Soil 346, 1–14.
Root hairs: development, growth and evolution at the plant–soil interface.Crossref | GoogleScholarGoogle Scholar |

Deinlein U, Weber M, Schmidt H, Rensch S, Trampczynska A, Hansen TH, Husted S, Schjoerring JK, Talke IN, Krämer U (2012) Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation. The Plant Cell 24, 708–723.
Elevated nicotianamine levels in Arabidopsis halleri roots play a key role in zinc hyperaccumulation.Crossref | GoogleScholarGoogle Scholar | 22374395PubMed |

Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiology 103, 695–702.
Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices.Crossref | GoogleScholarGoogle Scholar | 12231973PubMed |

Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences of the United States of America 101, 15249–15254.
Engineering high-level aluminum tolerance in barley with the ALMT1 gene.Crossref | GoogleScholarGoogle Scholar | 15471989PubMed |

Demidchik V, Shabala S, Isayenkov S, Cuin TA, Pottosin I (2018) Calcium transport across plant membranes: mechanisms and functions. New Phytologist 220, 49–69.
Calcium transport across plant membranes: mechanisms and functions.Crossref | GoogleScholarGoogle Scholar | 29916203PubMed |

Diener AC, Gaxiola RA, Fink GR (2001) Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins. The Plant Cell 13, 1625–1638.
Arabidopsis ALF5, a multidrug efflux transporter gene family member, confers resistance to toxins.Crossref | GoogleScholarGoogle Scholar | 11449055PubMed |

Dilkes NB, Jones DL, Farrar J (2004) Temporal dynamics of carbon partitioning and rhizodeposition in wheat. Plant Physiology 134, 706–715.
Temporal dynamics of carbon partitioning and rhizodeposition in wheat.Crossref | GoogleScholarGoogle Scholar | 14764904PubMed |

Djikanović D, Kalauzi A, Jeremić M, Xu J, Mićić M, Whyte JD, Leblanc RM, Radotić K (2012) Interaction of the CdSe quantum dots with plant cell walls. Colloids and Surfaces. B, Biointerfaces 91, 41–47.
Interaction of the CdSe quantum dots with plant cell walls.Crossref | GoogleScholarGoogle Scholar | 22104400PubMed |

Doblas VG, Geldner N, Barberon M (2017a) The endodermis, a tightly controlled barrier for nutrients. Current Opinion in Plant Biology 39, 136–143.
The endodermis, a tightly controlled barrier for nutrients.Crossref | GoogleScholarGoogle Scholar | 28750257PubMed |

Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M, Madalinski M, Belkhadir Y, Geldner N (2017b) Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355, 280–284.
Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor.Crossref | GoogleScholarGoogle Scholar | 28104888PubMed |

Douchiche O, Soret-Morvan O, Chaïbi W, Morvan C, Paynel F (2010) Characteristics of cadmium tolerance in ‘Hermes’ flax seedlings: contribution of cell walls. Chemosphere 81, 1430–1436.
Characteristics of cadmium tolerance in ‘Hermes’ flax seedlings: contribution of cell walls.Crossref | GoogleScholarGoogle Scholar | 20884040PubMed |

Doussan C, Pierret A, Garrigues E, Pagès L (2006) Water uptake by plant roots: II – modelling of water transfer in the soil root-system with explicit account of flow within the root system – comparison with experiments. Plant and Soil 283, 99–117.
Water uptake by plant roots: II – modelling of water transfer in the soil root-system with explicit account of flow within the root system – comparison with experiments.Crossref | GoogleScholarGoogle Scholar |

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, 953–964e5.
Metal sensing by the IRT1 transporter-receptor orchestrates its own degradation and plant metal nutrition.Crossref | GoogleScholarGoogle Scholar | 29547723PubMed |

Dubrovsky JG, Rost TL (2012) Pericycle. In ‘eLS’. pp. 1–10. (John Wiley & Sons, Ltd: Chichester, UK)

Duque L, Villordon A (2019) Root branching and nutrient efficiency: status and way forward in root and tuber crops. Frontiers in Plant Science 10, 237
Root branching and nutrient efficiency: status and way forward in root and tuber crops.Crossref | GoogleScholarGoogle Scholar | 30886622PubMed |

Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant–soil system. Annual Review of Environment and Resources 30, 75–115.
Feedback in the plant–soil system.Crossref | GoogleScholarGoogle Scholar |

Eide D, Broderius M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proceedings of the National Academy of Sciences of the United States of America 93, 5624–5628.
A novel iron-regulated metal transporter from plants identified by functional expression in yeast.Crossref | GoogleScholarGoogle Scholar | 8643627PubMed |

Ennos AR, Fitter AH (1992) Comparative functional morphology of the anchorage systems of annual dicots. Functional Ecology 6, 71–78.
Comparative functional morphology of the anchorage systems of annual dicots.Crossref | GoogleScholarGoogle Scholar |

Enstone DE, Peterson CA, Ma F (2002) Root endodermis and exodermis: structure, function, and responses to the environment. Journal of Plant Growth Regulation 21, 335–351.
Root endodermis and exodermis: structure, function, and responses to the environment.Crossref | GoogleScholarGoogle Scholar |

Fasano JM, Swanson SJ, Blancaflor EB, Dowdb PE, Kaob T, Gilroya S (2001) Changes in root cap pH are required for the gravity response of the Arabidopsis root. The Plant Cell 13, 907–921.
Changes in root cap pH are required for the gravity response of the Arabidopsis root.Crossref | GoogleScholarGoogle Scholar | 11283344PubMed |

Fernandez‐Garcia N, Lopez‐Perez L, Hernandez M, Olmos E (2009) Role of phi cells and the endodermis under salt stress in Brassica oleracea. New Phytologist 181, 347–360.
Role of phi cells and the endodermis under salt stress in Brassica oleracea.Crossref | GoogleScholarGoogle Scholar | 19121032PubMed |

Fleck AT, Nye T, Repenning C, Stahl F, Zahn M, Schenk MK (2010) Silicon enhances suberization and lignification in roots of rice (Oryza sativa). Journal of Experimental Botany 62, 2001–2011.
Silicon enhances suberization and lignification in roots of rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 21172812PubMed |

Fleck AT, Schulze S, Hinrichs M, Specht A, Waßmann F, Schreiber L, Schenk MK (2015) Silicon promotes exodermal Casparian band formation in Si-accumulating and Si-excluding species by forming phenol complexes. PLoS One 10, e0138555
Silicon promotes exodermal Casparian band formation in Si-accumulating and Si-excluding species by forming phenol complexes.Crossref | GoogleScholarGoogle Scholar | 26383862PubMed |

Forde B, Lorenzo H (2001) The nutritional control of root development. Plant and Soil 232, 51–68.
The nutritional control of root development.Crossref | GoogleScholarGoogle Scholar |

Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant & Cell Physiology 48, 1081–1091.
An aluminum-activated citrate transporter in barley.Crossref | GoogleScholarGoogle Scholar |

Gao Y, Wang N, Li H, Hu X, Goikavi C (2015) Low-molecular-weight organic acids influence the sorption of phenanthrene by different soil particle size fractions. Journal of Environmental Quality 44, 219–227.
Low-molecular-weight organic acids influence the sorption of phenanthrene by different soil particle size fractions.Crossref | GoogleScholarGoogle Scholar | 25602337PubMed |

Ge L, Chen R (2016) Negative gravitropism in plant roots. Nature Plants 2, 16155
Negative gravitropism in plant roots.Crossref | GoogleScholarGoogle Scholar | 27748769PubMed |

Geldner N (2013) The endodermis. Annual Review of Plant Biology 64, 531–558.
The endodermis.Crossref | GoogleScholarGoogle Scholar | 23451777PubMed |

Gerrath JM, Matthes U, Purich M, Larson DW (2005) Root environmental effects on phi thickening production and root morphology in three gymnosperms. Canadian Journal of Botany 83, 379–385.
Root environmental effects on phi thickening production and root morphology in three gymnosperms.Crossref | GoogleScholarGoogle Scholar |

Giaquinta RT (1979) Sucrose translocation and storage in the sugar beet. Plant Physiology 63, 828–832.
Sucrose translocation and storage in the sugar beet.Crossref | GoogleScholarGoogle Scholar | 16660821PubMed |

Gilroy S, Jones DL (2000) Through form to functions: root hair development and nutrient uptake. Trends in Plant Science 5, 56–60.
Through form to functions: root hair development and nutrient uptake.Crossref | GoogleScholarGoogle Scholar | 10664614PubMed |

Gong H, Randall D, Flowers T (2006) Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow. Plant, Cell & Environment 29, 1970–1979.
Silicon deposition in the root reduces sodium uptake in rice (Oryza sativa L.) seedlings by reducing bypass flow.Crossref | GoogleScholarGoogle Scholar |

Gregory PJ (2006) Roots, rhizosphere and soil: the route to a better understanding of soil science? European Journal of Soil Science 57, 2–12.
Roots, rhizosphere and soil: the route to a better understanding of soil science?Crossref | GoogleScholarGoogle Scholar |

Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163, 161–179.
Plasticity of the Arabidopsis root system under nutrient deficiencies.Crossref | GoogleScholarGoogle Scholar | 23852440PubMed |

Guo X, Zhang S, Shan X-q (2008) Adsorption of metal ions on lignin. Journal of Hazardous Materials 151, 134–142.
Adsorption of metal ions on lignin.Crossref | GoogleScholarGoogle Scholar | 17587495PubMed |

Haas DL, Carothers ZB, Robbins RR (1976) Observations on the phi‐thickenings and Casparian strips in Pelargonium roots. American Journal of Botany 63, 863–867.
Observations on the phi‐thickenings and Casparian strips in Pelargonium roots.Crossref | GoogleScholarGoogle Scholar |

Hawes MC, Bengough G, Cassab G, Ponce G (2002) Root caps and rhizosphere. Journal of Plant Growth Regulation 21, 352–367.
Root caps and rhizosphere.Crossref | GoogleScholarGoogle Scholar |

Hedrich R (2012) Ion channels in plants. Physiological Reviews 92, 1777–1811.
Ion channels in plants.Crossref | GoogleScholarGoogle Scholar | 23073631PubMed |

Hetherington AJ, Dolan L (2018) Stepwise and independent origins of roots among land plants. Nature 561, 235–238.
Stepwise and independent origins of roots among land plants.Crossref | GoogleScholarGoogle Scholar | 30135586PubMed |

Hinrichs M, Fleck AT, Biedermann E, Ngo NS, Schreiber L, Schenk MK (2017) An ABC transporter is involved in the silicon-induced formation of Casparian bands in the exodermis of rice. Frontiers in Plant Science 8, 671
An ABC transporter is involved in the silicon-induced formation of Casparian bands in the exodermis of rice.Crossref | GoogleScholarGoogle Scholar | 28503184PubMed |

Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant and Soil 237, 173–195.
Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review.Crossref | GoogleScholarGoogle Scholar |

Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 162, 9–24.
The plastic plant: root responses to heterogeneous supplies of nutrients.Crossref | GoogleScholarGoogle Scholar |

Hoekenga OA, Maron LG, Piñeros MA, Cançado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 9738–9743.
AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 16740662PubMed |

Höfer R, Briesen I, Beck M, Pinot F, Schreiber L, Franke R (2008) The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid ω-hydroxylase involved in suberin monomer biosynthesis. Journal of Experimental Botany 59, 2347–2360.
The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid ω-hydroxylase involved in suberin monomer biosynthesis.Crossref | GoogleScholarGoogle Scholar | 18544608PubMed |

Hose E, Clarkson D, Steudle E, Schreiber L, Hartung W (2001) The exodermis: a variable apoplastic barrier. Journal of Experimental Botany 52, 2245–2264.
The exodermis: a variable apoplastic barrier.Crossref | GoogleScholarGoogle Scholar | 11709575PubMed |

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 of the United States of America 110, 14498–14503.
Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root.Crossref | GoogleScholarGoogle Scholar | 23940370PubMed |

Hou X, Yu M, Liu A, Wang X, Li Y, Liu J, Schnoor JL, Jiang G (2019) Glycosylation of tetrabromobisphenol A in pumpkin. Environmental Science & Technology 53, 8805–8812.
Glycosylation of tetrabromobisphenol A in pumpkin.Crossref | GoogleScholarGoogle Scholar |

Huynh K, Banach E, Reinhold D (2018) Transformation, conjugation and sequestration following the uptake of triclocarban by jalapeno pepper plants. Journal of Agricultural and Food Chemistry 66, 4032–4043.
Transformation, conjugation and sequestration following the uptake of triclocarban by jalapeno pepper plants.Crossref | GoogleScholarGoogle Scholar | 29637774PubMed |

Iannucci A, Fragasso M, Beleggia R, Nigro F, Papa R (2017) Evolution of the crop rhizosphere: impact of domestication on root exudates in tetraploid wheat (Triticum turgidum L.). Frontiers in Plant Science 8, 2124
Evolution of the crop rhizosphere: impact of domestication on root exudates in tetraploid wheat (Triticum turgidum L.).Crossref | GoogleScholarGoogle Scholar | 29326736PubMed |

Iijima MORI, Higuchi TOSH, Barlow PW (2004) Contribution of root cap mucilage and presence of an intact root cap in maize (Zea mays) to the reduction of soil mechanical impedance. Annals of Botany 94, 473–477.
Contribution of root cap mucilage and presence of an intact root cap in maize (Zea mays) to the reduction of soil mechanical impedance.Crossref | GoogleScholarGoogle Scholar |

Isaure M-P, Huguet S, Meyer C-L, Castillo-Michel H, Testemale D, Vantelon D, Saumitou-Laprade P, Verbruggen N, Sarret G (2015) Evidence of various mechanisms of Cd sequestration in the hyperaccumulator Arabidopsis halleri, the non-accumulator Arabidopsis lyrata, and their progenies by combined synchrotron-based techniques. Journal of Experimental Botany 66, 3201–3214.
Evidence of various mechanisms of Cd sequestration in the hyperaccumulator Arabidopsis halleri, the non-accumulator Arabidopsis lyrata, and their progenies by combined synchrotron-based techniques.Crossref | GoogleScholarGoogle Scholar | 25873676PubMed |

Ivanov V (1981) Cellular basis of root growth Soviet scientific reviews. Section D. Biology Reviews 2, 365–392.

Ivanov VB, Dubrovsky JG (2013) Longitudinal zonation pattern in plant roots: conflicts and solutions. Trends in Plant Science 18, 237–243.
Longitudinal zonation pattern in plant roots: conflicts and solutions.Crossref | GoogleScholarGoogle Scholar | 23123304PubMed |

Jones VAS, Dolan L (2012) The evolution of root hairs and rhizoids. Annals of Botany 110, 205–212.
The evolution of root hairs and rhizoids.Crossref | GoogleScholarGoogle Scholar |

Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant and Soil 321, 5–33.
Carbon flow in the rhizosphere: carbon trading at the soil–root interface.Crossref | GoogleScholarGoogle Scholar |

Julkowska MM, Koevoets IT, Mol S, Hoefsloot H, Feron R, Tester MA, Keurentjes JJ, Korte A, Haring MA, de Boer G-J (2017) Genetic components of root architecture remodeling in response to salt stress. The Plant Cell 29, 3198–3213.
Genetic components of root architecture remodeling in response to salt stress.Crossref | GoogleScholarGoogle Scholar | 29114015PubMed |

Kawasaki A, Donn S, Ryan PR, Mathesius U, Devilla R, Jones A, Watt M (2016) Microbiome and exudates of the root and rhizosphere of Brachypodium distachyon, a model for wheat. PLoS One 11, e0164533
Microbiome and exudates of the root and rhizosphere of Brachypodium distachyon, a model for wheat.Crossref | GoogleScholarGoogle Scholar | 27727301PubMed |

Kenrick P (2013) The origin of roots. In ‘Plant roots: the hidden half’, 4th edn. (Eds A Eshel, T Beeckman) pp. 1–14. (CRC Press: Boca Raton, FL, USA)

Kenrick P, Strullu-Derrien C (2014) The origin and early evolution of roots. Plant Physiology 166, 570–580.
The origin and early evolution of roots.Crossref | GoogleScholarGoogle Scholar | 25187527PubMed |

Kerkeb L, Krämer U (2003) The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea. Plant Physiology 131, 716–724.
The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea.Crossref | GoogleScholarGoogle Scholar | 12586895PubMed |

Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y (2007) The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. The Plant Journal 50, 207–218.
The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance.Crossref | GoogleScholarGoogle Scholar | 17355438PubMed |

Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annual Review of Plant Biology 46, 237–260.
Cellular mechanisms of aluminum toxicity and resistance in plants.Crossref | GoogleScholarGoogle Scholar |

Kochian LV, Hoekenga OA, Pineros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Review of Plant Biology 55, 459–493.
How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency.Crossref | GoogleScholarGoogle Scholar | 15377228PubMed |

Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annual Review of Plant Biology 66, 571–598.
Plant adaptation to acid soils: the molecular basis for crop aluminum resistance.Crossref | GoogleScholarGoogle Scholar | 25621514PubMed |

Kollmeier M, Dietrich P, Bauer CS, Horst WJ, Hedrich R (2001) Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar. Plant Physiology 126, 397–410.
Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar.Crossref | GoogleScholarGoogle Scholar | 11351102PubMed |

Kramer PJ (1932) The absorption of water by root systems of plants. American Journal of Botany 19, 148–164.
The absorption of water by root systems of plants.Crossref | GoogleScholarGoogle Scholar |

Krishnamurthy P, Ranathunge K, Franke R, Prakash H, Schreiber L, Mathew M (2009) The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.). Planta 230, 119–134.
The role of root apoplastic transport barriers in salt tolerance of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 19363620PubMed |

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.
The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy.Crossref | GoogleScholarGoogle Scholar |

Lee Y, Rubio MC, Alassimone J, Geldner N (2013) A mechanism for localized lignin deposition in the endodermis. Cell 153, 402–412.
A mechanism for localized lignin deposition in the endodermis.Crossref | GoogleScholarGoogle Scholar | 23541512PubMed |

Lee H-J, Ha J-H, Kim S-G, Choi H-K, Kim ZH, Han Y-J, Kim J-I, Oh Y, Fragoso V, Shin K (2016) Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots. Science Signaling 9, ra106
Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots.Crossref | GoogleScholarGoogle Scholar | 27803284PubMed |

Li B, Kamiya T, Kalmbach L, Yamagami M, Yamaguchi K, Shigenobu S, Sawa S, Danku JM, Salt DE, Geldner N (2017) Role of LOTR1 in nutrient transport through organization of spatial distribution of root endodermal barriers. Current Biology 27, 758–765.
Role of LOTR1 in nutrient transport through organization of spatial distribution of root endodermal barriers.Crossref | GoogleScholarGoogle Scholar | 28238658PubMed |

Li GZ, Wang ZQ, Yokosho K, Ding B, Fan W, Gong QQ, Li GX, Wu YR, Yang JL, Ma JF (2018) Transcription factor WRKY 22 promotes aluminum tolerance via activation of OsFRDL 4 expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytologist 219, 149–162.
Transcription factor WRKY 22 promotes aluminum tolerance via activation of OsFRDL 4 expression and enhancement of citrate secretion in rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 29658118PubMed |

Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010) Root hair systems biology. Trends in Plant Science 15, 641–650.
Root hair systems biology.Crossref | GoogleScholarGoogle Scholar | 20851035PubMed |

Linkohr BI, Williamson LC, Fitter AH, Leyser HMO (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. The Plant Journal 29, 751–760.
Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12148533PubMed |

Liu MY, Lou HQ, Chen WW, Piñeros MA, Xu JM, Fan W, Kochian LV, Zheng SJ, Yang JL (2018) Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress. Plant, Cell & Environment 41, 809–822.
Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress.Crossref | GoogleScholarGoogle Scholar |

Lomonte C, Wang Y, Doronila A, Gregory D, Baker AJ, Siegele R, Kolev SD (2014) Study of the spatial distribution of mercury in roots of vetiver grass (Chrysopogon zizanioides) by micro-PIXE spectrometry. International Journal of Phytoremediation 16, 1170–1182.
Study of the spatial distribution of mercury in roots of vetiver grass (Chrysopogon zizanioides) by micro-PIXE spectrometry.Crossref | GoogleScholarGoogle Scholar | 24933909PubMed |

López-Pérez L, Fernández-García N, Olmos E, Carvajal M (2007) The phi thickening in roots of broccoli plants: an acclimation to salinity? International Journal of Plant Sciences 168, 1141–1149.
The phi thickening in roots of broccoli plants: an acclimation to salinity?Crossref | GoogleScholarGoogle Scholar |

Lux A, Martinka M, Vaculík M, White PJ (2010) Root responses to cadmium in the rhizosphere: a review. Journal of Experimental Botany 62, 21–37.
Root responses to cadmium in the rhizosphere: a review.Crossref | GoogleScholarGoogle Scholar | 20855455PubMed |

Lyubenova L, Pongrac P, Vogel-Mikuš K, Mezek GK, Vavpetič P, Grlj N, Kump P, Nečemer M, Regvar M, Pelicon P (2012) Localization and quantification of Pb and nutrients in Typha latifolia by micro-PIXE. Metallomics 4, 333–341.
Localization and quantification of Pb and nutrients in Typha latifolia by micro-PIXE.Crossref | GoogleScholarGoogle Scholar | 22370692PubMed |

Lyubenova L, Pongrac P, Vogel-Mikuš K, Mezek GK, Vavpetič P, Grlj N, Regvar M, Pelicon P, Schröder P (2013) The fate of arsenic, cadmium and lead in Typha latifolia: a case study on the applicability of micro-PIXE in plant ionomics. Journal of Hazardous Materials 248–249, 371–378.
The fate of arsenic, cadmium and lead in Typha latifolia: a case study on the applicability of micro-PIXE in plant ionomics.Crossref | GoogleScholarGoogle Scholar | 23416480PubMed |

Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6, 273–278.
Aluminium tolerance in plants and the complexing role of organic acids.Crossref | GoogleScholarGoogle Scholar | 11378470PubMed |

Ma Q, Yi R, Li L, Liang Z, Zeng T, Zhang Y, Huang H, Zhang X, Yin X, Cai Z (2018) GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana. BMC Plant Biology 18, 212
GsMATE encoding a multidrug and toxic compound extrusion transporter enhances aluminum tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 30268093PubMed |

Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, Wang Y-H, Schaffert RE, Hoekenga OA, Pineros MA, Shaff JE (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics 39, 1156–1161.
A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum.Crossref | GoogleScholarGoogle Scholar | 17721535PubMed |

Mari S, Gendre D, Pianelli K, Ouerdane L, Lobinski R, Briat J-F, Lebrun M, Czernic P (2006) Root-to-shoot long-distance circulation of nicotianamine and nicotianamine–nickel chelates in the metal hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany 57, 4111–4122.
Root-to-shoot long-distance circulation of nicotianamine and nicotianamine–nickel chelates in the metal hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 17079698PubMed |

Meents MJ, Watanabe Y, Samuels AL (2018) The cell biology of secondary cell wall biosynthesis. Annals of Botany 121, 1107–1125.
The cell biology of secondary cell wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 29415210PubMed |

Meychik N, Nikolaeva Y, Kushunina M, Yermakov I (2014) Are the carboxyl groups of pectin polymers the only metal-binding sites in plant cell walls? Plant and Soil 381, 25–34.
Are the carboxyl groups of pectin polymers the only metal-binding sites in plant cell walls?Crossref | GoogleScholarGoogle Scholar |

Meychik N, Nikolaeva Y, Kushunina M (2019) The role of the cell walls in Ni binding by plant roots. Journal of Plant Physiology 234–235, 28–35.
The role of the cell walls in Ni binding by plant roots.Crossref | GoogleScholarGoogle Scholar | 30660944PubMed |

Meyer CJ, Seago JL, Peterson CA (2009) Environmental effects on the maturation of the endodermis and multiseriate exodermis of Iris germanica roots. Annals of Botany 103, 687–702.
Environmental effects on the maturation of the endodermis and multiseriate exodermis of Iris germanica roots.Crossref | GoogleScholarGoogle Scholar | 19151041PubMed |

Micallef SA, Shiaris MP, Colón-Carmona A (2009) Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. Journal of Experimental Botany 60, 1729–1742.
Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates.Crossref | GoogleScholarGoogle Scholar | 19342429PubMed |

Miwa K, Takano J, Omori H, Seki M, Shinozaki K, Fujiwara T (2007) Plants tolerant of high boron levels. Science 318, 1417
Plants tolerant of high boron levels.Crossref | GoogleScholarGoogle Scholar | 18048682PubMed |

Mohan D, Pittman CU, Steele PH (2006) Single, binary and multi-component adsorption of copper and cadmium from aqueous solutions on Kraft lignin – a biosorbent. Journal of Colloid and Interface Science 297, 489–504.
Single, binary and multi-component adsorption of copper and cadmium from aqueous solutions on Kraft lignin – a biosorbent.Crossref | GoogleScholarGoogle Scholar | 16375914PubMed |

Mönchgesang S, Strehmel N, Schmidt S, Westphal L, Taruttis F, Müller E, Herklotz S, Neumann S, Scheel D (2016) Natural variation of root exudates in Arabidopsis thaliana-linking metabolomic and genomic data. Scientific Reports 6, 29033
Natural variation of root exudates in Arabidopsis thaliana-linking metabolomic and genomic data.Crossref | GoogleScholarGoogle Scholar | 27363486PubMed |

Motte H, Beeckman T (2019) The evolution of root branching: increasing the level of plasticity. Journal of Experimental Botany 70, 785–793.
The evolution of root branching: increasing the level of plasticity.Crossref | GoogleScholarGoogle Scholar | 30481325PubMed |

Nakayama T, Shinohara H, Tanaka M, Baba K, Ogawa-Ohnishi M, Matsubayashi Y (2017) A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots. Science 355, 284–286.
A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 28104889PubMed |

Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N (2012) Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proceedings of the National Academy of Sciences of the United States of America 109, 10101–10106.
Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin.Crossref | GoogleScholarGoogle Scholar | 22665765PubMed |

Nawrath C, Schreiber L, Franke RB, Geldner N, Reina-Pinto JJ, Kunst L (2013) Apoplastic diffusion barriers. The Arabidopsis Book 11, e0167
Apoplastic diffusion barriers. Crossref | GoogleScholarGoogle Scholar | 24465172PubMed |

Nishizono H, Kubota K, Suzuki S, Ishii F (1989) Accumulation of heavy metals in cell walls of Polygonum cuspidatum roots from metalliferous habitats. Plant & Cell Physiology 30, 595–598.

North G, Nobel P (2000) Heterogeneity in water availability alters cellular development and hydraulic conductivity along roots of a desert succulent. Annals of Botany 85, 247–255.
Heterogeneity in water availability alters cellular development and hydraulic conductivity along roots of a desert succulent.Crossref | GoogleScholarGoogle Scholar |

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
Target or barrier? The cell wall of early-and later-diverging plants vs cadmium toxicity: differences in the response mechanisms.Crossref | GoogleScholarGoogle Scholar | 25814996PubMed |

Perumalla CJ, Chmielewski JG, Peterson CA (1990a) A survey of angiosperm species to detect hypodermal Casparian bands. III. Rhizomes. Botanical Journal of the Linnean Society 103, 127–132.
A survey of angiosperm species to detect hypodermal Casparian bands. III. Rhizomes.Crossref | GoogleScholarGoogle Scholar |

Perumalla CJ, Peterson CA, Enstone DE (1990b) A survey of angiosperm species to detect hypodermal Casparian bands. I. Roots with a uniseriate hypodermis and epidermis. Botanical Journal of the Linnean Society 103, 93–112.
A survey of angiosperm species to detect hypodermal Casparian bands. I. Roots with a uniseriate hypodermis and epidermis.Crossref | GoogleScholarGoogle Scholar |

Peterson CA (1987) The exodermal Casparian band of onion roots blocks the apoplastic movement of sulphate ions. Journal of Experimental Botany 38, 2068–2081.
The exodermal Casparian band of onion roots blocks the apoplastic movement of sulphate ions.Crossref | GoogleScholarGoogle Scholar |

Peterson CA (1989) Significance of the exodermis in root function. In ‘Structural and functional aspects of transport in roots’. (Eds BC Loughamn,O Gašparíková, J Kolek) pp. 35–40. (Springer: Dordrecht, Netherlands)

Peterson RL, Farquhar ML (1996) Root hairs: specialized tubular cells extending root surfaces. Botanical Review 62, 1–40.
Root hairs: specialized tubular cells extending root surfaces.Crossref | GoogleScholarGoogle Scholar |

Peterson CA, Perumalla CJ (1990) A survey of angiosperm species to detect hypodermal Casparian bands. II. Roots with a multiseriate hypodermis or epidermis. Botanical Journal of the Linnean Society 103, 113–125.
A survey of angiosperm species to detect hypodermal Casparian bands. II. Roots with a multiseriate hypodermis or epidermis.Crossref | GoogleScholarGoogle Scholar |

Peterson CA, Emanuel ME, Weerdenburg CA (1981) The permeability of phi thickenings in apple (Pyrus malus) and geranium (Pelargonium hortorum) roots to an apoplastic fluorescent dye tracer. Canadian Journal of Botany 59, 1107–1110.
The permeability of phi thickenings in apple (Pyrus malus) and geranium (Pelargonium hortorum) roots to an apoplastic fluorescent dye tracer.Crossref | GoogleScholarGoogle Scholar |

Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y, Vermeer JE, Yamazaki M, Li G, Maurel C, Takano J (2014) A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. eLife 3, e03115
A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects.Crossref | GoogleScholarGoogle Scholar | 25233277PubMed |

Plett D, Safwat G, Gilliham M, Skrumsager Møller I, Roy S, Shirley N, Jacobs A, Johnson A, Tester M (2010) Improved salinity tolerance of rice through cell type-specific expression of AtHKT1;1. PLoS One 5, e12571
Improved salinity tolerance of rice through cell type-specific expression of AtHKT1;1.Crossref | GoogleScholarGoogle Scholar | 21151904PubMed |

Rabbi SMF, Tighe MK, Flavel RJ, Kaiser BN, Guppy CN, Zhang X, Young IM (2018) Plant roots redesign the rhizosphere to alter the three-dimensional physical architecture and water dynamics. New Phytologist 219, 542–550.
Plant roots redesign the rhizosphere to alter the three-dimensional physical architecture and water dynamics.Crossref | GoogleScholarGoogle Scholar | 29774952PubMed |

Ragni L, Greb T (2018) Secondary growth as a determinant of plant shape and form. Seminars in Cell and Developmental Biology 79, 58–67.
Secondary growth as a determinant of plant shape and form.Crossref | GoogleScholarGoogle Scholar | 28864343PubMed |

Ranathunge K, Schreiber L (2011) Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin. Journal of Experimental Botany 62, 1961–1974.
Water and solute permeabilities of Arabidopsis roots in relation to the amount and composition of aliphatic suberin.Crossref | GoogleScholarGoogle Scholar | 21421706PubMed |

Raven J (1981) Nutritional strategies of submerged benthic plants: the acquisition of C, N and P by rhizophytes and haptophytes. New Phytologist 88, 1–30.
Nutritional strategies of submerged benthic plants: the acquisition of C, N and P by rhizophytes and haptophytes.Crossref | GoogleScholarGoogle Scholar |

Raven JA, Edwards D (2001) Roots: evolutionary origins and biogeochemical significance. Journal of Experimental Botany 52, 381–401.
Roots: evolutionary origins and biogeochemical significance.Crossref | GoogleScholarGoogle Scholar | 11326045PubMed |

Reinhardt DH, Rost TL (1995) Salinity accelerates endodermal development and induces an exodermis in cotton seedling roots. Environmental and Experimental Botany 35, 563–574.
Salinity accelerates endodermal development and induces an exodermis in cotton seedling roots.Crossref | GoogleScholarGoogle Scholar |

Reinhold-Hurek B, Bünger W, Burbano CS, Sabale M, Hurek T (2015) Roots shaping their microbiome: global hotspots for microbial activity. Annual Review of Phytopathology 53, 403–424.
Roots shaping their microbiome: global hotspots for microbial activity.Crossref | GoogleScholarGoogle Scholar | 26243728PubMed |

Rellán‐Álvarez R, Abadía J, Álvarez‐Fernández A (2008) Formation of metal‐nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. A study by electrospray ionization time‐of‐flight mass spectrometry. Rapid Communications in Mass Spectrometry 22, 1553–1562.
Formation of metal‐nicotianamine complexes as affected by pH, ligand exchange with citrate and metal exchange. A study by electrospray ionization time‐of‐flight mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 18421700PubMed |

Ricachenevsky FK, de Araújo AT, Fett JP, Sperotto RA (2018) You shall not pass: root vacuoles as a symplastic checkpoint for metal translocation to shoots and possible application to grain nutritional quality. Frontiers in Plant Science 9, 412
You shall not pass: root vacuoles as a symplastic checkpoint for metal translocation to shoots and possible application to grain nutritional quality.Crossref | GoogleScholarGoogle Scholar | 29666628PubMed |

Roberts SK (2006) Plasma membrane anion channels in higher plants and their putative functions in roots. New Phytologist 169, 647–666.
Plasma membrane anion channels in higher plants and their putative functions in roots.Crossref | GoogleScholarGoogle Scholar | 16441747PubMed |

Rodrigues M, Ganança JFT, da Silva EM, dos Santos TM, Slaski JJ, Zimny J, de Carvalho MÂP (2019) Evidences of organic acids exudation in aluminium stress responses of two Madeiran wheat (Triticum aestivum L.) landraces. Genetic Resources and Crop Evolution 66, 857–869.
Evidences of organic acids exudation in aluminium stress responses of two Madeiran wheat (Triticum aestivum L.) landraces.Crossref | GoogleScholarGoogle Scholar |

Roppolo D, De Rybel B, Tendon VD, Pfister A, Alassimone J, Vermeer JEM, Yamazaki M, Stierhof YD, Beeckman T, Geldner N (2011) A novel protein family mediates Casparian strip formation in the endodermis. Nature 473, 380–383.
A novel protein family mediates Casparian strip formation in the endodermis.Crossref | GoogleScholarGoogle Scholar | 21593871PubMed |

Ryan P, Delhaize E, Jones D (2001) Function and mechanism of organic anion exudation from plant roots. Annual Review of Plant Biology 52, 527–560.
Function and mechanism of organic anion exudation from plant roots.Crossref | GoogleScholarGoogle Scholar |

Ryan PR, Delhaize E, Watt M, Richardson AE (2016) ‘Plant roots: understanding structure and function in an ocean of complexity.’ (Oxford University Press: Oxford, UK)

Sakai T, Wada T, Ishiguro S, Okada K (2000) RPT2: a signal transducer of the phototropic response in Arabidopsis. The Plant Cell 12, 225–236.
RPT2: a signal transducer of the phototropic response in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 10662859PubMed |

Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum‐activated malate transporter. The Plant Journal 37, 645–653.
A wheat gene encoding an aluminum‐activated malate transporter.Crossref | GoogleScholarGoogle Scholar | 14871306PubMed |

Sattelmacher B (2001) The apoplast and its significance for plant mineral nutrition. New Phytologist 149, 167–192.
The apoplast and its significance for plant mineral nutrition.Crossref | GoogleScholarGoogle Scholar |

Schmidt H, Günther C, Weber M, Spörlein C, Loscher S, Böttcher C, Schobert R, Clemens S (2014) Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition. PLoS One 9, e102444
Metabolome analysis of Arabidopsis thaliana roots identifies a key metabolic pathway for iron acquisition.Crossref | GoogleScholarGoogle Scholar | 25549085PubMed |

Schreiber L, Franke RB (2011) Endodermis and exodermis in roots. eLS 2011, 333–339.

Schreiber L, Franke R, Hartmann K (2005) Effects of NO3 deficiency and NaCl stress on suberin deposition in rhizo-and hypodermal (RHCW) and endodermal cell walls (ECW) of castor bean (Ricinus communis L.) roots. Plant and Soil 269, 333–339.
Effects of NO3 deficiency and NaCl stress on suberin deposition in rhizo-and hypodermal (RHCW) and endodermal cell walls (ECW) of castor bean (Ricinus communis L.) roots.Crossref | GoogleScholarGoogle Scholar |

Seregin I, Kozhevnikova A (2008) Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium. Russian Journal of Plant Physiology 55, 1–22.
Roles of root and shoot tissues in transport and accumulation of cadmium, lead, nickel, and strontium.Crossref | GoogleScholarGoogle Scholar |

Shahid M, Pinelli E, Dumat C (2012) Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. Journal of Hazardous Materials 219–220, 1–12.
Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands.Crossref | GoogleScholarGoogle Scholar | 22502897PubMed |

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.
Glucose alleviates cadmium toxicity by increasing cadmium fixation in root cell wall and sequestration into vacuole in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25404058PubMed |

Shishkoff N (1987) Distribution of the dimorphic hypodermis of roots in angiosperm families. Annals of Botany 60, 1–15.
Distribution of the dimorphic hypodermis of roots in angiosperm families.Crossref | GoogleScholarGoogle Scholar |

Song W-Y, Choi KS, Geisler M, Park J, Vincenzetti V, Schellenberg M, Kim SH, Lim YP, Noh EW, Lee Y (2010) Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport. The Plant Cell 22, 2237–2252.
Arabidopsis PCR2 is a zinc exporter involved in both zinc extrusion and long-distance zinc transport.Crossref | GoogleScholarGoogle Scholar | 20647347PubMed |

Soukup A, Votrubová O, Čížková H (2002) Development of anatomical structure of roots of Phragmites australis. New Phytologist 153, 277–287.
Development of anatomical structure of roots of Phragmites australis.Crossref | GoogleScholarGoogle Scholar |

Stasovski E, Peterson CA (1993) Effects of drought and subsequent rehydratoin on the structure, vitality, and permeability of Allium cepa adventitious roots. Canadian Journal of Botany 71, 700–707.
Effects of drought and subsequent rehydratoin on the structure, vitality, and permeability of Allium cepa adventitious roots.Crossref | GoogleScholarGoogle Scholar |

Steudle E (2000) Water uptake by roots: effects of water deficit. Journal of Experimental Botany 51, 1531–1542.
Water uptake by roots: effects of water deficit.Crossref | GoogleScholarGoogle Scholar | 11006304PubMed |

Steudle E, Peterson C (1998) How does water get through roots? Journal of Experimental Botany 49, 775–788.

Steudle E, Murrmann M, Peterson CA (1993) Transport of water and solutes across maize roots modified by puncturing the endodermis. Plant Physiology 103, 335–349.
Transport of water and solutes across maize roots modified by puncturing the endodermis.Crossref | GoogleScholarGoogle Scholar | 12231941PubMed |

Stubbs CJ, Cook DD, Niklas KJ (2019) A general review of the biomechanics of root anchorage. Journal of Experimental Botany 70, 3439–3451.
A general review of the biomechanics of root anchorage.Crossref | GoogleScholarGoogle Scholar | 30698795PubMed |

Sun Q, Yoda K, Suzuki M, Suzuki H (2003) Vascular tissue in the stem and roots of woody plants can conduct light. Journal of Experimental Botany 54, 1627–1635.
Vascular tissue in the stem and roots of woody plants can conduct light.Crossref | GoogleScholarGoogle Scholar | 12730266PubMed |

Sunarpi HT, Motoda J, Kubo M, Yang H, Yoda K, Horie R, Chan WY, Leung HY, Hattori K, Konomi M, Osumi M, Yamagami M, Schroeder JI, Uozumi N (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells. The Plant Journal 44, 928–938.
Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na+ unloading from xylem vessels to xylem parenchyma cells.Crossref | GoogleScholarGoogle Scholar |

Swarup R, Kramer EM, Perry P, Knox K, Leyser HO, Haseloff J, Beemster GT, Bhalerao R, Bennett MJ (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nature Cell Biology 7, 1057–1065.
Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal.Crossref | GoogleScholarGoogle Scholar | 16244669PubMed |

Takahashi H (1994) Hydrotropism and its interaction with gravitropism. Plant and Soil 165, 301–308.
Hydrotropism and its interaction with gravitropism.Crossref | GoogleScholarGoogle Scholar |

Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, Miwa K, Hayashi H, Yoneyama T, Fujiwara T (2002) Arabidopsis boron transporter for xylem. Nature 420, 337–340.
Arabidopsis boron transporter for xylem.Crossref | GoogleScholarGoogle Scholar | 12447444PubMed |

Tang Z, Kang Y, Wang P, Zhao F-J (2016) Phytotoxicity and detoxification mechanism differ among inorganic and methylated arsenic species in Arabidopsis thaliana. Plant and Soil 401, 243–257.
Phytotoxicity and detoxification mechanism differ among inorganic and methylated arsenic species in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Tester M, Leigh RA (2001) Partitioning of nutrient transport processes in roots. Journal of Experimental Botany 52, 445–457.
Partitioning of nutrient transport processes in roots.Crossref | GoogleScholarGoogle Scholar | 11326051PubMed |

Torrey JG (1976) Root hormones and plant growth. Annual Review of Plant Physiology 27, 435–459.
Root hormones and plant growth.Crossref | GoogleScholarGoogle Scholar |

Tsai HH, Schmidt W (2017) Mobilization of iron by plant-borne coumarins. Trends in Plant Science 22, 538–548.
Mobilization of iron by plant-borne coumarins.Crossref | GoogleScholarGoogle Scholar | 28385337PubMed |

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.
Root-secreted nicotianamine from Arabidopsis halleri facilitates zinc hypertolerance by regulating zinc bioavailability.Crossref | GoogleScholarGoogle Scholar | 25118254PubMed |

Tsugeki R, Fedoroff NV (1999) Genetic ablation of root cap cells in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 96, 12941–12946.
Genetic ablation of root cap cells in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 10536027PubMed |

Vaculík M, Konlechner C, Langer I, Adlassnig W, Puschenreiter M, Lux A, Hauser M-T (2012a) Root anatomy and element distribution vary between two Salix caprea isolates with different Cd accumulation capacities. Environmental Pollution 163, 117–126.
Root anatomy and element distribution vary between two Salix caprea isolates with different Cd accumulation capacities.Crossref | GoogleScholarGoogle Scholar | 22325439PubMed |

Vaculík M, Landberg T, Greger M, Luxová M, Stoláriková M, Lux A (2012b) Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants. Annals of Botany 110, 433–443.
Silicon modifies root anatomy, and uptake and subcellular distribution of cadmium in young maize plants.Crossref | GoogleScholarGoogle Scholar | 22455991PubMed |

van Leeuwen HP (1999) Metal speciation dynamics and bioavailability: inert and labile complexes. Environmental Science & Technology 33, 3743–3748.
Metal speciation dynamics and bioavailability: inert and labile complexes.Crossref | GoogleScholarGoogle Scholar |

Vert G, Briat JF, Curie C (2001) Arabidopsis IRT2 gene encodes a root‐periphery iron transporter. The Plant Journal 26, 181–189.
Arabidopsis IRT2 gene encodes a root‐periphery iron transporter.Crossref | GoogleScholarGoogle Scholar | 11389759PubMed |

Vert G, Grotz N, Dédaldéchamp F, Gaymard F, Guerinot ML, 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.
IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth.Crossref | GoogleScholarGoogle Scholar | 12084823PubMed |

Villordon AQ, Ginzberg I, Firon N (2014) Root architecture and root and tuber crop productivity. Trends in Plant Science 19, 419–425.
Root architecture and root and tuber crop productivity.Crossref | GoogleScholarGoogle Scholar | 24630073PubMed |

von Wirén N, Klair S, Bansal S, Briat J-F, Khodr H, Shioiri T, Leigh RA, Hider RC (1999) Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants. Plant Physiology 119, 1107–1114.
Nicotianamine chelates both FeIII and FeII. Implications for metal transport in plants.Crossref | GoogleScholarGoogle Scholar | 10069850PubMed |

Wallace A, Romney E (1975) ‘Roots of higher plants as a barrier to translocation of some metals to shoots of plants.’ (Laboratory of Nuclear Medicine and Radiation, University of California: Los Angeles, CA, USA)

Wang R, Jing W, Xiao L, Jin Y, Shen L, Zhang W (2015) The Rice high-affinity potassium transporter1;1 is involved in salt tolerance and regulated by an MYB-type transcription factor. Plant Physiology 168, 1076–1090.
The Rice high-affinity potassium transporter1;1 is involved in salt tolerance and regulated by an MYB-type transcription factor.Crossref | GoogleScholarGoogle Scholar | 25991736PubMed |

Wang Y, Wang C, Liu Y, Yu K, Zhou Y (2018) GmHMA3 sequesters cd to the root endoplasmic reticulum to limit translocation to the stems in soybean. Plant Science 270, 23–29.
GmHMA3 sequesters cd to the root endoplasmic reticulum to limit translocation to the stems in soybean.Crossref | GoogleScholarGoogle Scholar | 29576076PubMed |

Wang P, Calvo-Polanco M, Reyt G, Barberon M, Champeyroux C, Santoni V, Maurel C, Franke RB, Ljung K, Novak O, Geldner N, Boursiac Y, Salt DE (2019) Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants. Scientific Reports 9, 4227
Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants.Crossref | GoogleScholarGoogle Scholar | 30862916PubMed |

Waters S, Gilliham M, Hrmova M (2013) Plant high-affinity potassium (HKT) transporters involved in salinity tolerance: structural insights to probe differences in ion selectivity. International Journal of Molecular Sciences 14, 7660–7680.
Plant high-affinity potassium (HKT) transporters involved in salinity tolerance: structural insights to probe differences in ion selectivity.Crossref | GoogleScholarGoogle Scholar | 23571493PubMed |

Whiting SN, Leake JR, Mc GRATHSP, Baker AJ (2000) Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytologist 145, 199–210.
Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar |

Wild E, Dent J, Thomas GO, Jones KC (2005) Direct observation of organic contaminant uptake, storage, and metabolism within plant roots. Environmental Science & Technology 39, 3695–3702.
Direct observation of organic contaminant uptake, storage, and metabolism within plant roots.Crossref | GoogleScholarGoogle Scholar |

Wilson CA, Peterson CA (1983) Chemical composition of the epidermal, hypodermal, endodermal and intervening cortical cell walls of various plant roots. Annals of Botany 51, 759–769.
Chemical composition of the epidermal, hypodermal, endodermal and intervening cortical cell walls of various plant roots.Crossref | GoogleScholarGoogle Scholar |

Xu Q, Pan W, Zhang R, Lu Q, Xue W, Wu C, Song B, Du S (2018) Inoculation with Bacillus subtilis and Azospirillum brasilense produces abscisic acid that reduces IRT1-mediated cadmium uptake of roots. Journal of Agricultural and Food Chemistry 66, 5229–5236.
Inoculation with Bacillus subtilis and Azospirillum brasilense produces abscisic acid that reduces IRT1-mediated cadmium uptake of roots.Crossref | GoogleScholarGoogle Scholar | 29738246PubMed |

Yang Y-Y, Jung J-Y, Song W-Y, Suh H-S, Lee Y (2000a) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiology 124, 1019–1026.
Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance.Crossref | GoogleScholarGoogle Scholar | 11080279PubMed |

Yang ZM, Sivaguru M, Horst WJ, Matsumoto H (2000b) Aluminium tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max). Physiologia Plantarum 110, 72–77.
Aluminium tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max).Crossref | GoogleScholarGoogle Scholar |

Yang H, Zheng M, Zhu Y (2008) Tracing the behavior of hexachlorobenzene in a paddy soil-rice system over a growth season. Journal of Environmental Sciences) 20, 56–61.
Tracing the behavior of hexachlorobenzene in a paddy soil-rice system over a growth season.Crossref | GoogleScholarGoogle Scholar |

Yang XY, Yang JL, Zhou Y, Pineros MA, Kochian LV, Li GX, Zheng SJ (2011) A de novo synthesis citrate transporter, Vigna umbellata multidrug and toxic compound extrusion, implicates in Al‐activated citrate efflux in rice bean (Vigna umbellata) root apex. Plant, Cell & Environment 34, 2138–2148.
A de novo synthesis citrate transporter, Vigna umbellata multidrug and toxic compound extrusion, implicates in Al‐activated citrate efflux in rice bean (Vigna umbellata) root apex.Crossref | GoogleScholarGoogle Scholar |

Yang X, Dong G, Palaniappan K, Mi G, Baskin TI (2017) Temperature‐compensated cell production rate and elongation zone length in the root of Arabidopsis thaliana. Plant, Cell & Environment 40, 264–276.
Temperature‐compensated cell production rate and elongation zone length in the root of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Zelazny E, Vert G (2014) Plant nutrition: root transporters on the move. Plant Physiology 166, 500–508.
Plant nutrition: root transporters on the move.Crossref | GoogleScholarGoogle Scholar | 25034018PubMed |

Zhang W-H, Ryan PR, Tyerman SD (2001) Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiology 125, 1459–1472.
Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots.Crossref | GoogleScholarGoogle Scholar | 11244125PubMed |

Zhang L, Wu X-X, Wang J, Qi C, Wang X, Wang G, Li M, Li X, Guo Y-D (2018) BoALMT1, an Al-induced malate transporter in cabbage, enhances aluminum tolerance in Arabidopsis thaliana. Frontiers in Plant Science 8, 2156
BoALMT1, an Al-induced malate transporter in cabbage, enhances aluminum tolerance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 29410672PubMed |

Zhao Z, Gao X, Ke Y, Chang M, Xie L, Li X, Gu M, Liu J, Tang X (2019) A unique aluminum resistance mechanism conferred by aluminum and salicylic-acid-activated root efflux of benzoxazinoids in maize. Plant and Soil 437, 273–289.
A unique aluminum resistance mechanism conferred by aluminum and salicylic-acid-activated root efflux of benzoxazinoids in maize.Crossref | GoogleScholarGoogle Scholar |