The barrier function of plant roots: biological bases for selective uptake and avoidance of soil compounds Ramces De-Jesús-García A , Ulises Rosas B and Joseph G. Dubrovsky A,C 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 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. Received 24 May 2019, accepted 16 December 2019, published online 26 March 2020 Introduction The soil system contains water and the nutrients necessary for a plant to complete its life cycle. The physical, chemical and biological interactions occurring between plant roots and the surrounding soil environment are highly complex (Ehrenfeld et al. 2005; Gregory 2006). To maintain plant growth and development, water and nutrient uptake taking place in the root is tightly controlled (Steudle 2000; Tester and Leigh 2001; Hodge 2004). Thereby the root is the main organ through which water and mineral nutrients enter the plant organism. Roots face both, essential elements (e.g. minerals such as N, P and K ions and salts) and non-essential, or unfitting compounds (such as heavy metals, metalloids, organic xenobiotics), and must deal with them. In this challenging scenario, the roots have to perform the selective ‘pickup and delivery’ of soil solutes to the inside of the plant. To accomplish this task, the roots implement an ‘avoid and exclude’ and ‘select the needed one and deliver it’ strategies. To fulfil these functions, several molecular, cellular and tissue barriers have evolved. These barriers selectively avoid, restrict, exclude or cope with the entry of any unsuitable compound to both the root and the aboveground plant tissues (Clemens 2006; Seregin and Kozhevnikova 2008; Lux et al. 2010; Vaculík et al. 2012b; Kochian et al. 2015). This suggests that the root, viewed as a whole organ, fulfils a barrier function for the plant organism. Despite of this, in literature, the barrier function of plant roots is not considered as such. Here, we review the morpho-anatomical, structural and other components that support our understanding that the roots fulfil the barrier function. To substantiate the proposed barrier function of plant roots, we discuss what properties or components of the root structure can perform processes of selectivity, permeability or barrier at a cellular, tissue, and organ level. Additionally, we review evolutionary aspects of this barrier function of plant roots. Finally, we analyse cases where natural variants with selective root permeability have been described, which suggest that the barrier function is constantly evolving. Defining the plant root and its functions: recognising the barrier function The plant root is commonly a heterotrophic multicellular organ of vascular plants whose aerial organs are autotrophic. We can define the plant root as a highly specialised and multicellular organ, found only in the sporophytes of vascular plants. Root growth and intensive branching allow soil exploration around the aerial plant organs in the search and foraging for water and nutrients. This organ is formed by a complex network of individual root axes, each of which is a multicellular organ, which displays certain specific properties. These properties, among others, include: (a) positive gravitropism (Blancaflor and Masson 2003; Swarup et al. 2005; Ge and Chen 2016) and hydrotropism (Takahashi 1994; Cassab et al. 2013) and negative phototropism (Sakai et al. 2000); (b) the presence CSIRO PUBLISHING Functional Plant Biology, 2020, 47, 383–397 Review https://doi.org/10.1071/FP19144 Journal compilation Ó CSIRO 2020 www.publish.csiro.au/journals/fpb