Root plasticity under abiotic stress

Abstract

Abiotic stresses increasingly threaten existing ecological and agricultural systems across the globe. Plant roots perceive these stresses in the soil and adapt their architecture accordingly. This review provides insights into recent discoveries showing the importance of root system architecture (RSA) and plasticity for the survival and development of plants under heat, cold, drought, salt, and flooding stress. In addition, we review the molecular regulation and hormonal pathways involved in controlling RSA plasticity, main root growth, branching and lateral root growth, root hair development, and formation of adventitious roots. Several stresses affect root anatomy by causing aerenchyma formation, lignin and suberin deposition, and Casparian strip modulation. Roots can also actively grow toward favorable soil conditions and avoid environments detrimental to their development. Recent advances in understanding the cellular mechanisms behind these different root tropisms are discussed. Understanding root plasticity will be instrumental for the development of crops that are resilient in the face of abiotic stress.

Figure 1

Plant RSA responses to abiotic stresses and their molecular regulation. A, Control: RSA under conditions with minimal abiotic stresses. B, Drought and heat: root growth and expansion in deeper soil layers, caused by an increase in gravitropic response and elongation of the roots. Local high moisture patches are sought through active growth toward water gradients known as positive hydrotropism. Moreover, root systems branch extensively in these areas by a process called hydropatterning. The side of the root with lower water potential accumulates cytokinin (CK), stimulating cell division asymmetrically, thereby allowing curvature of the root. CK accumulates at the site of the root with low water content and induces the expression of ARR16 and ARR17, which activate asymmetric cell division, resulting in bending of the roots. ABA can also induce the expression of MIZ1 and regulate hydrotropism. The bending of to root toward water is induced in the elongation zone where SnRK2.2 and MIZ1 regulate the differential growth response. C, Salt: depending on the severity of the salt concentration, salt type and plant sensitivity, root systems show positive or negative halotropism. Salt tolerant species, known as halophytes grow toward mild salt concentrations (positive halotropism), while most salt-sensitive plants, known as glycophytes, display negative halotropism. The gravitropic response is repressed. Salt stress induces ABA accumulation in the root tip, which inhibits GA and BR signaling and meristem size and PR elongation as well as reducing local auxin (AUX) levels. Salt stress induces PIN2 internalization and redistribution at one side of the root, causing differential auxin accumulation (green) and bending of the root away from the salt stress through negative halotropism. D, Flooding: root systems of plants respond to hypoxia by halting root growth, and stimulating ARs that grow sidewards to increase chances of improved oxygen uptake. The PR tip gravitropic response is inhibited leading to more lateral growth. This phenomenon of growth toward oxygen gradients is driven by ethylene (ET) signaling and has been referred to as aerotropism. Auxin regulates AR emergence by stimulating ethylene synthesis genes. Hypoxia induces auxin polar redistribution which leads to root bending (opposite of gravity) toward the soil surface. Hypoxia together with ethylene also induces the expression of ERFVII TFs that in turn can inhibit root bending. E, Soil compaction. For many plants, it remains unknown how plants respond to soil compaction, which is induced by agricultural practices and land management. Soil compaction leads to hypoxia, mimicking flooding stress; and leads to stimulation of ARs. Moreover, ethylene signaling represses root growth as well as the gravitropic response, thought to increase the tortuosity (curving nature) of the roots to increase maneuverability toward local cracks, soil pores, and less dense soils. Note that for water and salt gradients the image presents a directional response while in the case of submergence and compaction the root angle reflects repression of gravitropic response and can be in either direction.