Amanda Rasmussen1 and Susanne Schmidt,2
1Centre for Plant Integrative Biology, University of Nottingham, UK; 2School of Agriculture and Food Science, University of Queensland
Plants require at least 14 essential elements called ‘mineral nutrients’ to sustain life function and complete their life cycle, in addition to carbon (in the form of CO2), oxygen, and hydrogen (in the form of water). Some plants have specific requirements for additional elements. The acquisition via the roots and use of these elements are the topic of plant nutrition.
Figure 4.1 Young wheat seedlings with a mass of elongated seminal roots that were excavated and washed (left) or imaged in situ using microCT (right). Note that in situ imaging preserves the lateral growth of lateral roots. Images courtesy of E. Delhaize (left) and S. Mairhofer (right).
By responding to signals and gradients in the soil, the root system can maximise growth in local nutrient patches while minimising growth in areas of deficiency. This is extremely important for plant survival particularly in deficient or marginal soils. Efficient root growth is also an important factor in maximising yield with lower fertiliser applications because ‘wasted’ root growth costs energy that could otherwise be invested in the crop of interest (whether seeds, leaves, stems or tubers). For this reason understanding the root environmental responses and breeding crops with efficient root systems for the conditions of interest are currently highly active areas of agronomic research.
This section covers the different nutrients required for plant growth, and the different root architectures and structures which help the plants maintain sufficient nutrient uptake to support the above ground biomass.
Although the absolute quantities of nutrients required vary between plant species, genotypes and growth environments, essential nutrients are categorised into so-called macronutrients (N, K, Ca, P, Mg, S) that plants require in larger quantities, and micronutrients (Fe, Cl, Mn, B, Zn, Cu, Mo, Ni) that are needed in small amounts (Figure 4.2). Additional beneficial elements include Si (e.g. for grasses) and Na (for many sea-shore plants).
Figure 4.2 Mineral nutrient concentrations in plant leaves. Concentrations can be larger or smaller than shown here. Note, lower concentrations occur in roots and wood. (Adapted from Marschner 1995)
Micronutrients mainly provide functional groups in enzymes (BOX 1 shows how Ni forms the active site in urease, as an example).
BOX 1 – Nickel (Ni) at the centre of UreaseIn 1926 James B. Sumner from Cornell University studied the structure of Urease from Jack Bean plants and demonstrated that the enzyme is also a protein. This work led to the recognition that most enzymes are in fact proteins and in 1946 Sumner was awarded the Nobel Prize in Chemistry. Urease is an enzyme that breaks down urea to ammonia and carbon dioxide in plants, bacteria and fungi and contains a nickel active site. (NH2)2CO + H2O -> CO2 + 2NH3 For 3D structure see http://www.proteopedia.org/wiki/index.php/Urease Further reading: Follmer 2008; Carter et al. 2009. |
In terrestrial ecosystems and in agriculture, the availability of nitrogen (N) and phosphorus (P) are often limiting and so affect plant growth and productivity most strongly. However, other elements can also be limiting. Plants showing nutrient deficiencies will exhibit symptoms such as stunted growth, leaf or shoot tip chlorosis, and defoliation, and will die if supplements are not provided. Fertilisers are applied to supply essential elements in agriculture to maximise plant growth and enhance yields. Along with the discovery of ‘dwarfing genes’ and development of short stature crop varieties, it was the use of synthetic nitrogen fertilisers that played a significant role in the Green Revolution of the 1930s-1960s.
The acquisition of mineral nutrients starts with their movement from the surrounding soil to root surfaces. The movement of nutrients from bulk soil towards plant roots occurs via diffusion or mass flow (Figure 4.3). Root interception occurs as the root comes in contact with, and displaces the soil through which it is growing. Nutrient availability in soils and the physical and chemical factors influencing their movement from soils to the root surface is comprehensively described in a review by Marschner and Rengel (2012). Nutrients are taken up into roots by active or passive transport across cell membranes, which is described later in this chapter (Section 4.5).
Figure 4.3 Element movement to root surface. Root interception occurs as the root displaces soil; diffusion occurs along a concentration gradient; mass flow is driven by plant transpiration and is the movement of soil solution along a water potential gradient. (Based on Marschner and Rengel 2012)
Diffusion occurs along a concentration gradient, over relatively short distances (in the order of 1 cm). As roots take up nutrients and ions from the soil a depletion zone can be established allowing diffusion to occur into the depletion zone. The rate of diffusion depends on how fast the roots are taking up the nutrient, how much of the nutrient is present in the soil (this determines the steepness of the concentration gradient that forms) and also on the mobility of the ions by diffusion. Soluble ions would take about a day to diffuse 1 cm; ions bound to the soil matrix would take longer. For examples, Marscher and Rengel (2012) show that nitrate by diffusion in a ‘typical’ soil travels 3 mm in a day, potassium about 1 mm in a day, and phosphate moves only about 0.1 mm in a day. This illustrates the importance of root hairs in intercepting and accessing phosphate.
Mass flow is driven by the uptake of water caused by the transpiration rate of the plants and can occur over long distances. Many soluble nutrients such as nitrate are dissolved in the soil water and as the plant pulls the water from the soil, the nutrients move too. Some nutrients move by mass flow faster than their uptake rate so they build up on the surface of the root during daylight hours (Marschner and Rengel, 2012). The rate of movement by mass flow of solution depends basically on the rate of transpiration of the plant, so there is little movement at night. It is also influenced by soil water content and soil texture (see Chapter 3, Section 3.4).
Nutrients are unevenly distributed in the soil, generally being concentrated in the topsoil due to decomposition of leaf litter, but also dispersed elsewhere in pockets. Uneven surface enrichment arises from diverse sources such as dead fauna, urine patches from grazing animals, and localised application of fertiliser. Phosphorus and all cations are relatively immobile as they bind to the soil while nitrate and other anions (except phosphorus) are soluble and can readily be leached to deeper soil layers.
Because the soil is so heterogeneous, plants have developed adaptable (plastic) root systems so that the roots proliferate close to the nutrients for uptake.
Figure 4.4 Root systems of young (left) wheat and (right) lupin plants. Wheat, a monocot, has a dual root system. Seminal roots emerge from the seed and nodal roots (thicker roots on the outside of the picture) emerge from the crown, a group of closely packed nodes from which tillers emerge. Lupin, a dicot, has a tap root from which lateral roots emerge and which thickens with time as continued cambial activity leads to secondary growth.
The root system architecture is the arrangement of different roots in solid space. Just like a building has walls, roof, and floors, plant root systems also contain different structures including root types (primary, lateral, adventitious), root hairs, and specialized features such as nodules and cluster roots (see case study). In contrast to a fixed structure like a building, the root system is dynamic with new structures forming as needed to explore the soil and old structures breaking down when their use has expired. This four dimensional architecture within soil can now be visualized using technology such as X-ray microscale computed tomography (microCT) and magnetic resonance imaging (MRI).
In order to understand root architecture it is important to understand the different structures that make up the root system. This section will focus on the different root types while cluster roots are explained in the case study that follows. Root hairs are described in the section on the rhizosphere (Section 4.2) and the formation of N2-fixing nodules in Section 4.4.
Figure 4.5 MicroCT images of crop root systems. A, Single wheat plant with primary root (P), lateral roots (L) and seminal roots (S). Roots are false-coloured in white, and soil is false-coloured in brown. Scale bar = 1 cm. (Reproduced from Atkinson et al. (2014) Plant Physiol 166: 538-550. doi:10.1104/pp.114.245423. Copyright American Society of Plant Biologists). B) Two wheat plants grown in the same pot. Roots are false-coloured in blue or orange; each colour shows a single root system. (Image courtesy S. Mairhofer)
Figure 4.6 Root types. White = primary root, cream = seminal roots, blue = first order lateral roots, pink = second order lateral roots, yellow = crown roots, orange = brace roots. Crown and brace roots are both adventitious root types. (Original drawing courtesy A Rasmussen)
Lateral roots: roots that form from other roots. The lateral roots that form from the primary root are first order lateral roots; the lateral roots that form from the first order laterals are second order laterals and so on. This class of root is post-embryonic.
Seminal roots: form adjacent to the radicle and dominate the early root growth in monocots. This root type is embryonic.
Adventitious roots: any root that forms from anything other than another root. This includes roots that form on the base of stem cuttings, from leaf explants, from stems in flooded plants and also from nodes of cereal crops (often called crown roots). These root types are very diverse (Steffens and Rasmussen, 2015) so can include both embryonic and post-embryonic roots.
Figure 4.7 Examples of adventitious root types. This figure highlights a few examples of the diversity of adventitious roots; A and B show types of adventitious roots that form during normal development while C and D are examples of stress-induced adventitious roots. A, Those potentially established in the embryo. B, The dominant root system of monocots including maize (top image) crown roots (yellow) and brace roots (orange) and nodal roots on other grasses (lower image) and on eudicots such as strawberry. C, Low or no light (e.g. Arabidopsis used as a model for adventitious root regulation) or flooding (lower image) can induce adventitious roots from either nodal or non-nodal stem positions. D, Wounding such as taking a cutting induces de novo adventitious root development. Primary and seminal roots are depicted in white, first order lateral roots in blue and second order laterals in pink. (Based on Steffens and Rasmussen (2016) Plant Physiol. 170: 603-617. doi:10.1104/pp.15.01360. Copyright American Society of Plant Biologists)
Root hairs: single-cell, hair-like extrusions from the epidermis which increase root surface area for nutrient uptake (Jones and Dolan, 2012) and are important for nodulation (Section 4.4).
The combination of different root types present in the root system differs across species. In particular the root systems of cereal crops (monocots) differ dramatically to the root systems of tree crops (eudicots) (Figure 4.8).
Figure 4.8 Eudicot and monocot root systems. A ,C and E represent eudicot roots while B, D and F represent monocot roots. Schematic showing the dominant root types of tomato (A) and maize (B). SR = stem roots, P = primary root, L = lateral root, Br = brace root, Cr = crown root, S = seminal root (original diagram courtesy A. Rasmussen). MicroCT images of tomato (C) and maize (D) (images courtesy J. Johnson and S. Mairhofer). Cross section schematics of the eudicot Arabidopsis (E) and rice (F) showing where new roots initiate. (Reproduced from Atkinson et al. (2014) Plant Physiol 166: 538-550. doi:10.1104/pp.114.245423. Copyright American Society of Plant Biologists)
Eudicots typically develop a primary (tap) root from a single radicle that emerges from a seed. This primary root, plus the first order lateral roots which emerge from it, provide a framework on which higher-order lateral roots are formed. Such a framework strengthens due to secondary thickening when division of the cambium gives rise to more cell layers, leading to massive roots that are often seen radiating from the base of a tree trunk (Figure 4.9).
Monocots such as grasses and cereal crops do not have a cambium for secondary thickening and develop a fibrous root system. This root system begins with the radicle which grows into the primary root. Adjacent to the radicle, several seminal roots also emerge and combined with the primary root these roots dominate the young root systems of monocots. Next nodal adventitious roots (often called crown roots) emerge from lower stem nodes and these thicker roots gradually dominate the root system. Finally in some monocots, such as maize (corn), nodal adventitious roots emerge above the soil level (brace roots) to provide additional structural support. Stems of monocots are typically anchored by the nodal roots, which are more numerous than seminal roots (Hochholdinger et al. 2004; Hochholdinger 2009).
Despite these structural differences between monocot and eudicot root systems, they can all vary the soil volume which they explore depending on water and nutrient availability. In this way the root distribution in the soil can vary both vertically and locally depending on available resources.
Figure 4.9 Dimorphic root system of a six-year-old Banksia prionotes tree growing in Western Australia in a deep sand. The trunk (T) is connected through a swollen junction (J) to the root system which comprises a dominant sinker root (S) with smaller sinkers (S2). A system of lateral roots (L) emerge horizontally from the junction, some bearing smaller sinker roots (arrows). Other laterals give rise to cluster roots (CR). (W.D. Jeschke and J.S. Pate, J Exp Bot 46: 907-915, 1995)
The amount of roots present in a volume of soil varies both vertically and locally depending on resource availability and physical restrictions. This is often measured as the total length of all roots present per unit volume of soil (root length density, L, expressed in km m–3).
Figure 4.10 Root length density in relation to depth in the soil for a wheat crop and a jarrah forest (Eucalyptus marginata). (Jarrah data from B.A. Carbon et al., Forest Sci 26: 656-664, 1980; wheat data courtesy F.X. Dunin)
Vertically, the root length density is often large in surface layers of the soil and typically decreases with increasing depth. Commonly, hundreds of kilometres of root per cubic metre of soil are observed near the soil surface.
Figure 4.10 shows root length density, L, as a function of depth in a wheat crop in early spring, and under a jarrah forest, also in spring. Both have a dense population of roots near the surface but wheat roots barely penetrate below 1 m, whereas jarrah roots penetrate to well below the 2.5 m shown here, often to 20 m. Dense root proliferation near the soil surface probably reflects an adaptation of plants to acquire phosphorus, potassium and other cations such as the micronutrients zinc and copper. These nutrients do not move readily in soil as they are bound to the soil surfaces, hence roots branch prolifically to ensure close proximity (a few millimetres) between adsorbing surfaces and these soil-immobile ions. Roots of jarrah are also concentrated near the soil surface (Figure 4.10) to access phosphate and nutrients released by litter decomposition, but some roots penetrate very deeply to tap subsoil moisture.
Nutrients are distributed unevenly in the soil. Root systems respond to enriched zones of nutrients by high levels of branching. Figure 4.11 shows an example of such a proliferation; the dense roots in the centre of the figure are a response by the row of wheat plants to application of a large pellet of nitrogen fertiliser (see arrow).
Figure 4.11 Excavated root system of wheat plants whose roots were provided with a concentrated band of ammonium sulphate fertiliser at the head of the arrow. (Photograph courtesy J.B. Passioura)
Such proliferations around bands of fertilizer ensure plants maximise nutrient uptake with the minimum cost to plant development. This efficiency fits within optimal partitioning theory which states that plants respond to environmental variation by partitioning biomass among the plant organs to optimize the acquisition of nutrients, light, water and carbon to maximize plant growth (Reich, 2002). This means that in low nutrient conditions the plants will put more energy into growing roots and less into shoot growth (Reich, 2002). Likewise when light is limiting, plants will invest more energy in leaf area and less in root development (Weaver and Himmel, 1929; Reich, 2002). Maintaining the balance between root and shoot is important as the roots must be extensive enough to supply nutrients and water in proportion to the demand and hydraulic pull from the leaves and vice versa the leaves must produce enough sugars to continue the growth of the root system (Weaver and Himmel, 1929). Consistent with this, Butler et al. (2010) found in Sitka spruce forest, the root absorbing area was correlated with the tree stem diameter and to the transpiring leaf area index. This highlights the link in hydraulics between leaf and root areas.
Young roots absorb nutrients more rapidly than old roots. New roots supply annual plants with abundant sites for nutrient uptake, especially during establishment. A feature of the roots of perennials is that they have a large turnover of the fine, high-order lateral roots that emerge from the secondarily thickened framework each year. This turnover draws heavily on photoassimilate, equivalent to half the CO2 fixed in annuals and up to 90% of the standing biomass of temperate forests. Production of fine (and often ephemeral) roots ensures uptake of nutrients over many years.
Because many soils are deficient in key nutrients, plants have developed a special relationship with certain fungi called mycorrhizae (Section 4.4). In this symbiosis the fungi obtain fixed carbon from the host plant, and in turn supply the host with poorly mobile nutrients, especially phosphorus. This is achieved by proliferating their hyphae to provide a much greater surface area for nutrient uptake than could be provided by roots alone. Another adaptation, common in the Proteaceae, and also occurring in some species of lupin, is proteoid roots, clusters of tiny rootlets that greatly enlarge the available surface area for ion uptake and which are inducible by low levels of phosphorus (see Case study 4.1).
M. Watt
Figure 1 Cluster roots in Banksia serrata growing on Hawkesbury Sandstone hillslopes in the Sydney region. a, Roots that have grown across a dead eucalypt leaf extract nutrients remaining in the decaying leaf. b, Clusters of fine rootlets at the tips of roots increase the surface area for nutrient extraction from surrounding soil. Scale bar = 100 µm. (Scanning electron micrograph courtesy S. Gould)
Australian soils generally contain low concentrations of plant-available phosphate, much of it bound with iron–aluminium silicates into insoluble forms or concentrated in the remains of decaying plant matter. Because very little of this phosphate is soluble, most roots extract it only slowly. Plants with cluster roots gain access to fixed and organic phosphate through an increase in surface area and release of phosphate-solubilising exudates. Hence plants with cluster roots grow faster on phosphate-fixing soils than species without clusters.
Cluster roots have a distinct morphology. Intense proliferation of closely spaced, lateral ‘rootlets’ occurs along part of a root axis to form the visually striking structures. Root hairs develop along each rootlet and result in a further increase in surface area compared to regions where cluster roots have not developed.
In the Proteaceae, clusters generally form on basal laterals so that they are abundant near the soil surface where most nutrients are found. For example, Banksia serrata produces a persistent, dense root mat capable of intercepting nutrients from leaf litter and binding the protecting underlying soil from erosion (Figure 1a). New clusters differentiate on the surface of this mat after fires and are well placed to capture nutrients. In contrast, Banksia prionotes forms ephemeral clusters which export large amounts of nutrients during winter. Lupinus albus has more random clusters which appear on up to 50% of roots (Figure 2).
Figure 2 Basal roots of a two-week-old Lupinus albus plant grown in nutrient culture with 1 µM phosphate. Proteoid roots have emerged along the primary lateral roots (arrowhead) and the oldest proteoid rootlets have reached a determinate length of 5 mm. As rootlets approach their final length, they exude citrate for 2-3 d. (mm scale on left side) (Photograph courtesy M. Watt)
Rootlets not only represent an increase in surface area but also exude protons and organic acids, solubilising phosphate and making it available for uptake (Watt and Evans 1999a). Exudates from cluster roots represent up to 10–23% of the total weight of an L. albus plant, suggesting that they constitute a major sink for photoassimilates. However, not all this additional carbon comes from photosynthesis because approximately 30% of the carbon demand of clusters is met by dark CO2 fixation via phosphoenolpyruvate carboxylase. Because cluster roots form on roots of L. albus even when phosphate supply is adequate, growth of L. albus in soils with low phosphate availability is not restricted by an additional carbon ‘drain’ to roots. On the other hand, the great many species which produce cluster roots in response to environmental cues like phosphate deficiency might experience a carbon penalty to support these roots.
Cluster roots on L. albus are efficient with respect to carbon consumption by generating citrate on cue. Most of the citrate exuded by clusters is released during a two to three day period when the cluster is young (Watt et al. 1999b). A large root surface area in clusters works in concert with this burst of exudation to solubilise phosphate before it is re-fixed to clay surfaces or diffuses away.
Cluster roots can mine a pocket of phosphate-rich soil which would otherwise not yield its nutrients. They are an elegant adaptation of root structure and biochemistry to nutrient-poor soils.
Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Bot Acta 108: 183–200
Lamont BB (1993) Why are hairy root clusters so abundant in the most nutrient impoverished soils of Australia? Plant Soil 156: 269–272
Purnell HM (1960) Studies of the family Proteaceae 1. Anatomy and morphology of the roots of some Victorian species. Aust J Bot 8: 38–50
Watt M, Evans JR (1999a) Proteoid Roots. Physiology and Development. Plant Physiol 121: 317–323
Watt M, Evans JR (1999b) Linking development and determinacy with organic acid efflux from proteoid roots of Lupinus albus L. grown with low phosphorus and ambient or elevated atmospheric CO2 concentration. Plant Physiol 120: 705–716
