Organ system

This article is about the part of a plant. For other uses, see Root (disambiguation).

«Rooted» redirects here. For the 1969 play and TV movie adaptation, see Rooted (film). For the song, see Ciara discography.

Primary and secondary roots in a cotton plant

The cross-section of a barley root

Ranunculus Root Cross Section

Large, mature tree roots above the soil

Root system architecture (RSA)

Extrinsic factors affecting root architecture include gravity, light exposure, water and oxygen, as well as the availability or lack of nitrogen, phosphorus, sulphur, aluminium and sodium chloride. The main hormones (intrinsic stimuli) and respective pathways responsible for root architecture development include:

Growth from apical meristems is known as primary growth, which encompasses all elongation.
Secondary growth encompasses all growth in diameter, a major component of woody plant tissues and many nonwoody plants. For example, storage roots of sweet potato have secondary growth but are not woody. Secondary growth occurs at the lateral meristems, namely the vascular cambium and cork cambium. The former forms secondary xylem and secondary phloem, while the latter forms the periderm.

Tree roots at Port Jackson

Fluorescent imaging of an emerging lateral root.

Shade avoidance response

A true root system consists of a primary root and secondary roots (or lateral roots).

Stilt roots of Maize plant

Cross section of an adventitous crown root of pearl millet (Pennisetum glaucum)

Roots forming above ground on a cutting of an Odontonema («Firespike»)

The growing tip of a fine root

Cross section of a mango tree

The distribution of vascular plant roots within soil depends on plant form, the spatial and temporal availability of water and nutrients, and the physical properties of the soil. The deepest roots are generally found in deserts and temperate coniferous forests; the shallowest in tundra, boreal forest and temperate grasslands. The deepest observed living root, at least 60 metres below the ground surface, was observed during the excavation of an open-pit mine in Arizona, USA. Some roots can grow as deep as the tree is high. The majority of roots on most plants are however found relatively close to the surface where nutrient availability and aeration are more favourable for growth. Rooting depth may be physically restricted by rock or compacted soil close below the surface, or by anaerobic soil conditions.

Roots can also protect the environment by holding the soil to reduce soil erosion

The term root crops refers to any edible underground plant structure, but many root crops are actually stems, such as potato tubers. Edible roots include cassava, sweet potato, beet, carrot, rutabaga, turnip, parsnip, radish, yam and horseradish. Spices obtained from roots include sassafras, angelica, sarsaparilla and licorice.

Sugar beet is an important source of sugar. Yam roots are a source of estrogen compounds used in birth control pills. The fish poison and insecticide rotenone is obtained from roots of Lonchocarpus spp. Important medicines from roots are ginseng, aconite, ipecac, gentian and reserpine. Several legumes that have nitrogen-fixing root nodules are used as green manure crops, which provide nitrogen fertilizer for other crops when plowed under. Specialized bald cypress roots, termed knees, are sold as souvenirs, lamp bases and carved into folk art. Native Americans used the flexible roots of white spruce for basketry.

Trees stabilize soil on a slope prone to landslides. The root hairs work as an anchor on the soil.

Vegetative propagation of plants via cuttings depends on adventitious root formation. Hundreds of millions of plants are propagated via cuttings annually including chrysanthemum, poinsettia, carnation, ornamental shrubs and many houseplants.

Roots can also protect the environment by holding the soil to reduce soil erosion. This is especially important in areas such as sand dunes.

• Clark L (2004). «Primary Root Structure and Development – lecture notes» . Archived from the original on 3 January 2006.
• Sutton RF, Tinus RW (1983). «Root and root system terminology». Forest Science Monograph. 24: 137.

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The two types of root systems in plants. The fibrous root system (A) is characterized by many roots with similar sizes. In contrast, plants that use the taproot system (B) grow a main root, with smaller roots branching off. The letters indicate where the root systems begin.

The taproot system contrasts with the adventitious or fibrous root system of plants with many branched roots, but many plants that grow a taproot during germination go on to develop branching root structures, although some that rely on the main root for storage may retain the dominant taproot for centuries, for example Welwitschia.Taproot also store nutrition. Plants with taproots are often vegetables.

A dandelion taproot (left) with the rest of the plant (right)

The edible, orange part of the carrot is its taproot

Many taproots are modified into storage organs.
Some plants with taproots:

Development of taproots

Many plants with taproots are difficult to transplant, or even to grow in containers, because the root tends to grow deep rapidly and in many species comparatively slight obstacles or damage to the taproot will stunt or kill the plant. Among weeds with taproots dandelions are typical; being deep-rooted, they are hard to uproot and if the taproot breaks off near the top, the part that stays in the ground often resprouts such that, for effective control, the taproot needs to be severed at least several centimetres below ground level.

Root and shoot systems in a eudicot

Other animals have similar organ systems to humans although simpler animals may have fewer organs in an organ system or even fewer organ systems.

Nervous system in a human body

Root systems There are two main types of root systems: tap root and fibrous root system.

Functions of Roots Some functions of roots are given below:

Activity Aim: To observe anchorage by roots Method: Try pulling out a handful of grass from the ground. Observation: It would not be easy to pull out the grass and something would prevent the grass from being pulled out. Carefully dig out some grass and see what prevented the grass from being pulled out. Conclusion: Roots bind soil particles and hold the plant firmly in one place to the ground.

ActivityAim: To observe absorption by rootsMaterials needed: A carrot, a glass of water, and blue colouring agentMethod: 1. Put a carrot in a glass of water containing some blue colouring agent. 2. Leave the carrot in water for some days.

3. Then cut it into half (lengthwise) and look inside.Observation: Blue colouring can be seen from the bottom to the top of the carrot.Conclusion: Water is absorbed by the tip of the carrot and travelled up inside it along with the blue colouring agent.

Root Modifications Roots of some plants are modified to perform additional functions. Let us study some of these modifications and their functions.

Roots are a prime target for crop improvement towards a more frugal and environmentally friendly agriculture. However, root traits have long been neglected in breeding programs, especially because the first green revolution was based on massive use of water and fertilizers. Global changes are now encouraging a more rational use of agricultural inputs in order to reduce soil degradation, water and air pollution, and resource depletion. Meeting production needs while limiting the use of water and mineral elements is a major challenge. What role can roots, the plant’s nourishing organs, play in the development of a more sustainable and resilient agriculture in the face of current and future climates? An essential role, as shown by recent research that allows us to better understand root system development, functions, diversity and adaptations to the environment, bringing roots from the shadows to the light.

Roots capture water and nutrients for the plant

Roots are organs of higher plants that are specialized in exploring the soil and taking up water and mineral ions (See How to feed plants while polluting less?). They play an essential role in plant survival and development. Each plant has several categories of roots organized in a root system. This set of roots anchors the plant in the soil and communicates with the stem(s), which carry the leaves, flowers and fruits. The root system develops through the repeated formation of new roots and their growth in length. Roots form and grow in tight relation to the plant’s environment. In doing so, roots allow plant adaptation to the heterogeneous and variable soil resources and constraints of its living environment (See The fixed life of plants and its constraints, The tireless quest for water by plants & Water needs of plants: how to satisfy them?).

Architecture and anatomy of the root system

The root system has a branched architecture and a specialized anatomy that influence its soil exploration and exchange properties. During germination, the first so-called seminal roots develop from the embryo located in the seed. Later, and throughout the life of the plant, other so-called post-embryonic roots develop from existing roots or stems. There is great variation in the proportions of the different categories of roots that contribute to the root system, as well as in their rate of growth and branching. Thus, there is a great diversity of root systems.

The specific properties of these different root tissues allow the root to modulate its exchange capacities with the soil:

The vascular tissues channel sap exchanges between the roots and the aerial organs:

In perennial species, old roots enlarge over the years by adding new layers of tissues. These so-called secondary tissues form, among other things, cork in the periphery and wood in the center of the root.

Development and plasticity of the root system

Root development in the soil is very sensitive to the environment. Root growth, development, and functional properties are influenced by signals circulating within the plant and stimuli perceived from the soil. These modifications of the root system in response to changing environmental conditions are crucial for plant adaptation and are referred to as root plasticity.

Thus, the plant root system is a complex structure that develops continuously in the soil and adapts dynamically to it. Adaptive root plasticity is favorable for plant nutrition under resource-limited conditions. Moreover, through their activity, these roots interact with the soil and modify its characteristics.

Roots interact with the soil and its microbial communities

Influence of roots on soil characteristics

Fabaceae, or legumes, produce flavonoids that stimulate symbiotic interactions with nitrogen-fixing soil bacteria according to similar principles (See Plants that live on air). These symbioses are characterized by the formation of new root organs, called nodules, where the bacteria are hosted and carry out the transformation of atmospheric nitrogen into a form of nitrogen that is assimilable by the plant. Furthermore, other exudates can act, on the contrary, as repulsive signals for pathogenic microorganisms or soil parasites.

By their continuous and plastic development, their adaptable properties and their beneficial actions on the rhizosphere, roots promote the nutrition and health of the plant. Improving the characteristics of the root system of cultivated plants allows to optimize these properties in increasingly constrained agronomic contexts.

A target for plant improvement

The root development of a single plant develops and adapts dynamically to environmental conditions. A great diversity in the way root systems develop and adapt to different environments can be observed between individuals of the same plant species. This diversity of root systems between varieties of the same species is the result of a progressive selection, over the course of evolution, of certain genetically controlled adaptive traits.

In rice, distinct root architectural traits have been identified in varieties adapted to different growing systems:

This diversity of root traits between plants of the same species can be exploited for varietal improvement. The transfer of beneficial root traits from one variety to another by crossing is an improvement strategy.

However, roots are complex systems and their performance depends on how architectural and anatomical features combine and function synergistically. Improving a trait without considering the overall functioning of the root system in its environment can produce detrimental effects. The development of deep roots, for example, may promote the acquisition of water when it is more abundant at depth. However, more roots at depth may hinder phosphorus acquisition. Indeed, phosphorus, that is an essential element for the plant, generally accumulates in the shallow soil.

In silico models of root systems interacting with soil models have been developed and allow simulating root system structure and functions as a whole (Figure 9). These models facilitate the identification of root traits that will, ultimately, show beneficial effects on plant nutrition and development in a given environment.

Utility of root systems for plant breeding

Powerful methods are now available to visualize and describe quantitatively the characteristics of the root system of plants without disturbing them. Nevertheless, these data are generally collected using laboratory experimental set-ups that poorly reflect the conditions of plants grown in the field. To meet the need of characterizing plant root systems under agronomic conditions and to facilitate their consideration in plant breeding programs, several methods for studying root systems in field have been developed.

By increasing the number of observations and collected data, the development of these new methods of root exploration in the field are decisive to:

Take home messages

The Encyclopedia of the Environment by the Association des Encyclopédies de l’Environnement et de l’Énergie (www.a3e.fr), contractually linked to the University of Grenoble Alpes and Grenoble INP, and sponsored by the French Academy of Sciences.

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Introduction to Roots and Root System Architecture

Roots are essential for plant productivity and serve a variety of functions, such as water and nutrient uptake, forming symbioses with other microorganisms in the rhizosphere, anchoring the plant to the soil, and acting as storage organs. The different interactions of a root with its environment depend on its organization and structure, from the cellular to whole-plant level. The root contains a stele, comprised of the xylem, the phloem, and the pericycle (Smith and De Smet, 2012). The stele is encircled by concentric layers of epidermal, cortical, and endodermal tissues. The root apical meristem forms the basic stem cell pool from which other cell types develop. This root apical meristem also holds the quiescent center (QC), with rarely dividing cells that signals the surrounding cells to organize and maintain the initial stem cells (Dolan et al., 1993). There are generally two types of roots: (i) those that are formed in the embryo, such as the primary and seminal roots in maize (Hochholdinger, 2009), tap or primary root in common bean (Lynch and Brown, 2012); (ii) those formed post-embryonically from consecutive nodes on shoots, normally referred to as adventitious roots (ARs). These include basal roots in beans, nodal roots in maize, ARs of sweetpotato, potato, cassava, as well as yam, and lateral roots (LRs; Lynch and Brown, 2012). LRs are formed post-embryonically from the pericycle of all root classes through auxin-dependent cell cycle activation. This cell cycle forms the LR founder cells that undergo several rounds of cell division to initiate LRs (Overvoorde et al., 2010). The elongation, growth angles from the main axis, lateral branching and longevity of all root classes forms the root system which is determined by genetic, physiological, and environmental factors (Lynch and Brown, 2012).

Root system architecture (RSA) therefore refers to the spatial configuration of the root system or the explicit deployment of root axes (Lynch, 1995). Under poorly understood genetic control, RSA exhibits plasticity and responds to external environmental conditions such as soil moisture, nutrients, temperature, pH, and microbial communities (Bao et al., 2014). The study of RSA is important for agricultural productivity because most soils have uneven distribution of resources and/or localized depletions that make spatial distribution of the root system an important determinant of a plant’s ability to exploit these resources (Lynch, 1995). Progress in the study of RSA in agricultural crops has consequently been realized, especially for cereals, and evidence for the genetic control of RSA and its relationship to increased productivity under stress is currently well-documented. Despite these achievements, information on RSA in root and tuber crops (RTCs), which form the second largest group of crops for global food security after cereals, is still lacking. A recent review by Villordon et al. (2014b) on root architecture and RTC productivity clearly indicates this gap. In the current review, we discuss RSA with special reference to RTCs, the genetic control of RSA, the relationship between RSA and abiotic stresses, and how RSA can be manipulated to confer tolerance to abiotic stresses. We then draw conclusions on the way forward for RSA studies in RTCs.

Root System Architecture in Root and Tuber Crops

Understanding RSA and the mechanisms of its development will allow manipulation and exploitation of different root traits to improve plants’ adaptation to changing climates and increase yields for the growing global human population (Smith and De Smet, 2012). Vegetatively propagated RTCs such as potato (Solanum tuberosum), sweetpotato (Ipomoea batatas), cassava (Manihot esculenta), and yam (Dioscorea spp.) provide food security for vast populations, especially in sub-Saharan Africa where many resource-poor small holder farmers provide the majority of food. Of the four major RTCs, cassava and sweetpotato are storage roots, while potato and yam are tubers. Little literature is specifically targeted to root growth and development in RTCs compared to cereals. The little literature available also mainly focuses on the growth and development of the storage root or tuber, primarily at harvest and post-harvest evaluations, rather than the entire root system. In this section we describe the root systems in the four major RTCs, based on available literature (Figure 1).

FIGURE 1. Root system architecture of cassava, sweetpotato, yam, and potato showing different root types (potato and sweetpotato figures adapted from Villordon et al., 2014b).

Cassava, potato, sweetpotato, and yam have ARs originating from the shoot or subterranean stem, in contrast with the primary root in seed-propagated crops which originates from the embryo. In sweetpotato and cassava, RSA is composed of ARs, LRs and storage roots (SRs), whereas in potato, the ARs can be divided into basal (ARs in Figure 1) and stolon roots (STR). In yam, the ARs root system is the most pronounced. The simple recognition of the main AR axis and its spatial and temporal relationship to LRs and their initiation in RTCs would enable systematic investigations to further understand the mechanisms that trigger LR emergence and morphogenesis.

Root Architecture in Root and Tuber Crops

The Link between Root Architecture and Yield in Root and Tuber Crops

In sweetpotato, storage root formation is marked by the formation of cambia around the protoxylem and secondary xylem elements, but lignification in the stele region reduces storage root formation (Togari, 1950; Wilson and Lowe, 1973). The first evidence of a link between sweetpotato LR development and storage root yield suggested that LRs may be essential in supplying “internal growth elements” for storage root formation (Koshimizu and Nishida, 1949). Recent work demonstrated the link between LR development and lignification. In ARs with a prevalence of arrested or non-emerged LR primordia, the adjacent stelar tissue becomes lignified thus rendering it incapable of undergoing swelling due to the absence of vascular and anomalous cambia development (Villordon et al., 2012). The precise relationship between stele lignification and LR development is still not clear in sweetpotato. However, proteomics work with maize lrt1 (lateral rootless1) mutants showed the detection of proteins associated with lignin metabolism in the primary root, providing evidence that LRs influenced the proteome of the primary root (Hochholdinger et al., 2004). These findings suggest that intrinsic and external stimuli which promote LR development preclude stele lignification, rendering the juvenile AR competent for storage root formation. In cassava, LRs are responsible for root system plasticity during the critical storage root formation stage (Pardales and Yamauchi, 2003). There is currently a lack of evidence to suggest a relationship between LR development and the capacity of an AR to become a storage root. Early work describing anatomical changes associated with storage root formation in cassava did not mention LRs (Indira and Kurian, 1977). Related work examined the branching pattern of LRs and reported that LRs increased root surface area and compensated for the decrease in the main root length (Izumi et al., 1999). It was concluded that roots with a well-developed branching pattern likely absorbed water and essential nutrients for storage root growth better. In potato, root mass is positively correlated with shoot mass and tuber bulking, but negatively correlated with early tuber bulking. Final tuber yield is related to RSA component traits such as specific root length of basal roots and total root weight for various root classes of potato under field grown conditions. Basal roots are important for water uptake and anchorage, whereas stolon roots are connected with nutrient acquisition and tuber formation (Wishart et al., 2013). Despite these efforts, the link between storage root/tuber yield and the carbon partition to other root types as well as the regulatory networks involved in RTCs is yet to be established. Understanding the genetic, physiological and environmental factors influencing these components of RSA in RTCs is therefore critical in adapting genotypes to changing climates.

Hormonal and Genetic Control Pathways for Root System Architecture

In sweetpotato, the only study found specifically referring to genetic control of RSA is by Villordon et al. (2014a) who showed evidence that orthologs of genes associated with RSA in model crops were present in sweetpotato. They found increased expression of a putative nitrogen transporter and deceased expression of a high affinity nitrogen transporter as well as decreased expression of a MAD-box gene under low nitrogen (N) conditions. A substantial amount of information is however available for storage root formation which is part of RSA in sweetpotato and cassava. Cytokinin is important in regulating storage root development in sweetpotato (Hashizume et al., 1982). Zeatin Riboside (ZR), Trans-Zeatin Riboside (t-ZR) and 9-glucosyl-n-6-2-isopentenyl adenosine (i6Ado) are the major CK involved in developing and activating the primary cambium. Besides hormones, several genes are involved in storage root formation and development in sweetpotato. Tanaka et al. (2005) found SRF1 through SRF10 developmentally regulated genes to be involved in storage root formation. SRF1, SRF2, SRF3, SRF5, SRF6, SRF7, and SRF9 were upregulated while SRF4, SRF8, and SRF10 were downregulated during storage root formation. Tanaka et al. (2008) showed that knotted1-like homeobox (KNOX1) genes, Ibkn1, Ibkn2 and Ibkn3, are associated with storage root development in sweetpotato. Ibkn1 and Ibkn2 were upregulated in developing and mature storage roots relative to fibrous roots. Ibkn1 is homologous to shoot meristemless (STM) gene of Arabidopsis whose overexpression leads to higher CK levels, while Ibkn2 and Ibkn3 are homologous to Brevipedicellus gene of Arabidopsis which negatively regulates lignin biosynthesis. A group of MAD-box genes, IbMADS genes such as IbMADS3, IbMADS4, and IbMADS79 are also found in fibrous roots before thickening, mainly in the vascular cambium region where rapid cell division occurs during storage root thickening (Kim et al., 2002). Noh et al. (2010) found that a MADS-box protein copy DNA, SRD1 enhances the proliferation of the metaxylem and cambium cells during the auxin-dependent initial thickening and growth of storage roots. Storage root development in sweetpotato is enhanced when an expansin gene (IbEXP1) is down-regulated (Noh et al., 2012), but lignin biosynthesis is inhibited as starch biosynthesis is enhanced during early storage root formation (Firon et al., 2013). Details on the molecular regulation of storage root formation in sweetpotato have been reviewed by Ravi et al. (2009, 2014). No literature was available on the genetic control of ARs and LRs in cassava. However, de Souza et al. (2004) showed overexpression of the Mec1 gene which codes for a Pt2L4 glutamic acid-rich protein and a RING Zinc Finger and LEA protein genes in the secondary xylem tissue of storage roots relative to fibrous roots. Based on a correlation network, the relationship between KNOX1 genes, phytohormone biosynthesis and phytohormone-signaling genes was established, and it was hypothesized that phytohormones are involved in the initiation of storage root development in cassava (Sojikul et al., 2015). Both potato and cassava storage organs have been substantially studied, but not the genetic and hormonal control of RSA for either crop.

In addition to hormones, signaling components, and transcription factors, micro-interfering RNAs (miRNAs) and small-interfering RNAs (siRNAs) have been shown to affect RSA in plants, as reviewed by Meng et al. (2010) and Khan et al. (2011). The miRNAs and siRNAs are thought to be involved in auxin signaling, nutrition metabolism and stress response by mediating signal interactions. They have been identified in embryonic root development, radial patterning, formation of ARs and LRs. However, their role in RTCs has not yet been studied.

The Relationship Between Root System Architecture and Abiotic Stresses

Root system architecture has a central role in crop plants’ response to abiotic stresses. Since roots grow underground, they are the first to sense abiotic stresses and adjust their genetic program for post-embryonic development to survive the stress (Lynch, 1995). Plant roots obtain water and nutrients from the soil, which is a complex system with intrinsic properties, abiotic and biotic interactions. Modulation of RSA is therefore affected when changes in the plant nutritional status and external nutrient supply over time are perceived and integrated into the intrinsic root development program. The degree of root plasticity is based on variations in the number, extension, placement, and growth direction of individual components of the root system (Giehl et al., 2014). These changes in RSA consequently affect the growth and development of above-ground biomass (Paez-Garcia et al., 2015) by altering carbon allocation to shoots and/or triggering signaling pathways involving hormones, proteins, RNAs, among others (DoVale and Fritsche-Neto, 2015). In this case therefore, roots indirectly regulate leaf stomatal conductance and affect leaf blade posture and photosynthetic rate when exposed to abiotic stress.

TABLE 2. A summary of relevant phenotypes and required traits under different abiotic stresses.

In RTCs, it is known that the root system is made up of ARs and LRs which presumably are involved in water and nutrient uptake and hence respond to abiotic stress. However, some RTCs have complex RSA because the harvestable part is also underground with several root classes, e.g., in potato, which may have different functions with regard to adaptation to abiotic stress. The potato root system is known to be shallow, with poor ability to penetrate soils thereby being drought susceptible (Porter et al., 1999). Despite having a shallow root system, potato is still not efficient in P and N uptake because the larger root system has a respiration carbon cost (Balemi and Schenk, 2009). Furthermore, most findings studied the root system as a whole without identifying possible roles for different root classes. An attempt at this was done by Wishart et al. (2013) who reported genetic variation for potato root traits without any specific abiotic stress. They suggested that basal roots were responsible for water uptake and anchorage while stolon roots were responsible for nutrient uptake and tuberization. Cassava and sweetpotato have less root classes compared to potato because the harvestable part is also a root. Pardales et al. (1999) studied the effects of high root zone temperature on root systems of cassava and sweetpotato. They showed a reduction in the total length of ARs, number and total length of first order LRs, under high root zone temperature in both crops. Pardales and Yamauchi (2003) also showed a suppression of AR and LR formation and development under drought stress in both sweetpotato and cassava. Recent studies in sweetpotato indicate direct influence on RSA of spatial and temporal availability of water and N availability similar to model systems (Villordon et al., 2014a). In yam, Hgaza et al. (2012) found no fertilizer response of tuber yield but a positive correlation between thinner, longer roots with tuber yield.

Manipulating Root System Architecture for Abiotic Stress Tolerance

The aim of carrying out RSA studies in crop plants is to understand areas of interest within the root system and incorporate this information in crop improvement programs. Several approaches may be applied in manipulating RSA in order to adapt crops to changing climates.

Combined-Stress versus Single-Stress Selection

Most of the reported studies above were carried out for stress-specific responses. However, stresses always occur in combination, with different scenarios and complexity, to which responses are also varied. In this case therefore, combined stress scenarios may be considered in relation to RSA. The complexity of the root growing environment and the limitations associated with studying only one trait could be lessened by ideotype or trait-based breeding, originally proposed by Donald (1968). Ideotype breeding requires consideration of relationships between multiple traits in addition to each individual trait (Rasmusson, 1987). A potato root ‘ideotype’ as summarized by Wishart et al. (2013) for example, is hypothesized to be one which is architecturally plastic, long, deep, and thin, as well as being able to self-protect against parasites and pathogen. Such a system should ideally be responsive to water deficits, able to transport ABA to shoots, enable efficient stomatal closure, and have minimum carbon costs, either by producing aerenchyma or increasing specific root length, increasing root surface area, or desirable root exudates and symbioses in the rhizosphere. In sweetpotato, Villordon and Clark (2014) found an association among RSA, virus resistance and availability of N thereby indicating the necessity of a more systematic approach toward determining and managing yield constraints. They showed that AR and LR formation was decreased by about 51% under deficiency and virus infection. On the other hand, storage root formation is known to fail under excess moisture and high N as more biomass is partitioned to above-ground biomass (Villordon et al., 2012). An ideotype for sweetpotato therefore, in addition to being efficient in water and mineral uptake and utilization, and being pathogen resistance as indicated above for potato, should also be tolerant to excess moisture and have balanced biomass partitioning between storage root and above-ground biomass. Trait -based breeding does not always result in accumulation of additive effects, rather synergies among traits need to be considered. It is proposed to incorporate root phenes into breeding programs targeting RSA. A phene, which has variants referred to as phene states, is the basic functional unit of a phenotype, with a phenotype being defined as the particular combination of states of all phenes of an individual (York et al., 2013). With regard to RSA, Lynch and Brown (2012) propose ‘elementary’ and ‘unique’ root phenes which cannot be decomposed further and which are a result of only one set of genes and processes. Root growth angle may for example be considered one of the phenes of root depth as it is only one of the factors determining root depth, while root depth is referred to as a phene aggregate, being a result of several phenes. A group of interacting phenes that may be selected together are referred to as a phene module. York et al. (2013) proposed hypotheses for integrating root phenes in a breeding program. They considered synergies within a phene module which increase as the number of positively acting phene-state combination increases. Metabolic costs are to be expected with such synergies except in metabolically neutral, positively acting, phene-state combinations. The interactions between phenes within plants, between plants and with the environment are expected to result in genetic variation in RSA.

Model-Assisted Phenotyping

In breeding approaches such as ideotype or phene-integrated, structural-functional plant modeling and simulation may offer a robust way of understanding the complexity of the non-linear signals and transduction pathways involved in the roots’ responses to multiple abiotic stresses. This is expected to provide new mechanistic insights into the regulation of root growth and development (Chickarmane et al., 2010). In addition to advances in high-throughput phenotyping techniques that allow rapid evaluation of a large number of genotypes, model-assisted phenotyping enhances prediction of difficult traits such as those that vary with environmental conditions. It also allows precise prediction of genotype × environment × management interaction over a large number of environments thereby allowing the estimation of comparative advantage of a given phene state in different environments (Tardieu and Tuberosa, 2010). Multi-scale modeling which examines behavior at subcellular, cellular, tissue, organ, and whole organism states may allow the prediction of the effect of a given phene, phene state, phene module, or phenotype in a complex abiotic stress environment (Band et al., 2012). Leitner et al. (2014) showed that functional-structural root models were appropriate to better comprehend the role of roots in whole-plant adaptation to diverse drought scenarios, in addition to their contribution to distinct drought scenarios. Using a dynamic root architecture model and root xylem hydraulic properties model, they showed that plants which transpired more had root axes which matched the available water distribution. They also found that water saving genotypes had lower root conductance than the water spending genotypes. Despite these advantages, encouragement for the adoption of root models needs to be accompanied with realistic and more explicit plant regulatory networks, in addition to integration with phenomic databases (Dunbabin et al., 2013) in order to be more representative and applicable to actual field performance of genotypes. This approach has not been applied in RTCs yet.

Genomics-Based Approaches

Manipulating root traits has been carried out in several crops through the use of molecular markers. Several specific genes related with RSA were identified in crop plants, either from gene mutants with quantifiable characteristics, or from QTL analyses. The genetic control of LR formation as reviewed above was elucidated based on gene mutants with quantifiable characteristics. In rice, a gene controlling root angle, Deeper Rooting 1 (DRO1), was identified using QTL mapping and introgressed into an elite line through backcrossing, whereas Phosphorus Starvation 1 (PSTOL1), a pup-1-specific protein kinase gene confers early root growth for P-acquisition in rice (Gamuyao et al., 2012) and sorghum (Hufnagel et al., 2014). However, information on how these genes/QTL affect the phenotypes and/or their performance in different genetic backgrounds and/or different environments is still largely lacking. This is because RSA response to environmental conditions is normally quite different under field conditions, given the broader spectrum of stresses the roots find themselves in Rich and Watt (2013). Extrapolating results obtained from a response to a specific abiotic stress is not therefore adequate (Jung and McCouch, 2013). Most of these QTLs are small-effect QTLs, i.e., they are normally conditioned by a single gene and therefore not stable across environments. Kitomi et al. (2015) for example, established that genotypes having the same functional allele of DRO1 could have different rooting angles. Small-effect QTLs therefore are assumed to be part of a set of minor QTLs. In such cases, it is necessary to carry out comparative data analysis and integration across controlled environments and field studies to establish target variants for further investigation and introgression into genotypes of interest. Alternatively, identification of large-effect QTLs which are more stable across environments and genetic backgrounds seems to be the most promising way of ensuring impact from genomics-assisted breeding methods. Dixit et al. (2015) confirmed the multi-genic and multi-environment effectiveness of qDTY12.1, a large-effect QTL identified on chromosome 12 of the rice genome. They confirmed the central role of the no apical meristem (OsNAM12.1) transcription factor in the activity of qDTY12.1 together with promoters of six intra-QTL genes with NAM binding sites as well as three co-localized and/or partially co-expressed genes of OsNAM12.1. These findings suggested that identification and proper analysis of large-effect QTLs together with their component genes could lead to a more efficient breeding process for complex traits such as those involved in adaptation and abiotic stress tolerance.

These reports are mainly based on Arabidopsis and cereal crops with simple genetic make-ups. Most RTCs on the other hand are polyploid with very complex genetic backgrounds. Genetic analysis of these crops is complicated by multiple alleles and loci, mixed inheritance patterns, association between ploidy and variation in mating system, among others (Dufresne et al., 2014). Marker-based procedures developed in diploid species therefore present difficulty to apply in most polyploid RTCs and adoption of these approach is not therefore straight forward. Application of the most commonly used genotyping methods, including new generation sequencing techniques, in RTCs present problems in allele dosage determination, presence of null alleles, distinguishing orthologs from paralogs, and copy number variation (Dufresne et al., 2014). As a consequence, although new techniques such as genomic selection offer great potential in marker-based breeding, they are currently still difficult to adopt. Additive, dominant and epistatic genetic effects are all important in RTCs due to heterozygosity (Ceballos et al., 2015) while models developed for genomic selection in cereals mainly consider additive genetic effects. Marker-based approaches in this class of crops therefore require re-thinking on the methods and pipelines available so far.

In addition to identifying QTLs and genes of interest from a species, another approach for adapting roots to abiotic stress is through transgenic technology. For example, spermidine synthase genes (FSPD1) confer higher antioxidant enzyme activities to plants. Under abiotic stress, plants with higher antioxidant enzyme activities are generally more tolerant, as they are better able to remove by-product reactive oxygen species (ROS) that are harmful to the plant if allowed to accumulate. Using transgenic technology, sweetpotato transformation with spermidine synthase genes (FSPD1) from Cucurbita ficifolia increased their multiple stress tolerance, with a higher concentration of FSPD1 in leaves and storage roots (Kasukabe et al., 2006). Estrada-Melo et al. (2015) used a 9-cis-epoxycarotenoid dioxygenase gene from tomato (LeNCED1) overexpressed in petunia and confirmed that NCED increased drought resistance of the transgenic plants. A calcium-dependent protein kinase (OsCDPK7) conferred tolerance to cold and salt/drought in rice transgenics. Two distinct pathways for cold and salt/drought tolerance using a single CDPK were implied which showed that manipulation of CDPK has great potential to adaptation and abiotic stress tolerant crop improvement. ‘Gene stacking,’ a form of ideotype breeding, could be a good alternative to transgenic technology that relies on a single gene. However, this has only been successful in pest control engineering such as the Bt toxin resistance (York et al., 2013). Gene stacking for complex traits is therefore still a challenge due to trait interaction.

Genome editing, a new approach that involves targeted DNA sequence modification through creation of double-strand breaks using sequence specific nucleases, provides possibilities to change a protein’s amino acid sequence through specific nucleotide substitutions, delete genes or chromosome segments, and introduce foreign DNA at desired genomic regions (Voytas, 2013). Several nucleases are available for targeted genome engineering (reviewed by Esvelt and Wang, 2013), but the system receiving most attention recently is CRISPR/Cas9, which involves the use of a guided RNA to create targeted mutations in candidate genes of key pathways in order to identify their effects and create new variation within a relatively short time (Cong et al., 2013), among other potential uses. These methods are gaining application in crop plants including RTCs. Clasen et al. (2016) used a TALENs approach to improve cold storage and processing traits in potato. The vacuolar invertase (VINV)gene (VINV) encoding a protein that breaks down sucrose to glucose and fructose was silenced in order to minimize the accumulation of reducing sugars which turn into anti-nutrients upon processing.

Phenotyping Root System Architecture Traits

Since roots grow below ground, studying the entire root system naturally requires digging it out, a complex process in itself, and it is difficult to extract the entire system without breaking off the finer parts. For this reason, studies have mainly dwelled on above-ground traits related to abiotic stress tolerance. However, given the pressures on crop productivity caused by global climate change, with the associated abiotic stresses, and the notion that food production needs to double in the next few years to accommodate the growing global population, root manipulation seems to hold the key toward sustainable food production. Villordon et al. (2014a) suggested that a paradigm shift toward RSA studies would enable a truly inclusive green revolution and allow food-insecure, resource-poor farmers who depend on RTCs in developing countries to also benefit. With this mindset, plant biologists, geneticists, and breeders have now shifted some focus toward studying of root traits. Due to the aforementioned complexity of studying roots under the soil, plant scientists are now set on finding minimally intrusive, non-destructive, whole-root system evaluating platforms. Hydroponics and gels are the most widely used systems to phenotype root systems (Jung and McCouch, 2013). Although, they offer a simple way to study different root traits and have given insight into root growth and development, both are controlled and do not represent actual field environments, and correlation of the findings from such experiments with actual performance of a plant in its natural environment are limited. To address this bottleneck, plant scientists are continually seeking to develop methods that will allow study of RSA in a more natural environment. Several methods have been proposed and applied in various studies including ‘shovelomics’ (Trachsel et al., 2011), soil coring (Wasson et al., 2014), rhizolysimeters (Eberbach et al., 2013) and minirhizotrons (Maeght et al., 2013), which are all soil-based. However, these methods are also low throughput, slow, and not amenable to large numbers of genotypes like those required for genome-wide association mapping studies. Image-based systems have also been developed and proposed to study roots in their natural environments, including X-ray computed tomography (Tracy et al., 2010) where x-rays are used to acquire 3-D cross-sectional images of the roots within the soil, Laser (Braga et al., 2009) which allows collection of bio-speckle patterns of gel-grown roots, nuclear magnetic resonance (NMR: Menzel et al., 2007), ground penetrating radar (GPR; Hirano et al., 2012), infra-red (IR) imaging (Dokken and Davis, 2007), and near-infra-red (NIR) imaging (Tirlapur and König, 1999), among others. However, application of some of these methods is still limited by the costs involved and to a few genotypes. Another bottleneck associated with imaging methods is image analysis. Several root image analysis platforms have been developed to address this limitation2. With these large numbers of imaging and image analysis platforms, the need for sharing and use of data requires establishment of trait ontology across them to allow development of root ideotypes for different environments. Efforts by Lobet et al. (2015) to develop a unified root architecture development language are therefore right on time. This, combined with scaling up of the image analysis methods mentioned above, will be able to provide further knowledge required to adapt crops to their highly variable environments.

Conclusion

The increasing global population requires increased food production on the same or even less agricultural land as used currently, if the effects of climate change render some of the available marginal lands unfit for agricultural production. Most of the present and past crop improvement efforts have focused on above-ground traits to adapt crop plants to different production constraints. Although great progress has been made, and food production significantly increased, by manipulating above-ground traits, an estimated 800 million people are still food insecure, whereas yields, especially in cereal, have reached their yield potential and are plateauing in certain regions of the globe. It is therefore time for crop scientists to tap into un-explored and less exploited diversity within RSA traits to ensure rapid genetic gains, and stable and enhanced productivity of agricultural systems for future environmental conditions and climate change scenarios. Due to the quantitative nature of RSA traits and complex interaction of several underlying pathways that control them, response of RSA to multiple individual stresses or combination of stresses is variable. Modeling of the responses of root traits to multiple stress scenarios in a combination of high-throughput root-trait phenotyping techniques, alongside a robust database and data analytical pipeline, could be a way to go. This proposed strategy is applicable to all crops, but is more urgent in RTCs, as the second largest source of food security after cereals, mainly growing in marginal areas where many cereals cannot survive. Also, for RTCs, the harvestable organs are part of the RSA. It is recommended to increase focus on RSA research by investing more resources. RTCs can learn from what has been found so far in cereals and adopt some of their methods, while developing high-throughput techniques to quantify RSA traits under optimal and stressful conditions.

Author Contributions

Review was conceptualized and written by MK, DG, and AV.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.