EN中文

Journal of Resources and Ecology >

2023 , Vol. 14 >Issue 1: 15 - 24

DOI: https://doi.org/10.5814/j.issn.1674-764x.2023.01.002

Plant and Animal Ecology

Advances in Root System Architecture: Functionality, Plasticity, and Research Methods

  • ZHANG Zhiyong , 1 ,
  • FAN Baomin 1 ,
  • SONG Chao 1 ,
  • ZHANG Xiaoxian 1 ,
  • ZHAO Qingwen 2 ,
  • YE Bing , 1, *
Expand
  • 1. Research Institute of Forestry Policy and Information, Chinese Academy of Forestry, Beijing 100091, China
  • 2. Natural Resources Bureau of Bincheng District, Binzhou, Shandong 256600, China
*YE Bing, E-mail:

ZHANG Zhiyong, E-mail:

Received date: 2021-06-25

  Accepted date: 2022-03-20

  Online published: 2022-09-29

Supported by

The Fundamental Research Funds for CAF(CAFYBB2019ZC008)

The Research and Development Funds for RIFPI “Empirical Study on the Effect of Forest Activities on Decompression”(5000103-6019)

Fold

Abstract

Root system architecture (RSA) refers to the spatial distribution and extended morphology of plant root systems in soil. RSA not only determines the ability of plants to obtain water and nutrients but also affects other ecological functions. Hence, it plays a dominant role in the overall health of plants. The study of RSA can provide insight into plant absorption of water and fertilizers, the relationship between above- and belowground plant parts, and the physiological health and ecological functions of plants. Therefore, this paper summarizes research on the morphology, functionality, plasticity and research methods of RSA. We first review the basic structure, physiology, and ecological functions of root systems. Then the soil factors that shape RSA—including soil moisture, nutrients, temperature, aeration, and others—are summarized. After that, research methods for studying RSA are described in detail, including harvesting, two-dimensional morphological observation, and three-dimensional image reconstruction. Finally, future research developments and innovations are discussed to provide a theoretical basis for further investigations in this field.

Key words： plant root systems; root system architecture; soil factors; research methods; measurement techniques

Cite this article

ZHANG Zhiyong , FAN Baomin , SONG Chao , ZHANG Xiaoxian , ZHAO Qingwen , YE Bing . Advances in Root System Architecture: Functionality, Plasticity, and Research Methods[J]. Journal of Resources and Ecology, 2023 , 14(1) : 15 -24 . DOI: 10.5814/j.issn.1674-764x.2023.01.002

1 Introduction

As important functional organs of terrestrial plants, plant root systems anchor the aboveground parts, absorb water and mineral elements, and have a role in plant physiological activities (Badhon et al., 2021). Roots systems also have ecological roles in stabilizing soil structure, preventing soil erosion, and increasing soil water storage capacity, among other functions (Wang et al., 2017; Tran et al., 2019; Moldovan et al., 2020). Root system architecture (RSA) refers to the spatial distribution and extended morphology of plant root systems in soil, as defined by Fitter et al. (1991). RSA encompasses several important architectural features, including topology, link lengths and radii, and branching angles (Fitter et al. 1991; Lynch, 1995; Dhanapal et al., 2021). Root systems are in direct contact with the soil, and RSA is the result of long-term interactions between root systems and the soil environment. How efficiently plants explore the soil for essential supplies of water and nutrients is largely determined by the spatial distribution of their root systems. RSA can affect water absorption efficiency, nutrient acquisition, plant anchorage, and other functions, and it plays a decisive role in overall plant performance (Colombi et al., 2018). The study of RSA provides insight into patterns of water and fertilizer absorption and the relationship between above- and belowground plant parts. In addition, it is very important for understanding the physiological health and ecological functions of plants.
The study of RSA was first undertaken by plant nutritionists, and initial research focused on the relationship between RSA and nutrient acquisition. As this field developed, multidisciplinary research on RSA gradually became a topic of considerable interest. Since the 1990s, new technologies have provided many convenient approaches for studying RSA (Armengaud et al., 2009; Bot et al., 2010). In tandem with these technological developments, emerging measurement methods are giving us new insights into the relationship between RSA and function that could not previously be observed by destructive sampling. However, roots are belowground organs, and research on their architecture lags behind that on aboveground plant parts because roots are hidden by the opacity of the soil (Finér et al., 2011). Currently, most research on RSA tends to be in the form of case studies on single plants or single species. At the same time, most studies are based on experimental data obtained in a controlled laboratory cultivation environment (Koch et al., 2019; De Bauw et al., 2020; Lu et al., 2020; Barbosa et al., 2021), which inevitably has some limitations. Therefore, the aim of this review is three-fold: to systematically summarize current research on RSA from the standpoint of root structure and function, to describe soil factors that influence RSA, and to provide an overview of relevant research methods. Finally, based on the status of current research, future developments and innovations will be discussed to provide a theoretical basis for further investigations in this field.

2 Morphology and functions of root systems

2.1 Morphology of root systems

Root systems can be divided into taproot systems and fibrous root systems based on differences in their spatial morphology. Clearly, the taproot systems include a primary root and lateral roots. As the backbone of the root systems, the primary root is the main contributor to the overall RSA. From the perspective of static distribution, the contribution of lateral roots to the overall RSA seems relatively small, but from the perspective of dynamic growth and development, the degree of branching and the extension of lateral roots are direct determinants of RSA (Colombi et al., 2018; De Bauw et al., 2020). Root hairs are another important structure in root systems. These lateral outgrowths of epidermal cells expand the contact area between root systems and the soil, thereby increasing the absorptive area (Leitner et al., 2010). Notably, together with the root tip, the root hairs determine the initial growth direction and growth state of root systems and essentially determine their morphological structure (Fig. 1).
Fig. 1 A schematic diagram of RSA

2.2 Functions of root systems

As one of the six major organs of plants, the root systems have important physiological and ecological functions from different perspectives during plant growth and development. From the perspective of plant evolutionary history, the most important aspect of root systems is not their absorption of water and nutrients, but their function in plant anchorage (Kenrick and Strullu-Derrien, 2014). One of the greatest differences between plants and animals is that lower plants gradually abandoned the mobile life and became fixed in specific environments. The sessile nature of plants creates greater challenges to survival; therefore, during evolution, root systems gradually progressed from very simple to highly complex structures as their multiple functions improved and expanded. As root systems evolved from rhizoids to true roots, they gradually took on the physiological functions of water absorption and nutrient supply, which allowed plants to truly adapt to the terrestrial environment. From the perspective of plant physiology, the root system functions primarily to anchor and support plants and to acquire water and inorganic salts (Guo et al., 2019). It also has secondary functions, including photo-assimilate storage and phytohormone synthesis. From the viewpoint of ecology, root systems are an important organ of water transport in the soil-plant-atmosphere continuum (SPAC) and participate in ecosystem-level water cycling. At the same time, the extension of root systems into the soil increases soil shear strength and cohesion, promoting good soil consolidation and protecting slopes (Safitri et al., 2018; Bai et al., 2021).

3 Soil factors that steer RSA

During the growth and development of root systems, different factors may cause changes in RSA, which then feed back to influence the growth state of the whole plant. Healthy RSA is fundamental to the maintenance of normal physiological function in plants (Shahzad and Amtmann, 2017). Studying the factors that affect RSA is therefore a prime focus of root systems research. RSA depends primarily on genetic traits: genetic differences cause the root systems of different plants to exhibit unique aggregation states and specific branching modes (Dhanapal et al., 2021). Various processes can also affect RSA during growth and development; these include emergence of new main axes, branching, axial growth, radial growth, and root senescence and decay (Barbosa et al., 2021; Ogilvie et al., 2021). Root systems are in direct contact with the soil, and their morphology is an adaptive response to soil heterogeneity and pressure (Table 1).
Table 1 The RSA response to soil factors
Factors Materials Root traits and response to soil factors References
Soil moisture Forbs, grasses,woody species Water treatments revealed that a shift from low to high water was associated with significantly (P < 0.05) smaller root diameter (0.41-0.38 mm) and root mass fraction (0.59-0.52) and higher specific root length (187-197 m g-1), root elongation rate (5.8-7.6 cm d-1), and root growth rate (0.30-0.40 mg d-1) 2016
Perennial rangeland species RSA was affected by a range of spatial and temporal water availability. The biomass of root systems in the deep soil layer (40-60 cm) increased significantly (P < 0.001) during periods of low water availability 2017
Chenopodium populations from different habitats The specific root length of Chenopodium pallidicaule roots was three-fold finer on average than that of dry-habitat Chenopodium quinoa. The topological slope index differed significantly between dry-habitat C. quinoa (0.72) and Chenopodium hircinum (0.87). The dry-habitat C. quinoa generally had the highest total root length and deep root proliferation 2014
Soil nutrients Rice and Arabidopsis Nitrogen sculpted RSA into a narrow cone by inhibiting horizontal growth and promoting vertical expansion 2018
Maize, rape, spinach, tomato, wheat, Phaseolus vulgaris,
Arabidopsis, and others		 Plants adjust their RSA to low-P conditions through inhibition of primary root growth, promotion of lateral root growth, enhancement of root hair development and cluster root formation 2013
Arabidopsis Almost complete cessation of main root growth was observed 10 d after germination in P-deficient conditions. The number, density, and total length of lateral roots were higher under P starvation than under control conditions (P sufficient) 2016
Soil
temperature		 Norway spruce (Picea abies) A temperature of 9 ℃markedly decreased the fine root net increment rate, especially in short roots, but this decrease changed to enhanced growth at 16 ℃ Kilpeläinen et al.
2019
A mixture of temperate northern grassland species Soil warming significantly shortened the fine root lifespan, increased the root mortality rate and decreased the number and aggregation of roots Edwards et al.,
2004
Soil aeration Muskmelon The total root length and surface area were 83% and 63% higher, respectively, when plants received daily supplemental aeration than when no aeration was provided 2016
Pinus taeda There was a shift toward finer diameter roots in elevated CO2 plots compared with ambient plots, and 99% of the total root length sampled had a diameter < 2 mm. The average diameter of the entire pool of roots present in monoliths was significantly smaller in elevated CO2 plots (P < 0.001) Beidler et al.,
2015

3.1 Soil moisture

Soil moisture is a primary factor that affects the spatial distribution of root systems. When moisture is distributed nonuniformly, roots of several plant species can distinguish between a moist surface and the air environment; their lateral roots and root hairs are positioned toward the area with sufficient moisture by a patterning mechanism. Bao et al. (2014) described this phenomenon as hydropatterning. When water is scarce, plant growth is directly inhibited, root length is shortened, but the rooting depth and density increase in some species (Liu et al., 2019; Dhanapal et al., 2021).
At present, research on the effect of soil moisture on RSA is focused mainly on herbaceous plants. A recent study investigated the root traits of 18 Mediterranean seedlings across three moisture levels (11.5%, 17.8%, and 25.3%); the results showed that drought increased the root mass fraction, decreased the relative proportion of thin roots, and lowered the rates of root elongation and growth. Specifically, root diameter increased, and root length decreased. The study also indicated that drought may decrease nitrogen uptake, contributing to stunted root growth (Larson and Funk, 2016). Few studies have explored the relationship between RSA and soil water content in trees and shrubs, but their findings have been broadly consistent with those from herbaceous plants. Coordination between RSA and soil water use strategy has been discussed, and one study showed that deep rooting characteristics were closely related to water absorption ability in the deep soil. Deep roots with a large diameter and a low specific root length increase the plant’s ability to extract water from deep soil (Fort et al., 2017).
Excessive water (e.g. flooding) can also damage root systems and cause their spatial distribution to change. Waterlogging significantly decreased root length, root length density, and number of root tips of summer maize (Zea mays L.) (Ren et al., 2016). However, the effect of excessive water on root systems is caused primarily by hypoxia, and these effects will be discussed under soil aeration, below. Some recent studies have also found that certain xerophytes increase root systems growth when faced with drought stress (Alvarez-Flores et al., 2014), and this may represent a stress response to adversity.

3.2 Soil nutrients

Fertilizer-oriented growth is one characteristic of root systems. When nutrient elements are distributed nonuniformly in the soil, root systems will proliferate in the soil space that contains adequate nutrients by adjusting their metabolic response (Liang et al., 2018). This change in RSA can be regarded as a plastic response to a lack of soil nutrients (Niu et al., 2013). When they encounter a nutrient-rich soil zone, root systems often proliferate within it. It should be noted that root morphological responses are not consistent among different species, and even within a species, the size of the response depends on the magnitude of the heterogeneity (Hodge, 2004). At the community level, root growth rate was positively correlated with soil fertility, whereas root tissue density and branching rate were negatively correlated with soil fertility. On a large scale fertility gradient that contained ectomycorrhizal angiosperms, specific root length was negatively correlated with soil fertility, whereas root diameter was positively correlated with soil fertility (Kramer-Walter et al., 2016). At the species level, a substantial amount of research has been performed on the effects of nutrient deficiency on RSA. Nitrogen (N) is the main nutrient element for plants, and it is also the main limiting factor for root growth and development (Kant, 2018). When soil was deficient in N, the length of the primary root increased, lateral root elongation was reduced, and the fractal dimension of the root systems decreased. But under extreme nitrogen deficiency, the growth of the primary root was also reduced (Krouk et al., 2010; Gruber et al., 2013). In addition, the timing of N deficiency can also effect root growth and architecture: early nitrogen deficiency is beneficial to deeper soil root growth in wheat (Tian et al., 2019). Phosphorus (P) is also an essential element for plants (Chen et al., 2021). Under P deficiency, the growth of the primary root is inhibited and its length reduced, while at the same time the growth of lateral roots is promoted and the number of root hairs increases. The whole root systems present a dense spatial distribution (Niu et al., 2013; Péret et al., 2014). Changes in whole RSA can increase the specific surface area of root systems, markedly increasing nutrient absorption from the soil.
Recent research on the influence of soil nutrients on RSA has focused mainly on N and P, and the mechanisms that underlie their effects are now relatively clear. However, there has been far less research on other nutrients (Kawa et al., 2016). Finally, it is important to note that nutrient availability also depends on other factors, such as soil moisture, soil pH, microbial activity, redox potential, and organic matter content (Giehl and Wiren, 2014).

3.3 Soil temperature

Heat is one of the most basic energy forms for plant growth and development, and the most direct manifestation of heat is temperature. Although root systems do not display obvious light-responsive growth like aboveground plant parts, soil temperature does affect their growth.
Cold stress can affect gene expression and functional pathways in maize root systems (Ma et al., 2019). In warm soil, regardless of warming mode or location, trees from two spruce stands formed longer and less branched absorbent roots with higher specific root lengths and areas and lower root tissue densities (Parts et al., 2019). However, this does not imply that higher temperatures produce better root systems growth. Higher soil temperatures can accelerate roots senescence in spring maize (Zea mays L.), thereby reducing root biomass accumulation (Lu et al., 2020). In experiments that manipulated the soil temperature of Norway spruce (Picea abies), root mortality was also highest in the warmed soil (Majdi and Öhrvik, 2004; Kilpeläinen et al., 2019). The effect of temperature on root growth also differs among seasons. A full-year experiment demonstrated that any positive response to temperature was short-lived and that over the full growing season, soil warming led to a reduction in root number and mass due to increased root death during the autumn and winter (Edwards et al., 2004).
At present, the mechanisms by which soil temperature affects RSA are unclear, and some disputes remain. Some studies have suggested that soil temperature changes are caused primarily by changes in other soil properties (such as soil moisture, nutrients, etc.), thus leading to changes in RSA.

3.4 Soil aeration

Root systems grow in the soil and must acquire oxygen in order to generate energy through respiration and maintain their growth, development, and function. Therefore, soil aeration is often considered to be one of the most important indexes of soil fertility.
In compacted soil, insufficient aeration can result in a state of low energy supply; root tips must apply growth pressure to overcome the resistance of the surrounding soil, and the root systems growth is hindered, root elongation is decreased, and in severe cases, even death may result (Kolb et al., 2017). The objective of one study was to examine the effects of aeration levels on the RSA of potted tomato plants (Solanum lycopersicum). The results showed that total root length, surface area, and volume all increased with increasing aeration. The effect on fine roots (especially roots with a diameter of ~1 mm) was more obvious (Li et al., 2019). This study also demonstrated that soil aeration could counteract the negative effects of NaCl stress. Another fractional factorial experiment was designed to study the response of greenhouse-produced muskmelon root systems to different frequencies of supplemental soil aeration. In this case, total length and surface area were significantly increased, and aeration effects were due primarily to changes in these morphological parameters for roots ≤1 mm diameter (Li et al., 2016).
At present, the effect of soil CO2 on RSA is unclear. Most studies have focused on the effects of elevated atmospheric CO2 concentration on root systems growth, and there are differences of opinion regarding its effects on RSA. One study investigated the morphological response of fine roots exposed to atmospheric CO2 enrichment for 14 years in a Pinus taeda forest. The results showed that CO2 promoted the growth of fine roots, and the positive effect of high CO2 concentrations on root growth was greater than that of mycorrhizae (Beidler et al., 2015). Additional research is needed to explore the extent to which elevated atmospheric CO2 affects soil CO2 concentrations, and thereby influences RSA.

3.5 Other soil factors

RSA is also affected by rhizosphere microorganisms, heavy metals, and other factors like soil compaction, salinity, and pH. Some studies have shown that a consortium can be formed among the rhizosphere soil microflora, root systems, and the soil, which together can affect the development of RSA (Vidal et al., 2018). Soil microorganisms and their ecological interactions with roots can have potential effects on root systems growth and traits, as different mycorrhizal species can influence the secretion of root phytohormones under normal and stress conditions (Saleem et al., 2018). However, our understanding of these microorganisms remains limited because mainstream research has focused on rhizobia, arbuscular mycorrhizae, and important pathogens, which make up only a small part of the soil microflora. In addition, because of the limitations of research techniques, previous research methods have focused on the interactions between RSA and individual microorganisms in the laboratory, and the laboratory environment cannot fully reflect the real situation in the field (Xiong et al., 2021). The content of heavy metals in the soil also affects the growth and development of root systems. Some heavy metals are essential for plant growth (iron, manganese, zinc, copper, nickel, etc), whereas others are not essential and even toxic to plant growth (cadmium, lead, chromium, arsenic, mercury, etc.) (Bhatti et al., 2018; Hattab et al., 2018; Xie et al., 2018). When their concentrations are high, these heavy metals can damage membrane systems and antioxidant systems, resulting in chromosomal aberration, affecting metal ion homeostasis, and thereby causing toxic effects on roots (Anjum et al., 2015). Soil compaction can also create unfavorable growth conditions for root development and production. A study on the effect of compaction on the RSA of grass/red clover mixtures found that compaction caused differences in root parameters, primarily a reduction in root biomass and length in the 5-15 cm soil layer (Głąb, 2013). Another study on the effects of soil compaction on forage quality in the Brazilian savanna showed that increasing soil compaction caused changes in the fermentation and nutrient properties of forage and silage (Linhares et al., 2020). Studies have shown that the effect of compaction on root architecture is mainly due to its negative impact on soil physical properties. For example, compaction can significantly reduce soil density and increase soil water content, thereby affecting normal root physiological functions (Orzech et al., 2021). From the perspective of plant cultivation, especially in a saline-alkali environment, salinity stress appears to be an important factor that restricts plant roots growth. As salinity increases, ion concentrations and composition ratios in and around the roots change, resulting in ion toxicity and thereby affecting root growth and architecture (Parihar et al., 2014). Soil pH is another important factor that affects the development of plant roots. A study simulating the effect of acid rain on root growth found that root biomass was significantly lower in seedlings exposed to pH 3.0 than in the controls, and RSA was markedly affected by pH (Ramlall et al., 2015). In addition, fire can also affect the RSA of plants. Studies have shown that fire disturbance has a strong effect on the morphological traits of <0.5 mm roots, and higher length and lower tissue density of very fine roots have been reported following wildfire (Makita et al., 2016).
However, some studies have also shown that the presence of a specific element may reduce the harm caused by other factors. It has been widely reported that as the second most abundant element in soil, silicon can alleviate drought and salt stress in plants (Rizwan et al., 2015). In summary, RSA often results from a combination of factors. When one factor inhibits the growth of root systems, other unfavorable factors may aggravate this effect. At the same time, the mutual restriction of different factors may also reduce the effect of a single factor (Fig. 2).
Fig. 2 Factors affecting RSA and their interrelationships

4 Research methods for studying RSA

Root systems are complex and dynamic entities that grow in multiphase, composite, and opaque soil. Compared with aboveground plant parts, it is very difficult to perform direct research on RSA (Schnepf et al., 2018). Now, supported by modern technology, research methods for studying RSA include harvesting, two-dimensional morphological observation, and three-dimensional image reconstruction (Table 2). These methods contribute to understanding root biomass, length distribution, and geometry or structure. By taking multiple measurements, it is possible to obtain some information on the growth or turnover rate of root systems over time (Ogilvie et al., 2021).
Table 2 Characteristics of RSA research methods
Research method Mature technologies Advantages Limitations
Harvesting Digging tool
Weighing tool
Washing tool		 Root systems can be well represented It is time-consuming to dig and clean the roots;
The lateral roots are lost during cleaning with water;
Plants may suffer irreversible damage and even death
Two-dimensional
morphological observation		 Minirhizotron technology
Simulation modeling
Image recognition technology		 Root systems are measured digitally in situ;
Non-destructive, direct observation of fixed points		 There are some errors in automatic image analysis;
Manual image analysis requires significant labor and material resources
Three-dimensional image reconstruction Ground penetrating radar
Magnetic resonance imaging
X-ray computed tomography		 Omni-directional, three-dimensional observation
of root systems can be achieved;
Non-destructive observation		 Excessive water content and uneven soil texture will interfere with the results;
Paramagnetic elements in soil can interfere with signals;
It is difficult to detect root systems composed of thick and thin roots

4.1 Harvesting method

Direct harvesting of roots from soil is the most traditional method of root systems research. Notably, it is the most mature method. RSA can be well represented by digging the soil around root systems. This method is widely used to explore the characteristics, functions, and ecological adaptation strategies of root systems (Augusto et al., 2015). At the same time, this method can also be used as a reference for other methods, such as 2D morphological observation, and 3D image reconstruction. However, in the field, it is time consuming to dig soil samples and clean soil from root systems, even with the assistance of advanced automation equipment. In actual operation, it is very difficult to distinguish the target roots (especially fine roots) from those of other plants. Meanwhile, fine roots and root hairs are lost in the process; even using a sieve with a mesh size of 0.2 mm2, dry weight losses of 20% to 40% may occur (Judd et al., 2015). At the same time, irreversible damage and even plant death can occur after root harvesting, and this is a major disadvantage of the harvesting method. More recently, the use of the harvesting method has declined as computer technology has improved and the measurement of root growth characteristics has become easier.

4.2 Two-dimensional morphological observation

Two-dimensional morphological observation methods have been used to measure the primary root, lateral roots, and adventitious roots digitally in situ using pinboards, rhizotrons, minirhizotrons, WinRhizo image scanning technology, the RootTyp model, and other approaches (Pateña and Ingram, 2000; Judd et al., 2015). RSA parameters can be acquired after uploading images to a computer and processing them with image analysis software. Two-dimensional observation is widely used to study the architecture of fine roots in crops. It involves the non-destructive, direct observation of fixed points and combines traditional minirhizotron technology, simulation modeling, and image analysis (Kawa et al., 2016; Kilpeläinen et al., 2019). This approach enables better observation of root systems function and growth dynamics (Schnepf et al., 2018). As a feasible way to study RSA, in addition to measuring root growth, angle, and spatial structure, rhizotrons and minirhizotrons can also be used to monitor fine root growth, development, and decomposition rate. Rhizotrons and minirhizotrons have been used to measure various aspects of soil root interactions, sample specific types of roots in the field, and to observe root symbionts and natural components of the soil biosphere (fungi, invertebrates, etc.). However, there are significant challenges associated with in situ rhizotrons. First, installing many observation ports can cause serious damage to the soil profile, and ensuring that root systems are present near the observation ports is also a significant challenge (Ogilvie et al., 2021). WinRhizo is a professional root analysis system that is typically used after roots are washed from soil. Because of its powerful functions and simple operation, WinRhizo is widely used in the study of RSA; the shape, color, diameter and length of root systems can be determined by WinRhizo image analysis (Bodner et al., 2014; Perkons et al., 2014). However, during the washing process, some fine roots may be lost. The RootTyp model is a generic model for many species that can differentiate among several root types. This model has been used in recent years because it is easy to calibrate for several species with different structures and to simulate root development. With continued, some limitations have been exposed; the geometry of fine roots may not be measured precisely, the parameter values of the model database are not best suited to every developmental stage, and some root types are not yet present (Cast et al., 2019). Finally, two-dimensional morphological observation still has some limitations; for example, very fine (<0.2 mm diameter) and dead roots cannot be accurately identified with current image analysis software (Bodner et al., 2014). In addition, some errors occur in automatic image analysis, but manual image analysis requires significant labor and material resources.

4.3 Three-dimensional image reconstruction

Three-dimensional image reconstruction is a quantitative research method for the analysis of RSA that has developed gradually over recent years. Based on non-destructive observation technology, it can achieve omnidirectional, three- dimensional observations of root systems (Gribbe et al., 2020). At present, mature technologies include ground penetrating radar (GPR), magnetic resonance imaging (MRI), X-ray computed tomography (XCT), neutron computed tomography (neutron CT), and others (Koch et al., 2019). For GPR observation, a GPR antenna consisting of an electromagnetic transmitter and receiver is pulled cross-section to propagate electromagnetic waves into the soil at specific intervals (typically 100 -200 per m). The receiver accurately records the arrival time and amplitude of the energy reflected from buried objects and returned to the soil surface. Based on the dielectric properties of the soil, 3D maps of RSA can be constructed (Butnor et al., 2016). At present, GPR is used mainly to study coarse roots (diameter >0.5 cm); it can minimize damage to plants and the environment while achieving high accuracy (Zou et al., 2020). There have also been some problems with the use of GPR for root systems observation. For example, excessive water content and uneven soil texture can interfere with its results to some extent. Therefore, GPR is restricted to specific soil conditions (such as dry sandy soils) that are not prone to signal attenuation. The roots (taproot + lateral root) beneath tree stumps are underestimated, and lateral roots adjacent to trees also lead to considerable uncertainty (Samuelson et al., 2014; Guo et al., 2015). MRI uses electromagnetic field gradients as information carriers and provides data on the spatial morphology of root systems by detecting different resonance signals (Pflugfelder et al., 2017). In recent years, MRI has been used as a 3D, noninvasive and continuous technique to map RSA (Perelman et al., 2020). When MRI is used to reconstruct RSA in three or four (space and time) dimensions, or to evaluate the structural-function relationships of root systems, the simulated and observed quantitative information are similar, but their actual values may differ. A possible explanation is that aspects of the rhizosphere environment, such as water content, may influence the simulation results (Gribbe et al., 2020). Furthermore, paramagnetic elements in soil can also interfere with MRI signals and greatly influence the results. XCT is a 3D architectural method that uses X-rays as the information carriers; it provides data on root systems by detecting the attenuation coefficient of X-rays that have passed through an object (Kettridge and Binley, 2015; Gharedaghloo et al., 2018). XCT technology causes no damage to the soil, plants, or environment and can characterize the RSA of individual plants or sample plots (Cercioglu et al., 2018). Overall, three-dimensional image reconstruction is currently the most suitable non-destructive technology for RSA research (Mooney et al., 2012), but it still has limitations. For example, it is difficult to detect root systems that are composed of thick and thin roots (Metzner et al., 2015). The thickness of root systems, theirs water content, and the distance between root systems can affect measurement accuracy (Hirano et al., 2009).

5 Conclusions

To date, a number of insights into RSA have been acquired, especially in the fields of agriculture and crop science. As an important indicator of root structure and function, RSA plays a critical role in plant physiological health. There is increasing evidence that RSA is an important aspect of root systems function and plant performance. Researchers have striven to explore RSA in different habitats in order to understand the impact of environmental factors on root systems growth and, on this basis, to improve plant plasticity. Advances in this field will potentially underpin future developments and innovation in the selection and breeding of more robust crops, shrubs, and trees. Some studies has been devoted to understanding how RSA development affects the long-term performance of plants (especially trees); that is, the spatial structure and development level of RSA in young plants may affect their health throughout their life cycle. Once healthy and intact RSA has been damaged, recovery takes a long time, and the effects are often delayed. These studies have provided significant insight. Other studies have focused on the controlled field environment, and additional data has been provided through comparative studies, providing a useful reference for future research.
Having summarized previous research work, we propose the following suggestions. First, rhizosphere microorganisms play an important role in the regulation of RSA. The regulatory mechanisms and modes of action by which rhizosphere microorganisms influence RSA should be thoroughly explored from multiple standpoints, including plant physiology, plant nutrition, and plant cultivation. Meanwhile, different root systems show different textures, colors, and morphologies. At the same time, more accurate and convenient in situ observation methods are urgently needed to resolve the current difficulty in distinguishing living and dead roots. Each emerging method for RSA quantification (such as rhizotrons, minirhizotrons, MRI, and XCT, etc.) has some limitations in application, and more advanced tomographic imaging technologies should therefore be applied to this field, and the study of controlled environment should not be neglected. When performing research on RSA, one method or a combination of methods should be selected based on plant species, environmental conditions, and technical considerations. Therefore, when carrying out a specific study, it is necessary to verify the applicability and accuracy of the relevant methods and models selected or established. By making comparisons and corrections, the most appropriate research method will be selected, thereby accurately assessing and simulating the spatial distribution of roots and their relationship with the surrounding environment. Finally, RSA can objectively reflect the plasticity of root systems in relation to the external environment and establish a connection between the plant and the environment. Therefore, exploring the relationships among RSA, the environment, and ecosystem functions at multiple temporal and spatial scales is very important. With in-depth research and the use of advanced technology, we believe that research on RSA will produce significant breakthroughs in the near future.

References

Publishing order | Descend order by publishing year | Descend order by cited within
[1]
Alvarez-Flores R, Winkel T, Nguyen-Thi-truc A, et al. 2014. Root foraging capacity depends on root system architecture and ontogeny in seedlings of three Andean Chenopodium species. Plant and Soil, 380(1-2): 415- 428.

DOI

[2]
Anjum S A, Tanveer M, Hussain S, et al. 2015. Cadmium toxicity in maize (Zea mays L.): Consequences on antioxidative systems, reactive oxygen species and cadmium accumulation. Environmental Science and Pollution Research, 22(21): 17022-17030.

DOI

[3]
Armengaud P, Zambaux K, Hills A, et al. 2009. EZ-Rhizo: Integrated software for the fast and accurate measurement of root system architecture. The Plant Journal, 57(5): 945-956.

DOI PMID

[4]
Augusto L, Achat D L, Bakker M R, et al. 2015. Biomass and nutrients in tree root systems-sustainable harvesting of an intensively managed Pinus pinaster (Ait.) planted forest. GCB Bioenergy, 7(2): 231-243.

DOI

[5]
Badhon F F, Islam M S, Islam M A, et al. 2021. A simple approach for estimating contribution of vetiver roots in shear strength of a soil-root system. Innovative Infrastructure Solutions, 6(2): 1-13.

DOI

[6]
Bai H, Li R, Wang W, et al. 2021. Investigation on parameter calibration method and mechanical properties of root-reinforced soil by DEM. Mathematical Problems in Engineering, 27(2): 1-18.

[7]
Bao Y, Aggarwal P, Robbins N E, et al. 2014. Plant roots use a patterning mechanism to position lateral root branches toward available water. Proceedings of the National Academy of Sciences of the USA, 111(25): 9319-9324.

DOI

[8]
Barbosa R S, de Souza Z M, Carneiro M P, et al. 2021. Root system and its relations with soil physical and chemical attributes in orange culture. Applied Sciences, 11(4): 1790. DOI: 10.3390/app11041790.

DOI

[9]
Beidler K V, Taylor B N, Strand A E, et al. 2015. Changes in root architecture under elevated concentrations of CO2 and nitrogen reflect alternate soil exploration strategies. New Phytologist, 205(3): 1153-1163.

DOI

[10]
Bhatti S S, Sambyal V, Nagpal A K. 2018. Analysis of genotoxicity of agricultural soils and metal (Fe, Mn, and Zn) accumulation in crops. International Journal of Environmental Research, 12(4): 439-449.

DOI

[11]
Bodner G, Leitner D, Kaul H P. 2014. Coarse and fine root plants affect pore size distributions differently. Plant and Soil, 380(1-2): 133-151.

PMID

[12]
Bot J L, Serra V, Fabre J, et al. 2010. DART: A software to analyse root system architecture and development from captured images. Plant and Soil, 326(1): 261-273.

DOI

[13]
Butnor J R, Samuelson L J, Stokes T A, et al. 2016. Surface-based GPR underestimates below-stump root biomass. Plant and Soil, 402(1-2): 47-62.

DOI

[14]
Cast S C, Meredieu C, Défossez P, et al. 2019. Modelling root system development for anchorage of forest trees up to the mature stage, including acclimation to soil constraints: The case of Pinus pinaster. Plant and Soil, 439(1-2): 405-430.

DOI

[15]
Cercioglu M, Anderson S H, Udawatta R P, et al. 2018. Effects of cover crop and biofuel crop management on computed tomography-measured pore parameters. Geoderma, 319(1): 80-88.

DOI

[16]
Chen H, Wang Y, Yuan J, et al. 2021. Effect of P fertilizer reduction regime on soil Olsen-P, root Fe-plaque P, and rice P uptake in rice-wheat rotation paddy fields. Pedosphere, 31(1): 94-102.

DOI

[17]
Colombi T, Torres L C, Walter A, et al. 2018. Feedbacks between soil penetration resistance, root architecture and water uptake limit water accessibility and crop growth—A vicious circle. Science of the Total Environment, 626: 1026-1035.

DOI

[18]
De Bauw P, Mai T H, Schnepf A, et al. 2020. A functional-structural model of upland rice root systems reveals the importance of laterals and growing root tips for phosphate uptake from wet and dry soils. Annals of Botany, 126(4): 789-806.

DOI PMID

[19]
Dhanapal A P, York L M, Hames K A, et al. 2021. Genome-wide association study of topsoil root system architecture in field-grown soybean [Glycine max (L.) Merr.]. Frontiers in Plant Science, 11: 590179. DOI: 10.3389/fpls.2020.590179.

DOI

[20]
Edwards E J, Benham D G, Marland L A, et al. 2004. Root production is determined by radiation flux in a temperate grassland community. Global Change Biology, 10(2): 209-227.

DOI

[21]
Finér L, Ohashi M, Noguchi K, et al. 2011. Factors causing variation in fine root biomass in forest ecosystems. Forest Ecology and Management, 261(2): 265-277.

DOI

[22]
Fitter A H, Stickland T R, Harvey M L, et al. 1991. Architectural analysis of plant root systems. 1. Architectural correlates of exploitation efficiency. New Phytologist, 118(3): 375-382.

DOI

[23]
Fort F, Volaire F, Guilioni L, et al. 2017. Root traits are related to plant water-use among rangeland Mediterranean species. Functional Ecology, 31(9): 1700-1709.

DOI

[24]
Gharedaghloo B, Price J S, Rezanezhad F, et al. 2018. Evaluating the hydraulic and transport properties of peat soil using pore network modeling and X-ray micro computed tomography. Journal of Hydrology, 561(2): 494-508.

DOI

[25]
Giehl R F H, von Wirén N. 2014. Root nutrient foraging. Plant Physiology, 166(2): 509-517.

DOI PMID

[26]
Głąb T. 2013. Effect of tractor traffic and N fertilization on the root morphology of grass/red clover mixture. Soil and Tillage Research, 134(8): 163-171.

DOI

[27]
Gribbe S, Blume-Werry G, Couwenberg J. 2020. Digital, three-dimensional visualization of root systems in peat. Soil Systems, 4(1): 13. DOI: 10.3390/soilsystems4010013.

DOI

[28]
Gruber B D, Giehl R F, Friedel S, et al. 2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology, 163(1): 161-179.

DOI

[29]
Guo L, Liu Y, Wu G L, et al. 2019. Preferential water flow: Influence of alfalfa (Medicago sativa L.) decayed root channels on soil water infiltration. Journal of Hydrology, 578: 124019. DOI: 10.1016/j.jhydrol.2019.124019.

DOI

[30]
Guo L, Wu Y, Chen J, et al. 2015. Calibrating the impact of root orientation on root quantification using ground-penetrating radar. Plant and Soil, 395(1-2): 289-305.

DOI

[31]
Hattab S, Bougattass I, Hassine R, et al. 2018. Metals and micronutrients in some edible crops and their cultivation soils in eastern-central region of Tunisia: A comparison between organic and conventional farming. Food Chemistry, 270(1): 293-298.

DOI

[32]
Hirano Y, Dannoura M, Aono K, et al. 2009. Limiting factors in the detection of tree roots using ground-penetrating radar. Plant and Soil, 319(1-2): 15-24.

DOI

[33]
Hodge A. 2004. The plastic plant: Root responses to heterogeneous supplies of nutrients. New Phytologist, 162(1): 9-24.

DOI

[34]
Judd L A, Jackson B E, Fonteno W C. 2015. Advancements in root growth measurement technologies and observation capabilities for container-grown plants. Plants, 4(3): 369-392.

DOI

[35]
Kant S. 2018. Understanding nitrate uptake, signaling and remobilisation for improving plant nitrogen use efficiency. Seminars in Cell & Developmental Biology, 74(4): 89-96.

[36]
Kawa D, Julkowska M M, Sommerfeld H M, et al. 2016. Phosphate-dependent root system architecture responses to salt stress. Plant Physiology, 172(2): 690-706.

PMID

[37]
Kenrick P, Strullu-Derrien C. 2014. The origin and early evolution of roots. Plant Physiology, 166(2): 570-580.

DOI PMID

[38]
Kettridge N, Binley A. 2011. Characterization of peat structure using X-ray computed tomography and its control on the ebullition of biogenic gas bubbles. Journal of Geophysical Research, 116(G1): G01024. DOI: 10.1029/2010JG001478.

DOI

[39]
Kilpeläinen J, Domisch T, Lehto T, et al. 2019. Root and shoot phenology and root longevity of Norway spruce saplings grown at different soil temperatures. Canadian Journal of Forest Research, 49(11): 1441-1452.

DOI

[40]
Koch A, Meunier F, Vanderborght J, et al. 2019. Functional-structural root-system model validation using a soil MRI experiment. Journal of Experimental Botany, 70(10): 2797-2809.

DOI PMID

[40]
Koch A, Meunier F, Vanderborght J, et al. 2019. Functional-structural root-system model validation using a soil MRI experiment. Journal of Experimental Botany, 70(10): 2797-2809.

[41]
Kolb E, Legué V, Bogeat-Triboulot M B. 2017. Physical root-soil interactions. Physical Biology, 14(6): 065004. DOI: 10.1088/1478-3975/aa90dd.

DOI

[42]
Kramer-Walter K R, Bellingham P J, Millar T R, et al. 2016. Root traits are multidimensional: Specific root length is independent from root tissue density and the plant economic spectrum. Journal of Ecology, 104(5): 1299-1310.

DOI

[43]
Krouk G, Lacombe B, Bielach A, et al. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell, 18(6): 927-937.

DOI PMID

[44]
Larson J E, Funk J L. 2016. Seedling root responses to soil moisture and the identification of a belowground trait spectrum across three growth forms. New Phytologist, 210(3): 827-838.

DOI PMID

[45]
Leitner D, Klepsch S, Ptashnyk M, et al. 2010. A dynamic model of nutrient uptake by root hairs. New Phytologist, 185(3): 792-802.

DOI PMID

[46]
Li Y, Niu W, Cao X, et al. 2019. Effect of soil aeration on root morphology and photosynthetic characteristics of potted tomato plants (Solanum lycopersicum) at different NaCl salinity levels. BMC Plant Biology, 19(1): 331. DOI: 10.1186/s12870-019-1927-3.

DOI PMID

[47]
Li Y, Niu W, Xu J, et al. 2016. Root morphology of greenhouse produced muskmelon under sub-surface drip irrigation with supplemental soil aeration. Scientia Horticulturae, 201: 287-294.

DOI

[48]
Liang Y, Zhao X Y, Jones A M, et al. 2018. G proteins sculp root architecture in response to nitrogen in rice and Arabidopsis. Plant Science, 274(3): 129-136.

DOI

[49]
Linhares A, Gonalves W G, Cabral S M, et al. 2020. Soil compaction affects the silage quality of sunflower and Paiaguas palisadegrass (Brachiaria brizantha) grown on a Latosol in the Brazilian savanna. Australian Journal of Crop Science, 14(7): 1121-1130.

[50]
Liu Y, Miao H, Chang X, et al. 2019. Higher species diversity improves soil water infiltration capacity by increasing soil organic matter content in semiarid grasslands. Land Degradation & Development, 30(13): 1599-1606.

DOI

[51]
Lu H, Xia Z, Fu Y, et al. 2020. Response of soil temperature, moisture, and spring maize (Zea mays L.) root/shoot growth to different mulching materials in semi-arid areas of Northwest China. Agronomy, 10(4): 453. DOI: 10.3390/agronomy10040453.

DOI

[52]
Lynch J. 1995. Root architecture and plant productivity. Plant Physiology, 109(1): 7-13.

PMID

[53]
Ma Y, Li S, Lin H, et al. 2019. Effect of cold stress on gene expression and functional pathways in maize root system. Grassland Science, 65(4): 249-256.

DOI

[54]
Majdi H, Öhrvik J. 2004. Interactive effects of soil warming and fertilization on root production, mortality, and longevity in a Norway spruce stand in Northern Sweden. Global Change Biology, 10(2): 182-188.

DOI

[55]
Makita N, Pumpanen J, Köster K, et al. 2016. Changes in very fine root respiration and morphology with time since last fire in a boreal forest. Plant and Soil, 402(1-2): 303-316.

DOI

[56]
Metzner R, Eggert A, van Dusschoten D, et al. 2015. Direct comparison of MRI and X-ray CT technologies for 3D imaging of root systems in soil: Potential and challenges for root trait quantification. Plant Methods, 11: 17. DOI: 10.1186/s13007-015-0060-z.

DOI PMID

[57]
Moldovan M, Tăut L, Dîrja M. 2020. Studies on the role of improvement perimeters in preventing and combating soil erosion. Journal of Agricultural and Crop Research, 8(9): 192-199.

DOI

[58]
Mooney S J, Pridmore T P, Helliwell J, et al. 2012. Developing X-ray computed tomography to non-invasively image 3-D root systems architecture in soil. Plant and Soil, 352(1-2): 1-22.

DOI

[59]
Niu Y F, Chai R S, Jin G L, et al. 2013. Responses of root architecture development to low phosphorus availability: A review. Annals of Botany, 112(2): 391-408.

DOI PMID

[60]
Ogilvie C M, Ashiq W, Vasava H B, et al. 2021. Quantifying root-soil interactions in cover crop systems: A review. Agriculture, 11(3): 218. DOI: 10.3390/agriculture11030218.

DOI

[61]
Orzech K, Wanic M, Zauski D. 2021. The effects of soil compaction and different tillage systems on the bulk density and moisture content of soil and the yields of winter oilseed rape and cereals. Agriculture, 11: 666. DOI: 10.3390/agriculture11070666.

DOI

[62]
Parihar P, Singh S, Singh R, et al. 2015. Effect of salinity stress on plants and its tolerance strategies: A review. Environmental Science and Pollution Research, 22(6): 4056-4075.

DOI

[63]
Parts K, Tedersoo L, Schindlbacher A, et al. 2019. Acclimation of fine root systems to soil warming: Comparison of an experimental setup and a natural soil temperature gradient. Ecosystems, 22(3): 457-472.

DOI

[64]
Pateña G, Ingram K T. 2000. Digital acquisition and measurement of peanut root minirhizotron images. Agronomy Journal, 92(3): 541-544.

DOI

[65]
Perelman A, Lazarovitch N, Vanderborght J, et al. 2020. Quantitative imaging of sodium concentrations in soil-root systems using magnetic resonance imaging (MRI). Plant and Soil, 454(1-2): 171-185.

DOI

[66]
Péret B, Desnos T, Jost R, et al. 2014. Root architecture responses: In search of phosphate. Plant Physiology, 166(4): 1713-1723.

DOI PMID

[67]
Perkons U, Kautz T, Uteau D, et al. 2014. Root-length densities of various annual crops following crops with contrasting root systems. Soil and Tillage Research, 137(11): 50-57.

DOI

[68]
Pflugfelder D, Metzner R, van Dusschoten D, et al. 2017. Non-invasive imaging of plant roots in different soils using magnetic resonance imaging (MRI). Plant Methods, 13: 102. DOI: 10.1186/s13007-017- 0252-9.

DOI

[69]
Ramlall C, Varghese B, Ramdhani S, et al. 2015. Effects of simulated acid rain on germination, seedling growth and oxidative metabolism of recalcitrant-seeded Trichilia dregeana grown in its natural seed bank. Physiologia Plantarum, 153(1): 149-160.

DOI

[70]
Ren B, Zhang J, Dong S, et al. 2016. Root and shoot responses of summer maize to waterlogging at different stages. Agronomy Journal, 108(3): 1060-1069.

DOI

[71]
Rizwan M, Ali S, Ibrahim M, et al. 2015. Mechanisms of silicon-mediated alleviation of drought and salt stress in plants: A review. Environmental Science and Pollution Research, 22(20): 15416-15431.

DOI

[72]
Safitri L, Suryanti S, Kautsar V, et al. 2018. Study of oil palm root architecture with variation of crop stage and soil type vulnerable to drought. IOP Conference Series: Earth and Environmental Science, 141: 012031. DOI: 10.1088/1755-1315/141/1/012031.

[73]
Saleem M, Law A D, Sahib M R, et al. 2018. Impact of root system architecture on rhizosphere and root microbiome. Rhizosphere, 6(2): 47-51.

DOI

[74]
Samuelson L J, Stokes T A, Butnor J R, et al. 2014. Ecosystem carbon stocks in Pinus palustris forests. Canadian Journal of Forest Research, 44(5): 476-486.

DOI

[75]
Schnepf A, Leitner D, Landl M, et al. 2018. CRootBox: A structural-functional modelling framework for root systems. Annals of Botany, 121(5): 1033-1053.

DOI PMID

[76]
Shahzad Z, Amtmann A. 2017. Food for thought: How nutrients regulate root system architecture. Current Opinion in Plant Biology, 39(4): 80-87.

DOI

[77]
Tian Z, Liu X, Yu J, et al. 2019. Early nitrogen deficiency favors high nitrogen recovery efficiency by improving deeper soil root growth and reducing nitrogen loss in wheat. Archives of Agronomy and Soil Science, 66(10): 1384-1398.

DOI

[78]
Tran A T P, Chang I, Cho G C. 2019. Soil water retention and vegetation survivability improvement using microbial biopolymers in drylands. Geomechanics and Engineering, 17(5): 475-483.

[79]
Vidal A, Hirte J, Bender S F, et al. 2018. Linking 3D soil structure and plant-microbe-soil carbon transfer in the rhizosphere. Frontiers in Environmental Science, 6: 9. DOI: 10.3389/fenvs.2018.00009.

DOI

[80]
Wang S, Meng X, Chen G, et al. 2017. Effects of vegetation on debris flow mitigation: A case study from Gansu Province, China. Geomorphology, 282: 64-73.

DOI

[81]
Xie L, Hao P, Cheng Y, et al. 2018. Effect of combined application of lead, cadmium, chromium and copper on grain, leaf and stem heavy metal contents at different growth stages in rice. Ecotoxicology and Environmental Safety, 162: 71-76.

DOI PMID

[82]
Xiong Q, Hu J, Wei H, et al. 2021. Relationship between plant roots, rhizosphere microorganisms, and nitrogen and its special focus on rice. Agriculture, 11(3): 234. DOI: 10.3390/agriculture11030234.

DOI

[83]
Zou L, Wang Y, Giannakis I, et al. 2020. Mapping and assessment of tree roots using ground penetrating radar with low-cost GPS. Remote Sensing, 12(8): 1300. DOI: 10.3390/rs12081300.

DOI

Options
Outlines

/

〈 〉