Tree root architecture – form and function

Over 25 years ago, Fitter (1982) recognized that the form (architecture) of the branching root system was almost certainly related to the acquisition of essential soil resources (function). Since then, there have been many studies that have advanced our understanding of how plasticity in the birth and death of lateral root branches might confer a competitive advantage on individual plants and may structure plant communities, and the topic continues to generate significant scientific interest and debate to this day (e.g. Kembel & Cahill, 2005; de Kroon & Mommer, 2006; Hodge, 2006; Grime, 2007; Kembel et al., 2008). The primary focus to this point in the ecological literature has been on understanding rates of root length proliferation and we know that root length can sometimes respond dramatically to increased availability of 'patchy' soil resources. However, missing from many studies of root proliferation and acquisition of essential soil resources is a detailed understanding of how plants have altered their form (morphology and especially anatomy). Guo et al. (this issue; pp. 673–683) make an important contribution by comparing the lateral root branch anatomy of 23 species of temperate trees. They address the following questions. How are multitasking temperate tree root systems designed? Is the branching root system anatomically similar across species? Are lateral branches constructed so that only the most distal roots are responsible for absorption of nutrients? 'The questions of how plant root systems are constructed and how their form is related to the capture of essential soil resources have intrigued ecologists and plant biologists for decades ...' Trees, like all plants growing in the wild, must solve a host of problems using their root systems. Root systems anchor the plant, sometimes from gale-force winds. Perennial plants have a growth rhythm designed to help the plant survive periods of cold, drought and defoliation, and roots (as well as shoots) store nonstructural carbohydrates to provide the plant with the energy it needs to survive changes in climate and periodic disturbances that alter whole-plant source–sink relationships. Roots are a part of the plant vascular system that takes up soil solution and transports water and other compounds (Pratt et al., 2008). Finally, roots and their associated symbiotic bacteria and fungi are responsible for fixing atmospheric nitrogen and acquiring the essential nutrients required for growth. The questions of how plant root systems are constructed, and how their form is related to the capture of essential soil resources, have intrigued ecologists and plant biologists for decades because we have learned that there can be as much variation in the availability of essential nutrients across 20 cm of soil as there is across an entire field or across a significant ecological gradient (Gross et al., 1995; Farley & Fitter, 1999). An interesting example of how microsite mineralization of soil nitrogen can be influenced by plant roots and their associated mycorrhizas is presented by Schimel & Bennett (2004). Plants are basically sessile organisms, so the only way that they can 'forage' for 'patchy' essential soil resources is to dynamically change their form or their physiology, or both. Lateral roots are the plant modules that grow and die on small spatial scales in the soil and they, along with their associated mycorrhizas, are primarily responsible for nutrient acquisition. Variations in the size, shape, surface area and demography of lateral branches and associated mycorrhizas, along with concomitant changes in root physiology, are the way in which a plant can 'forage' for water and nutrients in the soil. Lateral root branches arise in the pericycle of the parent root, grow through the cortex and form lateral branches, which are sometimes complex in their architecture (Pregitzer, 2002; Pregitzer et al., 2002). The plant root system can sense a change in resource availability in the soil and initiate new lateral roots in 'hot spots', places in the soil where essential resources are more available (Walch-Liu et al., 2006; Nibau et al., 2008). Some years ago, Grime (1965) argued that comparative patterns in trait variation could tell us something about functional specialization. This is essentially the approach that Guo et al. have taken. They systematically dissected the lateral branches of 23 species of temperate trees growing in China following the protocol of Pregitzer et al. (2002). They also quantified and used the anatomy of the distal root branches as a surrogate for distinguishing root branches involved in active metabolic uptake of nutrients vs transport and storage. In addition to quantifying the anatomy of branching root segments, they quantified which of the lateral branch orders were colonized by mycorrhizal fungi. The results of Guo et al. suggest that most of the active absorption of nutrients occurs in first-order roots, the tiny lateral branches at the very distal end of the root system (Pregitzer et al., 2002). Mycorrhizas were associated with the first three orders of roots, although the degree of activity of mycorrhizas in the second-order and third-order roots is not clear from their results. Based on the results of Guo et al. and what we know about the relationship between root nitrogen concentration and rates of root respiration (Reich et al., 2008), I suspect that the first-order roots are the primary carbon depot for mycorrhizal hyphae, which ramify away from the root tip to forage widely in the spatially and temporally heterogeneous soil. Guo et al. also found that the morphology and anatomy of the root system seems to be conserved within a species, an observation increasingly reported in the literature (Pregitzer et al., 2002; Kembel & Cahill, 2005; Grime, 2007). The implication is that different species have evolved specialized mechanisms to sense changes in the availability of essential soil resources and to alter their lateral branch architecture and demography to compete effectively for limiting water or nutrients (Walch-Liu et al., 2006; Nibau et al., 2008). However, the evolutionary costs and benefits of lateral root plasticity have not yet received the attention they deserve (de Kroon & Mommer, 2006). The results of Guo et al. raise several unanswered questions. To start with, the systematic dissection of lateral root branches into orders is an arbitrary approach. Granted, this systematic approach has led us to understand that most of the absorptive length and metabolic activity in tree roots is correlated with the distal ends of the branching root system (Pregitzer et al., 1998; Pregitzer et al., 2002; Reich et al., 2008). However, we still do not really understand the variation in morphology and anatomy of lateral branches that arise in the pericycle. We know that the plant can sense external changes in essential soil resources, alter endogenous factors that regulate lateral root development and produce a plastic response – but how plastic? Do trees primarily produce new first-order roots and alter mycorrhizal fungi associations in response to changing soil conditions or are new lateral branches more complex in architecture? Is lateral root branch architecture highly conserved within a species, or highly plastic? How heritable is lateral root branch architecture? One of the dangers in trying to make global generalizations about root form and function is the comparison of roots that differ significantly in how they are constructed and how active they are metabolically. Guo et al. demonstrate that root order predicts root anatomy fairly consistently across 23 species of temperate trees. However, if we were to compare trees with perennial forbs and annual grasses we would find a different outcome. Studies of root relative growth rate in 'patchy' soil mostly ignore the fact that lateral roots can differ dramatically in both form and function (Pregitzer, 2002). Cumulative evidence now strongly suggests that the lateral roots of trees vary in their construction and maintenance costs depending on their position on the branching root system. As time progresses and our understanding of tree root systems improves, it increasingly seems as if 'fine roots'– roots actively involved in the uptake of nutrients and roots that have short life expectancies – consist primarily of first-order to third-order lateral roots that arise dynamically from the pericycle in response to changes in soil resource availability. In reality, this generalization is a gross over-simplification. The distal branches of the perennial roots system are the hub of mycorrhizal activity and the host to root hairs (Fig. 1). A more detailed understanding of the dynamic and integrated 'root–fungal module' awaits the attention of innovative new studies. Clearly, the metabolic action in woody plants with complex lateral branching root systems is at the tips of the lateral root branches. It seems that the functional architecture of plant roots is as diverse and interesting as the functional architecture of shoots. Perhaps we should not be surprised by this because biotic diversity is high, competition is keen and resource capture is spatially and temporally complex in the patchy soil. Prunus pennslvanica L. (pin cherry) lateral root tip and associated roots hairs growing ('foraging') in a patch of nitrogen-enriched sandy soil at the University of Michigan Biological Station in 1989. Individual grains of sand and scores of root hairs are visible in the image. The outline shows the position of the root and root hairs 12 h previously. Lateral root architecture, root hairs and mycorrhizal hyphae are all responsive to changes in soil resource availability, but relationships between root form and function remain relatively poorly understood. (See Pregitzer et al., 1993 for details of this particular study.) This work was supported by the Division of Environmental Biology (Ecosystem Studies) of the National Science Foundation, the Office of Biological and Environmental Research (BER) of the Department of Energy, and the Nevada Agricultural Experiment Station. I am grateful for this support.