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Invited Special Paper |
2Department of Plant Biology, 228 Plant Science, Cornell University, Ithaca, New York 14853 USA; 3United States Department of Agriculture, Agricultural Research Service, Appalachian Farming Systems Research Center, 1224 Airport Road, Beaver, West Virginia 25813 USA
Received for publication March 21, 2002. Accepted for publication June 7, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONTHEORETICAL AND PRACTICAL BASIS...MATERIALS AND METHODSOBSERVATIONSDISCUSSIONLITERATURE CITED |
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Key Words: adventitious roots • branching • root turnover • roots
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONTHEORETICAL AND PRACTICAL BASIS...MATERIALS AND METHODSOBSERVATIONSDISCUSSIONLITERATURE CITED |
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; Reynolds, 1975
; Burke and Raynal, 1994
; Fahey and Hughes, 1994
; Eissenstat, Wells, and Yanai, 2000
; Gill and Jackson, 2000
; Norby and Jackson, 2000
; Baker et al., 2001
) establish the concept that a large proportion of the fine roots (
0.5 mm) in a root system are routinely shed, without contributing to further growth of the root system. Typically fine roots are emphasized as the absorptive component of a root system, because as roots enlarge in diameter they go through anatomical changes (Esau, 1965
) that appear to render them less likely to absorb substances from the soil. Although woody roots retain some ability to absorb water and nutrients (Kramer, 1983
; MacFall, Johnson, and Kramer, 1991
; Escamilla and Comerford, 2000
), the question remains, where does the next population of fine roots come from?
The expected answer to this question is that (1) growth from apical meristems of the main and branch roots and (2) new branch roots from the pericycle of preexisting roots in primary growth are the two sources that account for the reappearance of fine roots. But an alternative to this scenario exists, in the formation of new branch roots from the secondary tissues of older root axes. A branch root formed from the secondary tissues of a parental root axis may be referred to as an "adventitious" root because its origin contrasts with the (typical) formation of a branch root in the pericycle of the parental axis. This use of the term "adventitious" fits the "broad" definition of adventitious roots as given by Hayward (1938)
, by Esau (1965)
, and by Fahn (1990)
. It is not intended to exclude any other application of the term, but this report will focus on adventitious roots that originate as branches within the secondary tissues of parental root axes.
The importance of adventitious roots to an understanding of rooting "strategies" is self-evident. It is a matter of general interest to determine whether generating the population of fine roots depends on proliferation of conserved apical meristems and primary tissues, or secondary tissues, or both. It is our thesis that the occurrence of adventitious roots on roots is vastly under-reported. This situation should be corrected because adventitious roots provide a plant with the potential to harvest water and nutrients where they are locally available around roots that have entered secondary growth.
We believe that adventitious branch roots form in the secondary tissues of normal root axes in a wide variety of plants as they grow in their normal habitats. The literature emphasizes the occurrence of adventitious roots on roots during regeneration of the root system after flooding (Kozlowski, 1984
) and pruning (Wilcox, 1955
; Bogar and Smith, 1965
). However, adventitious roots occur routinely on the fleshy storage roots of Pastinaca sativa (parsnip; Warning, 1934
) and Daucus carota (carrot; Esau, 1940; Thibault, 1946
) as part of the normal pattern of branching. In Medicago sativa (alfalfa; Jones, 1943
), adventitious roots have been studied in the context of the origin and loss of roots throughout a growing season.
In the present study roots of diverse plants (Fig. 1) were examined to establish whether the origin of new roots in secondary tissues of persistent roots is of widespread occurrence under field conditions that do not include flooding. Our purpose was to establish beyond reasonable doubt that branch roots form routinely in the secondary tissues of normal parental root axes and to show how their presence can be diagnosed using straightforward anatomical interpretations. We believe that it is practical to distinguish between roots of different origins when studying patterns of rooting. Our report emphasizes general features of adventitious roots and deals with details and specific examples only as they are needed to understand the generalizations. Descriptions of the many interesting anatomical features reflecting plant diversity that have been discovered during this study must be excluded in the name of brevity.
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THEORETICAL AND PRACTICAL BASIS FOR THE ANALYSIS |
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TOPABSTRACTINTRODUCTIONTHEORETICAL AND PRACTICAL BASIS...MATERIALS AND METHODSOBSERVATIONSDISCUSSIONLITERATURE CITED |
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Anatomical features relevant to diagnosing the origins of branch roots
1. When a branch root has formed in the pericycle of a parental root the xylary tissues of the branch trace can be followed to the immediate vicinity of the primary xylem near the center of the parental axis (Esau, 1965
; Byrne, Pesacreta, and Fox, 1977
; Fahn, 1990
).
2. When a branch root persists in a woody parental axis, the vascular system of the branch is augmented by a vascular cambium that is confluent with the vascular cambium of the parental axis (Byrne, Pesacreta, and Fox, 1977
), and the layering of new growth leaves the connection of the branch system to the primary xylem of the parental axis more or less intact. The insertion of the secondary xylem of the branch axis into the secondary xylem of the parental axis is V-shaped in sectional view (Fig. 2) and extends to the region of the primary xylem of the parental axis.
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has described these features in carrot (see also Figs. 4 and 5).
4. Any connection of an augmented trace to the primary xylem of the parental axis typically remains intact and is embedded in the earliest secondary xylem in the parental axis (Fig. 6). An augmented trace will be embedded in secondary phloem of the parental axis if any appreciable part of the girth of that axis depends on radial expansion of the secondary phloem (Thibault, 1946
; see also Figs. 8 and 15).
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; see Figs. 8 and 9). Added elements of the augmented trace, like the elements of the original trace, can record the accumulation of strain.
6. If an adventitious root is served by its own unique trace, its xylary elements will connect only with secondary vascular tissues in the parental axis (Wilcox, 1955
; see Fig. 7). Diagnostically, the branch trace does not penetrate to the primary xylem of the parental axis. (For convenience we refer to traces of this kind as "peripheral traces," as in Table 1.) The probable location for the formation of adventitious root primordia in this case is in recent external derivatives of the vascular cambium of the parental axis.
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) and carrot (Thibault, 1946
) it is reported that the traces to branch roots formed in the pericycle of the parental axis persist in spite of the loss of their respective branch roots. These persistent traces each connect multiple, superficially formed adventitious roots to the vascular system in the parental axis. They are strained and repaired during secondary growth of the parental axis, as described in item 3, above (see Thibault, 1946
, for carrot). Also, as is found in any augmented trace that originally served a root that was formed in pericycle, the connection of the xylem elements of the trace to the primary xylem of the parental axis remains detectable.
To add precision to further description, an augmented trace that serves multiple adventitious roots will be referred to as a "trace complex." In addition to showing evidence of destruction and replacement of vascular elements, a trace complex branches at its peripheral end (Thibault, 1946
, and see Fig. 8) because multiple adventitious root primordia form near that end of the trace complex.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONTHEORETICAL AND PRACTICAL BASIS...MATERIALS AND METHODSOBSERVATIONSDISCUSSIONLITERATURE CITED |
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; Esau, 1940; Thibault, 1946
). Legumes were included because of the report of adventitious roots in alfalfa (Jones, 1943
). The names of plants that had adventitious roots on root axes are listed in Table 1, and those that lacked them are included as a footnote to the table. The latter plants were not tested exhaustively, and one cannot be sure that their roots do not form adventitious branches under extraordinary circumstances. The main thrust of the sampling was to find plants that gave positive results without intensive searching, consistent with the notion that the phenomenon under study was normal and frequent in occurrence.
Plants were dug in the field, from their normal environments as listed in the local flora, throughout the growing season in 2001, except for Pachycereus pringlei, which was part of the materials for another study (Niklas et al., 2002
). None of the sites experienced flooding. Tree species were restricted to saplings. Root systems were washed with water and screened with a stereomicroscope for fine roots emerging from thick root axes (likely to be in secondary growth) and for the presence of branch roots that emerged in close proximity to each other (for examples, see Figs. 10–12). The screening was intended to increase the likelihood of finding adventitious roots. Adventitious roots form in groups near the end of a trace complex. We also reasoned that when adventitious roots are served by their own unique traces they may form at positions in close proximity to older root traces. If and when the first root persists beyond the initiation of the second, and so on, branch roots should occur in pairs or groups at the surface of the parental axis. We know, of course, that the emergence of branch roots in close proximity to each other is not unique to adventitious roots. Roots of pericyclic origin can also emerge close together (see Boke, 1979
for root spurs of Opuntia; Dell, Kuo, and Thomson, 1980
, for proteoid roots of Hakea).
Materials were examined fresh and preserved in FAA (1 part formalin, 1 part glacial acetic acid, 18 parts 70% ethanol), which was replaced with 70% ethanol for storage. Our specimens were collected as short segments of parental axes with the bases of the branch roots attached. We collected from parental axes that were healthy and undamaged and that were not truncated anywhere near the sites of collection. For this survey, it was not practical to ascertain features like the total lengths of branch roots. Information of this kind may be of interest for describing heterogeneity within the population of branch roots for any species, but not for determining whether or not branch roots are of adventitious origin.
Serial hand sections were cut from fresh and preserved materials and cleared in 70% lactic acid on a warming table. This approach allowed for observations on three-dimensional features of branch traces while minimizing the task of reconstruction. Staining was not essential because the arrangements of xylem-conducting elements were readily observed in unstained materials. Also, xylem-conducting elements were emphasized in this study because xylary tissues in a branch root trace record the accumulation of strain (due to radial expansion of the parental axis) via the distention and collapse of tracheary elements and because they occur in the parental axis as permanent and relatively undisturbed additions to secondary xylem.
After initial observations, sections of particular interest were inverted for observation from the obverse side. This procedure effectively increased the number of planes of sectioning that could be photographed clearly. Photographs were made via digital capture of images from stereo- and compound microscopes, assembled as montages as necessary, and used as working documents to record and test interpretations made with the microscope.
Because the purpose here is to emphasize the formation of adventitious branch roots on parental root axes, an effort was made to confirm that branch roots were attached to an axis that had typical root structure. In favorable materials, the geometric arrangement characteristic of exarch primary xylem can be used to diagnose root axes of advanced age (Esau, 1965
; see also Fig. 13). In addition, although it is not "diagnostic" for root structure, the absence of a pith generally distinguished root from hypocotyl in our materials.
The fleshy subterranean axes of parsnip and carrot contain both root and hypocotyl (Esau, 1965
), and lateral roots are borne all along the axis. The formation of branch roots from seedling hypocotyls has been documented (von Guttenberg, 1941
; Weinhold, 1967
). Because the material was available, we note in passing that we found adventitious roots in the secondary tissues of the elongate woody hypocotyl found in our sample of Aesculus and in fleshy hypocotyls where these were available for study, but we do not report these data.
Whereas a distinction between hypocotyl and root can be drawn on anatomical grounds, and both may be regarded as anatomically different from stems, there is no a priori reason to believe that adventitious roots differ in their functions or structural potential according to the place of origin with reference to anatomical arrangements along the main axis. We note, however, that Bushamuka and Zobel (1998a
, b
) claim that the roots of soybean and corn that arise directly from hypocotyl tissues are distinctly different (functionally and developmentally) from lateral branches of roots.
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OBSERVATIONS |
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TOPABSTRACTINTRODUCTIONTHEORETICAL AND PRACTICAL BASIS...MATERIALS AND METHODSOBSERVATIONSDISCUSSIONLITERATURE CITED |
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In this study, most of the adventitious roots that were diagnosed would be classified as fine roots (0.5 mm in diameter). However, it was verified that woody roots can arise as adventitious roots. We assumed that this observation meant that adventitious branch roots attained the full range of development attained by branch roots that formed in the pericycle. However, the proportions of adventitious roots that achieve various levels of persistence as part of the root system was not assessed.
Adventitious roots revealed by insertion of root traces
Of the 22 species listed in Table 1, 18 were diagnosed as having adventitious lateral roots on the basis of the depth of insertion of branch root traces. Although sometimes tedious, the observation that some traces did not penetrate to the center of the parental root (Figs. 7 and 14) was relatively straightforward, requiring only serial transverse sections that adequately revealed the branch trace end to end.
Across a parental axis that showed multiple roots in one series of transverse sections, different traces penetrated to different layers of the secondary xylem, suggesting that successively younger adventitious roots formed in the neighborhood of the vascular cambium of the parental axis as it traveled outward. The occurrence of augmented traces was a feature of all the nonwoody axes listed in Table 1. We observed different degrees of accumulated strain in the xylary components of traces that were in close proximity to each other, further suggesting that the traces and their respective roots were of different ages. Among defunct roots, the traces of some were attached to secondary and primary xylem of the parental axis whereas others were attached only to secondary xylem. Some traces of defunct roots showed disruption of xylem conducting elements that was not compensated for by addition of new vascular elements to the trace (Fig. 15), indicating a relatively long period of elapsed time since the death of the branch root, with no stimulus for further elaboration of vascular tissues within the trace.
The image of a persistent woody adventitious root provided an especially clear case for anatomical diagnosis if the branch axis was aligned with a radius of the parental axis as seen in transverse section and appended to the woody cylinder of the parental axis by a broad base (Fig. 3). This situation contrasted with the V-shaped insertion of a persistent branch root that was formed in the pericycle of the parental axis (Fig. 2).
Woody axes also offered very complex situations. In one sample of Acer, where a single fine, nonwoody root emerged from a much larger woody axis, there were four branch traces beneath the site of root emergence rather than one, inserted within an enlarged ray. One of the four traces penetrated to the vicinity of the primary xylem in the parental axis, whereas the other three (including the trace to the current, functional branch root) connected laterally to secondary xylem at different depths within the parental axis. All four traces were only weakly augmented. This situation was consistent with the repeated emergence of ephemeral adventitious roots at or near the site of emergence of the original branch root that was formed in the pericycle of the parental axis. Similarly, Wilcox (1955)
described the laterally directed attachment of the traces of adventitious roots in roots of noble fir. Also, Wilcox (1968)
reported the juxtaposition of adventitious roots to scars formed by defunct roots on woody root axes of Pinus resinosa, and Bogar and Smith (1965)
reported that the removal of a branch lateral root at its base instigated the formation of new, adventitious roots directly above and directly below the excision scar on parental roots of Pseudotsuga menziesii.
Adventitious roots associated with trace complexes
Trace complexes were branched at their peripheral ends (Fig. 8) to form vascular strands. The traces that entered roots were formed either from the ultimate branches of a trace complex or via anastomosis among the final branches of a trace complex. Some branches of trace complexes ended blindly, assumedly because the branch roots they once served were no longer in existence.
As one would anticipate, except for branching, the anatomical features listed below for trace complexes were also found in unbranched augmented traces.
1. The xylem of many trace complexes could be followed to the primary xylem of the parental axis. Typically, an abundance of collapsed and disjointed xylem conducting elements accumulated in a trace complex (Figs. 4 and 5), so that the identification of the xylary component of the original trace was uncertain except at the connection of the trace complex to the primary xylem of the parental axis.
2. With time, vascular elements were added all along the axis of a trace complex, from its peripheral end to the secondary xylem of the parental axis. Xylary elements of the complex that matured during secondary growth of the parental axis were attached to and integrated with the secondary vascular tissues of the parental axis. Thus, the more peripheral the elements of the trace within the trace complex, the younger the layer of secondary xylem to which they were attached (Figs. 8 and 9).
3. Tangential sections of parental axes revealed that a trace complex could have features like those expected in a trace to a persistent branch root that has secondary growth, viz., radial organization, a vascular cambium, and a differentiated ray system (Figs. 16 and 17). As a series of sections was followed into the secondary xylem of the parental axis, whole sectors of xylem conducting elements left the trace complex to join with adjacent axial components of the secondary xylem of the parental axis, in a sequence of younger to older vascular elements. Finally, only a small group of collapsed elements remained to join with the axial system in the region of the protoxylem of the parental axis. Assumedly, this part of the trace complex belonged to the original branch root trace.
Combined occurrence of augmented traces and trace complexes
The root primordia we observed during this study were located either (1) adjacent to and exterior to the vascular cambium of the parental root or (2) just beneath the periderm. These occurrences confirm that (a) when an adventitious root was served by its own unique trace, its primordium was formed near the vascular cambium and that (b) formation of multiple adventitious roots at the branched ends of trace complexes was consistent only with a peripheral location for the relevant root primordia.
It appears that some species utilized both of the above locations for the formation of adventitious roots. Although we do not have quantitative data, it is evident that the proportion of traces that were trace complexes varies widely. In some cases they were not detected, but in others they dominated. In chicory, there were few trace complexes, and these entered the bases of defunct roots and bore only solitary, laterally directed adventitious root primordia. In dandelion, trace complexes were relatively more frequent than in chicory, and they served multiple root primordia. One group of five roots analyzed in alfalfa was served by three separate augmented traces and one trace complex that served the remaining two roots (Fig. 18). In domestic and wild parsnip and carrot the relative frequency of trace complexes approached 100%.
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) into recognizable bumps or ridges (Fig. 10). However, grouping of roots was nearly universal, occurring whether or not trace complexes were present (Table 1). For example, what appeared to be a single group of roots at the surface of a parental axis was sometimes served by multiple separate traces that converged toward a single locus at the surface of the secondary xylem (e.g., dandelion). Or the group was served by a combination of separate traces and one or more trace complexes inserted separately along the axis within the same ray of the secondary xylem (e.g., alfalfa, Fig. 18). Often the ray was large and situated opposite protoxylem. But we have observed adventitious root traces opposite xylem rays that were formed by conversion of axial elements of the cambium (Fig. 7), especially in older axes, and this too suggested that new root traces were sometimes formed away from the locations of preexisting root traces.
Although one might be inclined to argue that in many cases preexisting traces had influenced the location of new traces, the observations were also open to the interpretation that anatomical features of the parental axis, and possibly the locations of large rays, determined the preferential sites of adventitious root formation. Bogar and Smith (1965)
reported that rays were important in the formation of adventitious roots originating in response to root pruning. The situation depicted in Fig. 3 suggested that the ray in which the root formed need not be large because there are no large rays seen in the secondary xylem of the parental axis at the base of the adventitious root.
We concluded that the association of rays and lateral traces reflected, to a large degree, coordination during development without revealing cause and effect. For example, large rays were sometimes formed in coordination with the formation of roots in the pericycle, but the persistence of a ray in the secondary vascular tissue of a parental axis might be influenced by the persistence of the resident branch trace or traces within the ray. Likewise, the formation of multiple roots in the same ray may have reflected the localization of some endogenous or external factor that affects the process.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONTHEORETICAL AND PRACTICAL BASIS...MATERIALS AND METHODSOBSERVATIONSDISCUSSIONLITERATURE CITED |
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; Esau, 1940; Jones, 1943
; Thibault, 1946
; Wilcox, 1955
, 1968
; Bogar and Smith, 1965
; Kozlowski, 1984
) offers sufficient grounds to investigate whether or not the phenomenon is widespread under conditions that do not involve flooding or artificial root pruning. The current report is based upon a preliminary survey to address this issue. Figure 19 summarizes the observations reported in this study from a developmental point of view. Trace complexes are augmented traces that support the formation of new, adventitious roots at their peripheral ends. Many trace complexes develop from traces that served branch roots that formed in the pericycle and later became defunct (Fig. 19, A2). It is quite likely that augmentation of a trace begins before the original branch root is lost. If a trace serves a persistent root, of course the trace becomes augmented (Fig. 19, B3). In a nonwoody axis, the persistent trace of such a root may eventually be converted to a trace complex, possibly when the original branch root becomes defunct (Fig. 19, B6 connects to A). A trace complex (Fig. 19, A5) is formed when multiple adventitious roots occur at the end of an augmented trace. Trace complexes may produce additional adventitious roots (Fig. 19, C9), repeatedly. Meanwhile, the parental axis can add adventitious roots more or less continuously by utilizing the external derivatives of the vascular cambium to form root primordia (Fig. 19, C8), whether or not trace complexes are formed, and whether or not the axes are nonwoody or woody. Traces to adventitious roots can be excised or persist, become augmented when they are persistent, and can be converted to trace complexes.
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). With respect to this mode of adventitious root formation, there is a direct parallel between the capabilities of woody axes and nonwoody axes (Fig. 19, C8). However, the formation of adventitious roots near the surface of the parental axis, in nonwoody and semi-woody axes (Fig. 19, C9), provides an alternative to the more generalized location for adventitious root formation near the vascular cambium. This location complies with the generalization that adventitious roots form where they are close to both xylem and phloem (Esau, 1965
) because a trace complex is well supplied by both vascular tissues. Trace complexes are developed maximally in nonwoody axes when extensive expansion throughout the parental axis is accompanied by a probably slow rate of sloughing of tissues at the surface (e.g., parsnip, Fig. 8). This situation creates a radially directed displacement of branch roots at the surface of the parental axis, which probably results in a buckling and collapse of attached roots when the mechanical resistance of the surrounding soil confines movement of a branch root to its base. One can suggest, therefore, that the well-developed capability of roots like parsnip and carrot to form adventitious roots is an adaptive response to their expansion as fleshy storage organs.
In woody axes, the augmentation of a branch trace is accomplished by a vascular cambium that is integrated with the axial vascular cambium of the parental axis, so that the "trace" (insertion of branch axis) does not appear to be embedded in secondary phloem and other peripheral tissues. The semi-woody axes investigated have hard, woody cores of secondary xylem that are covered by broad, complex layers of mostly parenchymatous tissues. For example, in the columnar cactus we investigated, persistent lateral roots have a woody core and a wide parenchymatous peripheral layer consisting of secondary phloem, secondary cortex, and periderm (Niklas et al., 2002
). Although trace complexes were not found in every nonwoody and semi-woody axis examined, none were found in fully woody axes.
Thus, trace complexes appear to be associated with broad parenchymatous layers of secondary tissues in the parental axis. Although the present study produced no evidence for typical trace complexes in fully woody species, it is clear that adventitious roots can emerge repeatedly from a small area on the surface of a woody parental axis. At these loci, branch traces that served now-defunct and probably ephemeral roots are crowded together in a single enlarged ray, as appendages of the woody cylinder of the parental axis, which they penetrate to varying depths.
The roles of adventitious roots on roots
The formation of adventitious roots in stems (shoots) is taken for granted as part of the normal growth patterns of intact plants in the grasses and many other species (Barlow, 1986
, 1994
). The present observations show that the formation of adventitious roots in the secondary tissues of roots (and hypocotyls) is also part of the normal and usual rooting patterns in dicotyledonous plants. The present sample includes herbaceous and woody species, enlarged storage roots, fibrous root systems, and roots with anomalous secondary growth (Chenopodium alba, Phytolacca americana). Included are 12 families in nine orders of dicotyledonous plants.
The widespread ability of roots (and hypocotyls) to form branch roots in secondary tissues can be viewed as one manifestation of the innate capacity for reiterative regeneration in plant tissues. The available literature emphasizes the formation of adventitious roots on root axes as a response to flooding and pruning (Wilcox, 1955
; Bogar and Smith, 1965
; Kozlowski, 1984
). The common feature in these reports appears to be substantial loss of the preexisting root system. Jackson and Drew (1984)
and Reid and Bradford (1984)
suggest that regeneration of the root system after flooding is prompted by altered hormonal status in the remaining parts of the root system. This assertion is supported by the large base of research demonstrating hormonal (especially ethylene and auxin) control of adventitious root initiation (see Jackson, 1986
; Haissig, Davis, and Riemenschneider, 1992
, and references therein; Blakesley, 1994
), including the findings of specific auxin-induced gene activity and protein synthesis during rooting (Oliver, Mukherjee, and Reid, 1994
; Chen et al., 1996
; Hutchison et al., 1999
; Li and Leung, 2001
). There has been no physiological research on the adventitious roots reported here, leaving open the question of endogenous control of their initiation. Moreover, adventitious rooting should be viewed as a process involving multiple phases (Kevers et al., 1997
; De Klerk, Van der Krieken, and De Jong, 1999
). We note, therefore, that the overwhelming majority of the information on adventitious rooting has been obtained from shoots, and the control mechanisms that regulate adventitious rooting on roots and hypocotyls may differ from those that regulate adventitious rooting on shoots.
Essentially all the adventitious roots we identified would be classified as fine or very fine, and this outcome may be influenced by the screening procedure. However, it was also observed that adventitious roots can become persistent and woody (e.g., Fig. 3). At this point in our investigation one can speculate that adventitious roots formed on parental roots explore the full range of capabilities in root growth, but it may turn out that adventitious roots play an important role in a particular part of rooting, such as the replacement and amplification of the population of fine roots in the soil.
However, the literature on turnover of fine roots in the soil does not address the issue of adventitious roots. For example, although Pritchard and Rogers (2000)
emphasize the importance of lateral branching in the dynamics of root turnover they discuss branching only in terms of the formation of branch roots in the pericycle of the parental root axis. For purposes of discussion, both the lateral branches formed in the pericycle and those formed in secondary tissues (adventitious roots) must be considered together when discussing the available data.
Ecological studies on the turnover of fine roots in the soil indicate that in general various environmental factors affect the processes that are involved. Temperature, availability of water and nutrients, salt stress, grazing stress, and carbon dioxide concentration are said to have effects on root turnover (Snapp and Shennan, 1992
; Smucker, 1993
; Fahey and Hughes, 1994
; Dawson, Grayston, and Paterson, 2000
; Eissenstat, Wells, and Yanai, 2000
; Gill and Jackson, 2000
; Norby and Jackson, 2000
; Pritchard and Rogers, 2000
).
For example, when plants are rewatered after a period of drought, they respond, sometimes extremely rapidly, with the formation of new roots (Kausch, 1965
; Nobel and Sanderson, 1984
; Lauenroth et al., 1987
; Nobel, 1988
, 1994
; Franco and Nobel, 1990
). Pritchard and Rogers (2000)
and Smucker (1993)
state that proliferation of lateral branches occurs during the dry-down of wet soils, with maximum response in pockets of retained moisture. It appears from the data of Huck, Hoogenboom, and Peterson (1987)
on soybean that a stable population of roots occurs when the initiation of new roots is balanced by an equivalent rate of root death and that rates of formation of new roots and root death may rise and fall together.
While we remain cognizant that species differ in many ways, it is useful to consider here Kramer's (1983)
finding that persistent roots of trees, well into secondary growth, may at times account for almost all of the root system and that they are capable of effective water uptake that offsets transpirational losses. One can visualize that as draw-down of soil moisture occurs around these roots their direct access to water is constrained, but the opportunistic retrieval of water continues as adventitious branch roots proliferate into pockets of soil that still contain abundant moisture.
The ability of adventitious roots to emerge repeatedly from the same area of the surface of a parental root creates a scenario where adventitious roots can enter and re-enter the same volume of soil. As the roots die off, they contribute to soil carbon and influence the microflora around the persistent roots, possibly in favor of nutrient recycling to the advantage of the plant. And all these events may themselves occur in cycles.
Cellular mechanisms underlie the branching of roots (Pritchard and Rogers, 2000
) in that cell division and cell enlargement at potentially meristematic regions of the parental root must respond to environmental triggers to form lateral root primordia. Clearly the factors that affect root turnover affect these cellular processes, putatively via hormonal regulation. We suggest that the formation of adventitious branch roots reflects the responses of potentially meristematic tissues (recent cambial derivatives and potentially meristematic cells at the peripheral ends of trace complexes) to endogenous and environmental triggers that are applied to roots in secondary growth, i.e., beyond the time in the life of a parental root when a pericycle is available to make the appropriate responses. Thus, adventitious roots should be expected to facilitate the opportunistic responses of persistent roots in circumstances that signal the availability of resources but require "outreach" from the existing root system for maximal utilization. Further research is needed to demonstrate that the adventitious roots we have described above account (at least in part) for the fine roots observed by others in the study of root turnover (Huck, Hoogenboom, and Peterson, 1987
; Snapp and Shennan, 1992
; Smucker, 1993
; Fahey and Hughes, 1994
; Dawson, Grayston, and Paterson, 2000
; Eissenstat, Wells, and Yanai, 2000
; Gill and Jackson, 2000
; Norby and Jackson, 2000
; Pritchard and Rogers, 2000
).
Concluding remarks
Our study suggests that regeneration or extension of root mass via adventitious roots is a frequent occurrence that does not require cataclysmic changes in the environment, nor the loss of extensive root mass. It is clear that local variations in soil environment result in local variations in rooting (Drew, 1975
; Reynolds, 1975
; Fahey and Hughes, 1994
). But the circumstances that provoke (or allow) the formation of adventitious roots on parental root axes must be widespread in the soil environment. Adventitious roots occur on healthy parental root axes, and they are not restricted to large root axes, nor to particular parts of the root system. In some cases (e.g., parsnip) the need for adventitious roots appears to be generated by the expansion of the parental axis as a storage organ, which crushes the bases of early formed roots. But the formation of adventitious roots also occurs in slender parental root axes, whether or not the latter can be expected to persist as part of the root system (see also Jones, 1943
).
The importance of the fact that roots routinely form adventitious branches lies in its putatively adaptive features. First, renewal and amplification of the population of fine roots in the soil can occur by this mechanism, as well as by the proliferation of meristems in primary tissues. Thus, the phenomenon is part of the cycle of formation and turnover in belowground biomass. Second, the phenomenon provides an ideal situation for the formation of "opportunistic" roots that take advantage of water and nutrients in parts of the soil that are not populated with the root apical meristems of primary root tissues. Third, because an adventitious root can be persistent, the formation of adventitious roots gives a plant the capability to restructure its root system, redirecting primary growth by supplying new meristems in locations where there are no preexisting root tips.
Tedious, fastidious studies are required to establish the actual role of adventitious roots in the life history of any particular organism. One study that attempts the task involves alfalfa (Jones, 1943
), but the factors controlling regrowth of the root system from adventitious roots could not be determined, and anatomical details are lacking in that study. However, it is clear from the results with alfalfa that formulating the scenario of how adventitious roots are utilized is neither simple nor intuitive.
In closing we emphasize that we do not claim that the present study has demonstrated the actual roles of root formation in the secondary tissues of roots in the rooting strategies of the plants that were investigated. However, we have established that the occurrence of adventitious roots in root systems is widespread under field conditions. Given this outcome, it follows that topics like root turnover in the soil remain incompletely described until the sources of new roots in the population of fine roots are characterized better.
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4 Author for reprint requests (djp4{at}cornell.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONTHEORETICAL AND PRACTICAL BASIS...MATERIALS AND METHODSOBSERVATIONSDISCUSSIONLITERATURE CITED |
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