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Anatomy and Morphology |
2Department of Plant Biology, Cornell University, Ithaca, New York 14853 USA; 3Department of Horticulture, Cornell University, Ithaca, New York 14853 USA
Received for publication August 6, 2004. Accepted for publication February 9, 2005.
ABSTRACT
Based on positive results for 11 of 17 species included in an anatomical survey of tree roots, we concluded that the origin of adventitious branch roots (ABR) on established, undisturbed woody parental root axes is a widespread occurrence. ABR were morphologically indistinguishable from branch roots formed in primary tissues of a parental axis, and they occurred without increase in branch root density. We concluded that ABR are an unrecognized component of undamaged root systems. Using continuous serial sectioning to perform a census of branch roots within parental root axes, we obtained definitive evidence that ABR participate in root turnover. Comparisons of older and younger axes, and the chronology of root formation in older axes fulfilled the expectation that with greater age of parental axis, ABR become increasingly predominant among intact branch roots. We confirmed this trend for one of the species scoring negative in the survey, which means that our survey results were probably influenced by age variation. Thus, any of the six negative results obtained in the survey may have been dependent on the young age and slenderness of the axes that were available for examination in those six species.
Key Words: adventitious roots • branching • determinate roots • ephemeral roots • root turnover • roots
The formation of adventitious roots on stems and hypocotyls has been studied from the phenomenological level to the mechanistic level for a variety of plants (e.g., Barlow, 1986
, 1994
; Haissig et al., 1992
; Blakesley, 1994
; Oliver et al., 1994
; Chen et al., 1996
; Kevers et al., 1997
; De Klerk et al., 1999
; Hutchison et al., 1999
; Li and Leung, 2001
; Casson and Lindsey, 2003
; Konishi and Sugiyama, 2003
; McDonald and Wynn, 2003
; Busov et al., 2004
; Molassiotis et al., 2004
). By comparison, the formation of adventitious branch roots (i.e., branches formed on parental root axes that are in secondary growth; herein abbreviated singly or in plural as ABR) has received much less attention (Paolillo and Zobel, 2002
). The literature on this topic is mainly concerned with the formation of ABR in response to loss of substantial portions of the root system due to mechanical injury (Wilcox, 1955
; Bogar and Smith, 1965
), or flooding (Koslowski, 1984
), and more rarely with seasonal study of root turnover (Jones, 1943
) and the structure of aging root systems (Puhe, 2003
). However, Paolillo and Zobel (2002)
reported that the formation of ABR is a common occurrence for intact, unflooded, field-grown dicotyledonous plants. ABR form either from specialized meristematic tissues at the periphery of the parental axis (Warning, 1934
; Esau, 1940
; Thibault, 1946
), or from derivatives of the vascular cambium of the parental axis (Wilcox, 1955
; Esau, 1965
), or both on the same parental axis (Paolillo and Zobel, 2002
).
If the formation of ABR is widespread, it stands to reason that ABR play a significant role in plant growth. Paolillo and Zobel (2002)
theorized that ABR contribute to the population of fine roots that are gained and lost during root turnover in the soil (Reynolds, 1975
; Fahey and Hughes, 1994
; Baker et al., 2001
). They also reported that some ABR show enduring growth. Thus ABR are capable of the full range of development expressed by branch roots formed in primary tissues (herein referred to as primary branch roots, and abbreviated singly or in plural as PBR).
The sample of species examined by Paolillo and Zobel (2002)
included only a few tree species, represented by seedlings. In the present study we extend the sample of woody species to a survey of fully grown trees, in an effort to establish that the occurrence of ABR is part of normal rooting without massive injury in a variety of tree species and to make more tenable the concept that ABR are significant in forest ecosystems. Toward the goal of establishing the participation of ABR in root turnover, we introduce the concept of a branch root census, whereby the history of root formation in an established woody parental root axis is reconstructed from continuous serial transverse sections, and we apply that concept to three species. We also discuss some practical problems encountered in making definitive diagnoses of branch root origins, and we comment on the prospects for more intensive studies of ABR in natural populations.
MATERIALS AND METHODS
The survey of species (Table 1) is based on collections of 16 species from the Underwire Arboretum (UA) of the City of Ithaca Department of Public Works, plus a collection of Thuja occidentalis L. from a residential lot in the city of Ithaca, all in July of 2002. At the UA, roots were uncovered using compressed air and a device known as an Air Knife (Easy Use Air Tools, Inc., Allison, PA). All other roots were exposed with a shovel. Second collections of Carpinus caroliniana Walt., Fraxinus americana L., and Thuja occidentalis were made on the Cornell campus in May of 2004 for selective amplification of the survey data. Survey data were gathered on two or more axes, and/or segments greater than 10 cm apart on the same axis. The axes were fixed in FAA (1 part formalin, 1 part glacial acetic acid, 18 parts 70% ethanol), and stored in 70% ethanol for further handling.
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Serial sections transverse to the parental axis were used in the diagnosis, and each trace that was diagnosed was followed for its full extent within the parental axis. For some roots, satisfactory results could be obtained with hand sections. For others, we cut sections at 40 or 80 µm, using unembedded axes and a sliding microtome. Serial sectioning proved essential because anatomical nuances in some species made the diagnosis of PBR and ABR dependent on reconstructions. In these species, no individual section demonstrated or even clearly indicated that a root was adventitious. In the simplest case, branch connections were straight but consistently oblique to the axis of the parental root, so that the full extent of a trace could not be appreciated from a single section. In other species, asymmetry and curvature of the branch root connections and clustering of branch roots complicated the reconstruction.
Locations for sectioning during the survey were guided by the presence of branch roots or their stubs at the surface of the parental root axis. In most instances, branch roots were diagnosed in sequence along their parental axes. Further sampling of the 2002 collection of Thuja occidentalis and sampling of all three species in the 2004 collections was refined to provide a census of branch roots by continuous serial sectioning for the entire lengths of the axes that were examined. In this way, excised roots were detected, and a characterization by year of origin of all branching for the axis segment could be developed.
Aqueous toluidine blue (0.05%) was used for rapid staining of the sections, as needed. Selected sections that were to be archived were dehydrated in ethanol, cleared in xylene, and mounted in synthetic resin. Photographs were made via videocapture, under the control of a microcomputer. Printouts of the electronic files were used as records and to allow reconstructions of root attachments when these were needed.
The diagnoses performed for this report determine the points of origin of branch roots within parental root axes. PBR have connections with the primary xylem of the parental axis, whereas ABR lack any such connection (Paolillo and Zobel, 2002
; Figs. 1–3). The latter circumstance indicates that ABR were initiated within the secondary body of the parental root axis, assumedly from cambial derivatives. Therefore, they are adventitious via their origin, by definition (Hayward, 1938
; Esau, 1965
; Fahn, 1990
).
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Our observations focused on diagnosing the points of origin of branch roots formed within established woody parental root axes (Figs. 1–6). Most of the laterals examined were 
1 mm in diameter, but larger, woody branches were a small minority of the observed cases. The degree of development of laterals was variable, and diameter, degree of woodiness, and degree of branching of the laterals were not dependent on whether the laterals were ABR or PBR.
Survey of 17 species
Table 1 lists the results of our survey of species, given in order of increasing frequency of ABR and shows the number of cycles of growth of secondary xylem in the axes that were examined. The range in age of samples for species with no ABR overlapped the range in ages of samples from species that scored positive for ABR.
Six species in Table 1 had no ABR in the survey, whereas 11 of the 17 species evaluated scored positive for this feature. Among the species with ABR, the frequency varied from very low to ca. two-thirds of the branch roots that were diagnosed (Table 1).
Census of branch roots on established root axes
Given the results of the survey, three species were chosen for a census revealing all the branch roots within the observed axes (Table 2).
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Our results fulfilled the expectation that ABR should increase in frequency with the passage of time. For Thuja occidentalis, ABR were absent from the first year of secondary growth in the census from the 2002 collection, and from the first 2 to 3 years of secondary growth in the 2004 collection (Table 2, last column). The 2004 data are divided in Table 2 to show the difference between older and younger axes with respect to frequency of ABR. The fact that ABR replaced dead PBR with the passage of time is reflected in the increase in percentage of ABR among intact roots as compared to that among all roots, the more so with older axes (Table 2, columns 5, 7). However, ABR were also subject to mortality (e.g., see Fig. 7), and like PBR, ABR varied in their rates of thickening, some increasing in diameter rapidly to become part of the established woody root system.
2. Fraxinus americana was chosen for a branch root census because this species scored the highest for ABR in the survey. We examined a younger and an older axis from the 2004 collection. The pattern of differences resembles that found for Thuja occidentalis. The younger axis had no ABR, but the older axis had 47% of all branch roots as ABR (again, a lower figure than in the survey) and 100% of the intact branch roots as ABR.
3. Carpinus caroliniana was chosen for a census because this species scored negative in the survey for ABR, using roots that were relatively slender compared to our 2004 collection. This species was of further interest because it is difficult to establish after transplanting. In the older axis, among all branch roots, 27% were ABR. Among intact branch roots, 56% were ABR, and all of these were formed in the third year or later in the life of the axis (Table 2, last column). Had this axis been the basis for the survey data, Carpinus caroliniana would have scored among the top three species for frequency of ABR. In the younger parental root axis, only one branch root, formed in the third year of growth of the parental root axis, was adventitious, for a score of 4% of all branch roots in the axis and 6% of intact branch roots.
Ease of diagnoses, features of adventitious rooting
In general, diagnoses of both ABR and PBR were definitive and straightforward. In species with the simplest geometry for branching, individual transverse sections were convincing indicators of the presence of ABR and PBR (Figs. 1–6). In all cases, serial sections were used to confirm that the full extent of the branch axis had been observed. But among these species, very rarely would one have been wrong to assume that solitary images like those in Figs. 1 and 3–6 indicate the presence of ABR.
ABR were inserted at the beginning or within a growth cycle, and consistently on the same radii as pre-existing rays, particularly those rays opposite protoxylem poles (Figs. 1, 3– 6). Typically, these were the broadest rays in a transverse section, so that the rays extending to the innermost portions of ABR connections were sometimes of extraordinary breadth compared to other rays in the same section (Fig. 6). But the attachment of the branch xylary system to the secondary xylem of the parental root was always significantly wider than the ray contacted at the point of origin of the branch root (Figs. 1, 3–6).
It was not possible to predict from external morphology which of the lateral roots encountered on a parental axes were ABR and which were PBR. However, in Acer negundo L. and Acer platanoides L. many of the branch roots were found in groupings of two or three roots in a cluster on the parental axis. All of the ABR diagnosed in these two species were within such clusters, but each cluster contained branch roots originating in primary tissues, and in some clusters ABR were absent. Also, the relative diameters of the roots found in clusters were not reliable predictors of which roots were ABR, i.e., contrary to expectations based on the greater age of PBR as compared to ABR, the thickest root in a cluster was sometimes one of the ABR.
Problematical diagnoses of ABR and PBR
In some species, identification of PBR and ABR was more difficult because the vascular connections to solitary PBR were curved and strongly asymmetric (Figs. 8, 9), or roots were closely clustered. In Acer platanoides, the geometry was further complicated because root clusters were found within depressions in the surface of the parental axis. These situations were resolved by reconstructions from serial sections.
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But careful study showed that the traces were repaired directly after they were broken, by newly differentiated connections to the secondary xylem of the parental axis. The new xylem connections did not involve the core of the branch root axis. Also, the complementary portion of a broken stump could be demonstrated within the base of a branch root in most cases (Fig. 12). And as one would expect, stretched xylem elements with extensible wall patterns were detected in regions of accumulated strain (deformation). We concluded that in our materials of Cercis canadensis, the PBR were conserved and their traces were broken and repaired annually, at least within the age of our samples. The pattern of tissue destruction and repair found in Cercis canadensis resembled that reported for fleshy roots (Paolillo and Zobel, 2002
) in which the traces span regions of more broadly distributed growth. Although it is not a feature typical of woody branch roots, we found it also in a simpler form in the older root of our 2004 collection of Carpinus caroliniana.
DISCUSSION
Production of ABR as a normal component of root turnover
The usual focus in scientific studies of adventitious rooting is on the aerial parts of plants. But root axes also generate branch roots from tissues other than pericycle, either from specialized loci at the periphery of the axis, or from derivatives of the vascular cambium, or both (Paolillo and Zobel, 2002
). The literature on ABR focuses largely on the response to situations that result in loss of portions of the established root system, such as pruning (Wilcox, 1955
; Bogar and Smith, 1965
), flooding (Koslowski, 1984
), or death and decay (Jones, 1943
; Puhe, 2003
). All the parental root axes used in this study were formed years after their respective trees were transplanted and reestablished, with no expectation of trauma in the root system other than would occur in any natural environment. The root system was intact where sampled, and there were no signs of injury in the roots that were scored. In the absence of contrary evidence, we believe we are dealing with normal growth patterns of healthy root systems, not with the patterns of adventitious root formation that are obtained with large trauma and surgical manipulation. Of course, we cannot eliminate the possibility that decline of the root system at a remote location had some effect on ABR formation in the roots that were examined. But Watson and Himelick (1997
; p. 143 and their fig. 8–6) report that ABR do not form far from the site of root loss, i.e., ABR are encouraged by decapitation only near the most distal portion of the root that remains (see also Wilcox, 1955
). Any such hypothetical location of ABR formation in response to injury would be far removed from our collections.
There is evidence that ABR form routinely on intact root axes of a wide variety of dicotyledonous plants (Paolillo and Zobel, 2002
). The data of Tables 1 and 2 support the conclusion that adventitious branch roots are of frequent occurrence among undisturbed roots of tree species. Given the results with Carpinus caroliniana (cf. Table 1 vs. Table 2), any and all of the negative results in the survey may be related to the age and girth of the specimens that were examined.
In forest ecosystems, slender, determinate roots die off and are replaced on a routine basis in a process described as root turnover (Reynolds, 1975
; Fahey and Hughes, 1994
; Baker et al., 2001
). We propose that the ABR we have described in this study form and die as part of the normal turnover of root mass. Our census of ABR and PBR in parental root axes (Table 2; Fig. 7) offers direct evidence for this conclusion. One surmises from our results that early in secondary growth of the parental axes, PBR would account for all of the branching on an axis segment. With the passage of time, PBR are subject to mortality, ABR are added, and eventually ABR predominate among the branch roots found intact on an established axis segment. ABR are also subject to mortality, and, within the limits of our sample, branch root density typically declines with aging.
It is possible that the loss of PBR is the only loss of root mass associated with the routine formation of ABR in healthy, vigorous root systems of woody species. In some species, mechanisms like the repair of broken traces (possibly a feature associated with rapid expansion during early season growth in ring porous species) may help delay the eventual dependence on ABR by sustaining the population of PBR. But as PBR yield to destruction, ABR can be expected to take their place and assume their functions. The process continues in later years (as at 14 years old in the older axis of Thuja occidentalis; Table 2), but we have not attempted to establish the maximum age at which a root axis can form ABR. In principle, however, age should not limit the process because the source of new ABR lies in the derivatives of the vascular cambium, centered on, or within, derivatives of the ray initials.
Once ABR have formed in woody species, their place or role in the root system seems to be indistinguishable from that of PBR, ranging from ephemeral to part of the established root system. Thus, the root mass contributed by ABR is probably proportional to their frequency of occurrence. However, the particular "destiny" of any individual branch root may be determined during its formation, the diameter of a branch root being correlated with the subsequent growth of the root (Cahn et al., 1989
; Pagès, 1995
; Thaler and Pagès, 1996
; Bidel et al., 1999
). ABR that thicken rapidly to become part of the established root system probably grow from larger than average root primordia. In contrast, PBR and ABR that remained slender had compact insertions that failed to broaden appreciably over their extents through multiple growth layers of secondary xylem in the parental root axes (Fig. 1, within brackets). These slender roots are probably determinate in their growth and destined for eventual destruction. But the persistence of slender branch roots for multiple years in tree species seems to present a marked contrast to the putatively rapid turnover of fine roots in herbaceous species, discussed by Zobel (2002)
.
However, the relatively enduring nature of slender branch roots on the axes we investigated does not preclude more rapid turnover elsewhere in the root systems of the same plants. Puhe (2003)
reported both the occurrence of persistent fine roots and rapid turnover of fine roots in Picea abies. But he also discounted the importance of ABR in undamaged root systems of that species. We contend that this view is unsustainable without the support of anatomical analyses. In our experience, ABR can replace PBR without effect on overall morphology and without increasing branch root density. Furthermore, ABR were detected on seedlings of tree species that were undisturbed before collection, in our earlier study (Paolillo and Zobel, 2002
).
The factors controlling ABR formation are unknown
To date, nothing is known about the genetic and physiological factors controlling ABR formation on undisturbed root systems. Paolillo and Zobel (2002)
assumed that the formation of ABR is responsive to the same factors that control the formation of branch roots in general, via cellular mechanisms (Pritchard and Rogers, 2000
). Many factors affect root turnover in the soil (Snapp and Shennan, 1992
; Smucker, 1993
; Fahey and Hughes, 1994
; Dawson et al., 2000
; Eisenstat et al., 2000
; Gill and Jackson, 2000
; Norby and Jackson, 2000
; Pritchard and Rogers, 2000
; Lloret and Casero, 2002
). We assume that the propensity to form ABR may vary among species, among individuals of the same species due to intrinsic and extrinsic factors, and within an individual plant as a function of local root environment, the place or function of the parental root axis within the root system, and the vigor of the axis with respect to increase in diameter and length.
Concluding remarks
The lack of morphological features that distinguish ABR from PBR necessitates the use of anatomical analyses in any in-depth study of the role of ABR in the turnover of roots on established root axes. Accurate determinations of the points of origin of ABR require the use of a compound microscope and serial sections, imposing an additional burden of effort on functional and ecological studies. Therefore, one should screen for anatomical simplicity and a high proportion of ABR when choosing species for further study.
We note that in contrast with the other species we sampled, Carpinus caroliniana is difficult to establish after transplanting. We do not regard the delay in forming ABR to the third year or longer as a contributing factor in this difficulty. Species in the survey that are easily transplanted were equally slow to manifest their capability for forming ABR in our study. A context different from the present is required to assess the role of ABR during the reestablishment of transplanted individuals. Our data concern only the replacement of PBR with ABR on undisturbed, established root axes, i.e., they are relevant to understanding root turnover. They do not bear upon the question of what happens immediately after transplanting or some other intense trauma involving the curtailment of the root system.
Although Shoemake et al. (2004)
found no relationship between adventitious rooting of stem cuttings and success of transplants in sycamore, it should be remembered that according to Koslowski and Pallardy (2002)
, regeneration of root systems via ABR is an important adaptive feature contributing to flood tolerance in tree species. Furthermore, Puhe (2003)
emphasizes the role of ABR in offsetting the early stages of decline in root systems of Picea abies.
FOOTNOTES
1 The authors thank the College of Agriculture and Life Sciences for financial support. 
4 Author for reprint requests (e-mail: djp4{at}cornell.edu
)
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