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Development and Morphogenesis |
2Centro de Investigaciones Biológicas del Noroeste, La Paz, Baja California Sur, 23000, Apdo. Postal 128, México; 3Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apdo. Postal 510-3, Cuernavaca 62250, Morelos, México
Received for publication July 5, 2002. Accepted for publication January 10, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: adaptation • Cactaceae • determinate root growth • lateral roots • meristem • Pachycereus pringlei • Sonoran Desert
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, b
). This type of growth is the result of the realization of a developmental program in which the root apical meristem is exhausted soon after germination, having undergone only 2–5 cell division cycles (in Stenocereus gummosus and Ferocactus peninsulae). In a desert environment, this type of growth is beneficial for a plant because termination of primary root growth induces development of the lateral roots and facilitates seedling establishment (Dubrovsky, 1997a
, b
). How this developmental program is maintained is still unknown. This problem is directly related to the understanding of the mechanism of meristem maintenance, and thus plants with determinate root growth could be a useful model system for understanding this process. Environmental factors significantly affect root development. Generally, water stress causes inhibition of root growth; however, moderate water deficit can stimulate net root growth (Sharp and Davies, 1979
; Jupp and Newman, 1987
; Nguyen and Lamant, 1989
; Creelman et al., 1990
; Triboulot, Pritchard, and Tomos, 1995
; Reid and Renquist, 1997
; Van der Weele et al., 2000
). We are interested in the analysis of the effects of moderate and severe water deficits on species with determinate root growth. In the work reported here we determined how water deficit affects the determinate developmental program and verified whether the determinate growth pattern can be reverted to an indeterminate growth pattern.
The species of Cactaceae in which determinate growth of the primary root was first analyzed (S. gummosus, S. thurberi, F. peninsulae) are characterized by a very short primary root growth period not exceeding 48 h (Dubrovsky 1997a
, b
). In the Sonoran Desert, these species belong to the clustering-stem-succulent (Stenocereus) life form and to monopodial-stem-succulent (Ferocactus) life forms (Crosswhite and Crosswhite, 1984
). Arborescent Cactaceae may have a different root growth pattern. We previously analyzed the cell cycle duration in the root apical meristem of a Sonoran Desert arborescent species, Pachycereus pringlei, and found that over a 7-d period the primary root continued growth and thus considered that this species has indeterminate root growth (Dubrovsky et al., 1998a
), although analysis of overall growth behavior has not been done. In the work reported here, we have analyzed primary root growth in P. pringlei and have found that it is characterized by determinate growth, but with a longer duration of growth compared to other studied species. Because of a longer growth period, this species is a more convenient object for the studies of the effect of water deficit on determinate root growth. For this analysis we adopted a polyethylene glycol (molecular weight 8000) diffusion method developed by Van der Weele et al. (2000)
that permits creating media with low water potential without affecting root growth directly.
Water deficit can stimulate lateral root initiation in some species. In F. acanthodes, during drying, the total number of lateral root primordia increased 2.9 times compared to wet conditions (North et al., 1993
). A similar increase in the number of primordia was observed under conditions of rapid and of gradual drying in Opuntia ficus-indica (Dubrovsky et al., 1998b
). Stimulation of lateral root primordium initiation by soil drying was observed in the epiphytes Epiphyllum phyllanthus and Rhipsalis baccifera (North and Nobel, 1994
). In non-succulent plants a similar tendency was found in Lolium perenne (Jupp and Newman, 1987
). Lateral root production was increased at soil matric potentials as low as –6 to –8 MPa and in other species at less severe water stress (Jupp and Newman, 1987
; Eshel, 1992
). Meristem exhaustion in roots of some Cactaceae with a determinate growth pattern was shown to be related to lateral root initiation under well-watered growth condition (Dubrovsky 1997a
, b
). Lateral root formation in P. pringlei has not been studied and here we also address this question and analyze the possible ecological significance of lateral roots in early root system development.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) and placed in 15-cm petri dishes on the agar-solidified (0.8% or 1.2%) medium composed of one-fifth strength of Hoagland's mineral solution (Hoagland and Arnon, 1938
) with or without 2% sucrose. Seeds were germinated in temperature-controlled chambers (29° ± 1°C) and grown at 12-h photoperiod and 38 or 240 µmol · m–2 · s–1. When testae were broken, seedlings were transplanted to petri dishes with growth media and dishes were maintained in a vertical position. Markings were made on the back of the petri dishes with a fine-point permanent ink pen at the position of the root tip and growth increments were measured with a ruler every 24 h until the end of the experiment.
Water deficit treatment
Water potential was lowered in the medium with polyethylene glycol (PEG) (molecular weight 8000; Polioles, Guadalajara, Mexico) using the method described by Van der Weele et al. (2000)
. Briefly, various amounts of PEG were diluted in 20 mL of the liquid growth medium. These solutions were poured on top of an equal volume of agar growth medium and left for 24 h to let the PEG diffuse into the medium. During diffusion, plates were exposed continuously to UV light for sterilization since PEG is altered by autoclaving, and this can result in a decrease in water potential of up to 20% (Van der Weele et al., 2000
). Water potential of the agar medium was measured at the end of the experiment with a HR-33T Dewpoint Microvoltmeter (Wescor, Logan, Utah, USA) using the dewpoint mode of measurement, and the data are reported as the mean of the measured potentials (Van der Weele et al., 2000
).
Root zones, cell length and cell flux measurements, and lateral root formation
In previous work it was shown that, in roots with determinate growth, the position of the most distal root hair indicates the proximal border of the growing part of the root (Dubrovsky, 1997b
). In the current work, the distance from the root tip to the first root hairs was measured on images of roots inside the petri dishes taken with a digital camera (DC 100; Leica Microsystems, Heerbrugg, Switzerland) attached to a compound microscope (Olympus BX51; Olympus America, New York, New York, USA) and a PC. To maintain the vertical position of roots in petri dishes during image acquisition a special support for horizontal positioning of the microscope was used. The images were taken at 4x magnification and analyzed with Leica IM 1000 image analysis software (Leica Microsystems).
Permanent whole-mount preparations of roots were used for determination of the length of the root apical meristem, the number of epidermal cells in the meristem, the length of fully elongated cells, and the number of lateral-root primordia and lateral roots. Roots were fixed in a solution of 7% formaldehyde and 30% ethanol for 48 h and then stored in 70% ethanol. Roots that had been stored in ethanol were hydrolyzed in 5 mol/L HCl at room temperature for 30 min and then subjected to Feulgen staining (De Tomasi, 1936
). Roots were then dehydrated in a series of ethyl alcohol-xylene solutions and whole roots were mounted in Canada Balsam. Some roots were cleared by the method of Malamy and Benfey (1997)
.
The relative meristem height (Rost and Baum, 1988
) was determined for the epidermis as the distance from the cap and root body junction to the proximal root portion where the interval between nuclei of neighboring cells in a cell file was approximately equal or less than the diameter of the nuclei and where the epidermis cells were small as judged by length (Dubrovsky, 1997b
; Dubrovsky et al., 1998a
, b
). At the onset of elongation zone, both cell length and the internuclear distance began to rapidly increase.
Cell length was measured with an ocular micrometer. Data on root growth, the length of the growing part of the root, meristem length, and the length of fully elongated cells were collected on individual roots, numbered during growth. The length of fully elongated cells was measured in the root portions when cells completed their elongation during 3, 4, and 5 d of growth after the start of radicle protrusion. The distal border of the root portion formed by the day of growth when cells terminated their elongation was determined in roots that completed their growth as the difference between the root length and the length of the growing part of the root at that day in an individual root. The proximal border of the root portion is at the same position as the distal border of the portion formed on a previous day (Fig. 1). Cell flux (cells per day) was estimated indirectly for each individual root as the number of epidermal cells per root portion in a cell file when cells completed elongation on a certain day. Generally, cell flux is a measure of cell production (Baskin, 2000
). In roots with determinate growth, cell flux may not necessarily reflect cell production as before termination of growth the meristem could be at different stages of its exhaustion (Dubrovsky, 1997b
). In our case, cell flux actually represents the acropetal rate of advance of cell differentiation within single longitudinal cell file (cells per day) and hereafter we use this term. Each experiment was repeated two or three times. The number of replicates of each experiment is indicated in the figures and table. Data were analyzed by Student's t test. Throughout the text plant age indicated in days refers to the day after the start of radicle protrusion.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, b
). When P. pringlei seedlings were grown in this medium with or without sucrose there was no difference in the final primary root length. With or without sucrose a determinate root growth pattern was observed, although final root length varied widely among individual plants (Fig. 2). The coefficient of variation for final root length in plants grown in the medium with sucrose and without sucrose was 16.1% and 20.3%, respectively. As the coefficient of variation of root length was least in the medium with sucrose, this medium was used in all other experiments and these conditions hereafter are called well-watered.
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). If we assume that the decrease in meristem size after 1 d of growth is caused by general blockade of cell division activity, then half of all cells in the meristem will leave the meristem during the time equal to the duration of the cell division cycle similar to the meristems of X-irradiated roots (Ivanov, 1994
). Taking the longest cycle time (equal to 19 h) determined for this species (Dubrovsky et al., 1998a
) and assuming a blockade in cell division, we predicted that the meristem size would decrease much more rapidly than it did in the experiment (Fig. 6B). The striking difference between the predicted curve and real data indicate that during the growth period meristematic cells maintain proliferative activity. The presence of mitotic figures in the root meristems up to 6 d also indicates that meristem exhaustion is a more gradual process in this species than in the previously described determinate growth in genera Stenocereus (Dubrovsky, 1997a
, b
) and Ferocactus (Dubrovsky, 1997b
).
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Under well-watered and moderate water deficit conditions, the duration of growth was on average 8.2 ± 0.4 d (mean ± 1 SE, N = 16) and 8.2 ± 0.3 d (N = 27), respectively, whereas under severe water stress growth was stopped on average at 6.3 ± 0.2 d (N = 24). In an independent experiment similar tendencies were found (Fig. 8). Based on the analysis of the duration of root growth we conclude that under moderate water stress, during the last 2 d, roots grew due to cell elongation. There were no differences in the length of the growing part of the root at day 3 in control plants and plants grown under moderate water deficit (–0.59 and –0.73 MPa, P > 0.05, independent Student's t test) contrary to the shorter root growth zone in roots grown at severe water stress (–1.92 and –2.48 MPa). At the latter conditions, at 8, 9, and 10 d, root hair formation approached the very tip in 63%, 88%, and 100% of roots grown at –1.92 MPa and in all of the roots at –2.48 MPa (Fig. 8C). This indicated that water deficit inhibited root growth by decreasing the duration of determinate root growth and thus induced the determinate developmental program to complete faster.
To determine whether this acceleration was caused by a decrease in cell production or by an inhibition of cell elongation, or both, we compared the length of fully elongated cells and estimated the acropetal rate of advance of cell differentiation. Under both moderate and severe water stress, there were no differences in cell length between samples at 3, 4, and 5 d (Table 1; P > 0.05, independent Student's t test). Under severe water stress, cell length was on average (during 3–5 d of growth) 61% of that in roots grown under well-watered conditions (Table 1). Under water deficit, the acropetal rate of advance of cell differentiation decreased with time similar to that in roots grown at well-watered conditions. It was significantly less at 5 d than at 3 d under both moderate (P < 0.05) and severe (P < 0.001, independent Student's t test) water stress. During the same days of growth, under moderate water deficit, the acropetal rate of advance of cell differentiation was similar to that under well-watered conditions, whereas under severe stress it was only 72% of that under well-watered conditions during days 3 and 4 (Table 1). This indicated that cell production was significantly affected under severe stress and independently showed acceleration of the determinate developmental program under water deficit. Thus, both decreased acropetal rate of advance of cell differentiation and shorter elongated cells caused inhibition of root growth under severe water stress.
Lateral root formation
In plants grown under well-watered conditions, lateral root formation started early in development, during the second day. At early stages, lateral root primordia grew very quickly. At the first day, no primordia were detected, whereas at the second day large primordia were already developed that were composed of hundreds of cells. At day 4, primordia started to emerge on the surface of the primary root as compact and very short lateral roots whose cells maintained the meristematic state (Fig. 9). Young lateral roots had small root caps (Figs. 9 and 10). Similar to the primary root, root hairs in the laterals approach the root tip (Fig. 10). A relatively short time, approximately 2.5 d, was required from lateral root initiation to root emergence. Most of the developed lateral roots were short; sometimes no longer that the length of the root hairs (Fig. 11). In 2 d after their emergence, most lateral roots terminated their growth and their meristem was completely exhausted. These roots developed root hairs up to the very tip similar to primary roots (Fig. 12). Some lateral roots, particularly those located close to the transition zone between root and hypocotyl, were longer due to maintenance of meristematic activity for a longer time. At day 8, initiation of lateral roots of the second order was observed. The second-order lateral roots were developed near the base of the first-order lateral roots. Second-order primordia were formed from the tissues of first-order lateral root (Fig. 13). It may look that they were developed from primary root (Fig. 14). Detailed analysis, however, showed that these are true second-order lateral roots, which start their initiation from the basal portion of the first-order lateral. During the emergence of the second-order laterals, broken tissue of the first-order laterals can be found (Fig. 14). This developmental pattern was similar in plants grown under well-watered and water deficit conditions. In 13-d plants, the total number of first order lateral roots and primordia was on average 13 ± 1 (mean ± 1 SE, N = 40), and there were no differences between well-watered and water stress conditions (P > 0.05, independent Student's t test).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Murawski et al., 1994
). Independent of this variability the pattern of primary root growth under all conditions was found to be determinate without exception.
The comparison of real and hypothetical dynamics of meristem exhaustion (Fig. 6) showed that meristem exhaustion in the P. pringlei root meristem is a gradual process during which cells continue to divide. The nature of determinate root growth in P. pringlei and in the cactus species studied earlier (Dubrovsky, 1997a
, b
; Dubrovsky et al., 1998a
) is similar because meristematic cells are programmed to stop their division activity and to be transformed to non-meristematic differentiated cells. However, there are some important differences. In P. pringlei, under well-watered conditions, root growth and meristematic activity in the root apical meristem were maintained during 8 and 6 d, respectively. If we assume constancy of the duration of cycle time in this species as it is considered in plants in general (Ivanov, 1981
; Ivanov and Dubrovsky, 1997
; Baskin, 2000
), then taking the cycle time (equal to on average 16.9 h) determined for the studied species under similar growth conditions (Dubrovsky et al., 1998a
), we can estimate that during the period after seed germination and before cells stop division, 8–9 cell division cycles should pass in the meristem before its exhaustion. The number of cells in the epidermal meristematic cell file in this species during the short steady-state period is on average 21 (Dubrovsky et al., 1998a
) or between 22 (day 2) and 27 (day 3, present study) indicating that a derivative of each initial cell passes only four or five cell division cycle before the cells start cell elongation. This analysis shows that initial-cell activity is required for the maintenance of the meristem in this species. The developmental program in previously studied species (Dubrovsky, 1997a
, b
; Dubrovsky et al., 1998a
) is completed during a much shorter time and on average meristematic cells pass through only 3–5 cell division cycles, implying the absence of initial-cell activity. So, the principal difference between P. pringlei and previously studied species with determinate growth is how the meristem maintains cell proliferation during or before its exhaustion.
The analysis of cell growth under well-watered conditions has revealed an interesting feature. Considering that up to day 5 the fully elongated cell length did not change (Table 1) and that at the end of root growth 35 distal cells in a single file (Fig. 7) occupied on average a portion of 4.2 ± 0.4 mm (mean ± 1 SE, N = 8), the proximal border of which was formed on average during 5.6 ± 0.4 d of growth (mean ± 1 SE, N = 16), we could conclude that (a) during the period of meristem exhaustion elongating cells have not been affected in their growth (except for the last day) and (b) just at the end of meristem exhaustion (during the last day, day 6) and after that, cells could not elongate to their final potential size (Fig. 7). This indicates that the presence of the meristem is a condition for rapid cell elongation after cells leave the meristem or for transition to elongation.
The water deficit conditions tested in this study are similar to those present in desert environments. For example, roots of Ferocactus acanthodes had maximum root growth at soil water potential equal to –0.6 MPa and higher. Their root growth decreased over 90% at –2 MPa (Jordan and Nobel, 1984
). It is known that dry desert soils can have soil water potentials of up to –10 MPa (Nobel, 1994
). In O. ficus-indica, characterized with indeterminate root growth, various developmental changes occurred in the root apex during gradual drying of the substrate. Over a 14-d period, the length of the meristem, the elongation zone and of the fully elongated cells decreased and the duration of the cell cycle increased as compared with well-watered conditions (Dubrovsky et al., 1998b
). In P. pringlei, the growing part of the root decreases under well-watered conditions as part of the developmental program. Under progressively lower water potential, the growing part of root (Fig. 6C) and the length of fully elongated cells (Table 1) become even shorter. This indicates the similarity in response to water deficit in Cactaceae roots with determinate and indeterminate growth patterns.
In Arabidopsis thaliana under moderate water deficit the length of elongated cells and cell production rate increased (Van der Weele et al., 2000
). In P. pringlei, moderate water deficit did not affect and severe stress significantly inhibited root growth and accelerated the determinate developmental program. Both cell elongation and cell production were inhibited. It is important to note that the acropetal rate of advance of cell differentiation estimated in this study reflected cell production only at earlier growth stages before meristematic cells that stopped proliferation activity. Interestingly, in maize, indeterminate root growth under water stress is inhibited mainly through the inhibition of cell elongation (Sharp et al., 1988
), whereas cell production is also affected (Sacks et al., 1997
). This again demonstrates similarity of response to water stress in species with determinate and indeterminate root growth.
Lateral root development in the studied species was surprisingly similar to that found in Opuntia arenaria and O. tunicata var. davisii. These species develop clusters of sympodially branched roots less than 1 mm long called "root spurs." The root tip of these roots is lacking a root cap (Boke, 1979
). In P. pringlei belonging to a different life form and to a different subfamily, short lateral roots also can be considered root spurs with similar developmental features. These short roots significantly increase root surface area and thus are important for water and solute uptake during short periods of rainfall (Boke, 1979
). Compact but highly branched root systems do not require high carbon input and thus are important for plant carbon economy (Dubrovsky, 1998
).
It was previously shown that, under well-watered growth conditions, the determinate root growth promotes lateral root initiation and was considered a root physiological decapitation leading to induction of lateral root primordia (Dubrovsky, 1997b
). Interestingly, in P. pringlei under well-watered conditions, lateral root primordium initiation apparently was not related to meristem exhaustion. At severe water stress, lateral root density increased on average 1.6 times. Under these conditions, the length of fully elongated epidermal cells decreased on average 1.6 times (between days 3 and 5; Table 1) compared to well-watered conditions. If we assume that pericycle cell length decreased proportionally, then the decreased cell length could explain the increased lateral root density. This then would indicate that increased density of lateral roots was not caused by induction of additional lateral roots, as it was hypothesized. This analysis and the data indicating that there are similar numbers of laterals per plant under all conditions tested demonstrated that even under severe water stress the primary root maintained its basic ability for lateral root formation and that this process is resistant to severe water stress. Such a response can be considered a developmental adaptation important for rapid root system formation and seedling establishment.
In P. pringlei, some lateral roots have determinate growth and others do not. Similar observations were done on S. gummosus (Dubrovsky, 1997a
, b
). It is intriguing to understand why these species stably express determinate developmental program in primary roots, whereas in lateral roots this program is facultative. One possible explanation is that in thin primary roots quiescent center is not established and thus the root apical meristem and root growth cannot be maintained. With age, the shoot biomass is increasing and then some lateral roots can become thicker. This would imply greater size of the meristem. Cell proliferation within the root meristem is one of the requirements for quiescent center establishment (Feldman, 1975
). In these thicker roots, the quiescent center may be established more plausibly. Then the meristem maintenace and root growth can become consistent. Our recent study showed that indeed quiescent center is not established in primary root of these species and these results will be published elsewhere.
Nutrient absorbtion and storage capacities of P. pringlei lateral roots are increasing with plant age when secondary tissues are already developed (Niklas et al., 2002
). This shows the importance of lateral root formation in young seedlings for subsequent plant survival. The most probable elements of early root system formation in this species deduced from developmental features of young seedlings can include the following: (a) formation of a primary root with determinate root growth that becomes a tap root due to the formation of a lateral root at the very tip that replaces the primary root and leads growth in the downward direction; (b) formation of few lateral roots with indeterminate root growth that have an impact on the formation of superficial supportive roots that form sympodially branched roots that extend a few meters from the plant, similar to that shown in other species (Dubrovsky, 1999
); (c) formation of many short-lived determinate lateral roots that are important for an increase in root surface and thus for water and solute uptake (Cannon, 1911
; Jordan and Nobel, 1984
).
Another ecological significance of determinate root growth is related to the root water uptake properties. If a root maintains the meristem, xylem cell differentiation usually occurs at some distance from the root apex and thus the root tip is hydraulically isolated (Steudle and Peterson, 1998
; Barrowclough et al., 2000
; Hsiao and Xu, 2000
). Determinate root growth is a way to avoid such hydraulic isolation of the apical region and thus to facilitate water uptake. Our observations indicate that differentiated xylem elements are in close proximity to the root tip as all meristem cells differentiate (data not shown). When water becomes progressively less available, the determinate state is achieved faster and thus it can be viewed as preparation for subsequent water and solute uptake when water becomes available.
Conclusions
Pachycereus pringlei primary roots exhibited a determinate growth pattern under all conditions tested. With increased water stress its roots terminate their determinate developmental program faster, thereby decreasing hydraulic isolation of the root tip faster. At the same time primary roots produce many short lateral roots that also have determinate growth. These small laterals are branched and increase root surface to promote water and solute uptake. Thus, the main strategy of young plants during seedling establishment is to economize resources needed for the root morphogenesis and to form a very compact root system. Formation of new laterals appears to be a very stable process resistant to severe water stress.
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FOOTNOTES |
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4 Author for reprint requests (jdubrov{at}ibt.unam.mx
)
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LITERATURE CITED |
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