| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Botany, University of Texas, Austin, Texas 78713
Received for publication October 21, 1997. Accepted for publication June 23, 1998.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: anatomy • Cactaceae • Cereus • development; environment; wood
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Environmental factors affect plant vigor and health, but little is known about how such factors might influence a plant's internal structure. Many agricultural studies have examined responses such as crop yield, but there have been few studies dealing with morphogenic effects (Nobel, 1988
, 1996
; Larcher, 1995
). Penfound (1931)
reported that Helianthus annuus and Polygonum hydropiper produced more and larger vessels if given increased water. Doley and Leyton (1968
, 1970)
found that moisture level affected vessel diameter in Fraxinus excelsior, and Bissing (1982)
had similar results in a study of several dicots. Formation of aerenchyma and root hairs was also affected by environmental factors (Drew, Jackson, and Gifford, 1979
; Kawase, 1979
; Etherington, 1984
; Heathcote, Davies, and Etherington, 1987
; Jackson, Manwaring, and Caldwell, 1990
), and increased light induced the formation of leaves with a higher density of stomata, veins, and chlorophyll (Tselniker, 1978
; Goryshina, 1980
, 1989
). Low nitrogen supply induced altered growth rate and lignification of leaf epidermis and nonveinal sclerenchyma in Poa, but few anatomical characters were examined (Van Arendonk et al., 1997
). Even experiments examining effects of elevated CO2 seem to study few anatomical responses other than changes in stomatal density (Raschi et al., 1997
). Surprisingly, this short list appears to be the bulk of the experiments related to the effect of environmental factors on plant structure. Yet a plant's developmental response to environmental conditions is a factor in determining whether that species survives environmental change or is affected deleteriously by it.
Due to the scarcity of experimental data we decided to examine anatomical responsiveness to environment. Cacti were chosen for the study because our experience has shown them to be morphologically responsive to variations in environmental factors, and many have complex polymorphic anatomy (Mauseth, 1993
; Mauseth and Plemons-Rodriguez, 1997
, 1998
) so anatomical responsiveness might also be expected. Because many cacti are adapted to habitats of extreme aridity, intense insolation, and mineral-rich soils, even small increases in global rainfall and cloudiness would be significant changes for them.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
After acclimation, plants of each species were randomly assigned to treatments. Plants were depotted and the roots gently washed to remove all fertilizer, then the plants were repotted using a 1:1 mixture of potting soil and vermiculite. Plants were measured for height and for diameter at base, mid-height, and 5 cm below the apex. Plants were allowed to recover from repotting by being irrigated with water only, once each week, until treatments began in August 1994.
Experimental treatments were high, medium, and low levels of light, water, nitrogen, and phosphorus. High light was full ambient light inside the greenhouse augmented with 12 h of fluorescent lighting per day. This provided an average photosynthetically active radiation (PAR) of 1720 µmol photons·m-2·s-1. Medium and low treatments were the same as high light except that plants were placed under shade cloth that reduced light by 50 % (PAR of 860 µmol photons·m-2·s-1) or 90 % (PAR of 170 µmol photons·m-2·s-1). PAR was measured ten times over the year using a LI-COR, Inc. model LI-1600 (LI-COR, Lincoln, Nebraska) steady-state poromoter with light meter. Plants receiving high or low light received medium water and medium nutrient levels.
Plants receiving high water treatment were watered twice each week, once with water only and once with fertilizer, each time receiving enough to exceed field capacity. The soil was never allowed to dry out. Plants in medium water treatments received enough fertilizer solution to exceed field capacity once each week. Soil in these pots was normally dry 1 or 2 d each week. Plants receiving low water treatment received 60 mL of fertilizer solution each week, and the soil was normally dry 4 or 5 d between watering. Plants receiving experimental treatments of water or one of the other factors were given medium light.
Fertilizer treatments were as follows. High nitrogen (53-20-20) was prepared by mixing 33-0-0 and 20-20-20 (total NPK concentration of 3200, 800, and 800 ppm). High phosphorus (20-66-20) was prepared with 20-20-20 plus 0-46-0 (total NPK concentration of 800, 3800, and 800 ppm). Medium fertilizer treatments were given 20-20-20 instant mix alone (NPK concentration of 800, 800, and 800 ppm). Low nitrogen treatment was a mix of 0-20-0 and 0-0-20 (NPK concentration of 0, 800, and 800 ppm). Low phosphorus treatment was prepared from 20-0-0 and 0-0-20 (NPK concentration of 800, 0, and 800 ppm). The water-soluble fertilizer used was Greenlight brand 20-20-20, produced by Greenlight, Inc., San Antonio, Texas. The N (as NH4NO3), P (as P2O5 either 800 or 3000 ppm), and K (as K2O-soluble potash) used to modify the solutions were granular fertilizers manufactured by Green Diamond, Inc., Bay City, Texas. The granules were ground to the consistency of fine powder to make them water soluble also. High treatment solutions were prepared by mixing 2.4 g of commercial instant mix per litre of water and the addition of either 0.8 g of NH4NO3 or 1.0 g of 3000 ppm P2O5. Low nitrogen treatment was prepared by mixing 0.9 g of 800 ppm P2O5 and 0.7 g of K. Low phosphorus treatment was a combination of 0.8 g of N (as NH3, NO3 and urea) and 0.8 g K (as K2O-soluble potash).
The treatments were as follows: "control" plants received medium light, water, nitrogen, and phosphorus. Experimental plants (everything except the control plants) received medium levels except for the experimental factor; for example, plants in the "high light" treatment received high light but medium water, nitrogen, and phosphorus.
Temperature was maintained between 24° and 27°C.
All plants were maintained in treatment from 1 August 1994 until they were harvested beginning 1 August 1995. At harvest, each plant was again measured for height and diameter. For Cereus tetragonus, whose plants are highly branched, all branches were removed and measurements taken from the main stem.
Plants were harvested by severing the main stem at ground level. To separate the original growth from growth that had occurred during treatment each plant was cut in two transversely at the height the plant had been when treatment was initiated. Histological samples were obtained from basal, middle, and apical regions of both the lower portion and the upper portion. All tissues in the upper portion had been initiated and had developed during treatment; in the lower portion, all primary tissues had been initiated and had matured prior to treatment. In the lower portion of the stem, the innermost, oldest wood had been produced prior to treatment and the outermost wood, adjacent to the vascular cambium, had been produced during treatment. Samples were fixed and processed as described by Mauseth, Montenegro, and Walckowiak (1984)
. Tissues were analyzed using brightfield microscopy.
When collecting wood data from the base of the plants (in the region of the stem that had existed before the experiment started), care was taken to ensure that only cells produced during the experimental period were used: measurements and counts were restricted to within 200 µm of the vascular cambium. For each species in each treatment, at least 250 vessels were measured for lumen diameter. They were also scored as to occurrence in clusters or as solitary vessels. Vessel density was measured as the number of vessels per square millimetre of axial wood only; rays were not included in the measurement. Vessel density has been calculated this way in other studies of cacti (Mauseth, 1996
; Mauseth and Landrum, 1997
; Mauseth and Plemens-Rodriguez, 1998
) to eliminate variability that would result from differences in relative volume of rays in wood. For each species in each treatment, 55 fields were sampled at 40x (field size = 21300 µm2) and all vessels in each field were counted.
Within each species, treatment means for each character were analyzed using the ANOVA function of PROC GLM in PC-SAS v6.11. If main effects were significant, then pairwise comparisons were made between the control and other treatment means using PROC TTEST with Cochran option (SAS, 1996
).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
|
Mean diameter of all vessels
In both species, vessels occurred either as solitary vessels or as small clusters of 2–5 vessels. In all treatments, vessels were narrow, with a grand mean diameter (mean ± 1 SE of all vessels in all treatments) of 31.0 ± 1.5 µm in C. peruvianus and 26.0 ± 0.8 µm in C. tetragonus. Mean vessel diameters in control plants (those receiving medium levels of light, water, and nutrients) were (32.4 ± 2.6 µm in C. peruvianus and 27.9 ± 0.5 µm in C. tetragonus) (Table 1, column 3). The only treatments that significantly altered mean vessel diameter were those of deprivation: low water, low nitrogen, and low phosphorus. In C. tetragonus, low water was correlated with narrower vessels (P < 0.05), but in plants receiving high water, vessels were not significantly different from those of either the control or the grand mean of all treatments. In C. peruvianus, neither water treatment produced a significant effect, even though high water had caused most plants to elongate greatly. Even if the aberrantly short plant no. 5 should be removed, mean vessel diameter would not change and would not become significantly different from the control. Low nitrogen and low phosphorus in C. peruvianus (which caused reduced shoot elongation) induced a significant reduction in vessel diameter relative to vessels in the control plants and relative to the grand mean of all treatments, but low light exerted no effect. In C. tetragonus, low nitrogen and low phosphorus did not produce any significant alteration in vessel diameter.
High levels of light, water, nitrogen, and phosphorus were not correlated with any significant change in vessel diameter. No treatment resulted in vessels significantly wider than those of control plants.
Diameter of solitary vessels vs. clustered vessels
Solitary vessels were significantly (P < 0.05) wider than clustered ones in both species: in every treatment, mean diameter of solitary vessels was wider than that of clustered vessels (Table 1, columns 4 and 5). Consequently, the effects of low nutrient treatments discussed above could have been due to the effects on vessels in general or due to the effects on just solitary vessels or just clustered vessels or on the ratio of solitary to clustered vessels. In C. tetragonus, low water treatment resulted in narrower mean vessel diameter due to significant decreases in the diameters of both solitary (P < 0.002) and clustered (P < 0.02) vessels. In C. peruvianus, low nitrogen also acted by significantly (P < 0.05) reducing mean diameters of both solitary and clustered vessels. However, the low phosphorus effect was due to a significant narrowing only of clustered vessels; solitary vessels were not significantly affected (P < 0.06). When both vessel types were considered together (above), variability was so great that high nitrogen treatment seemed to have no effect, but by obtaining mean values for solitary and clustered vessels separately, variability was reduced and revealed that in C. tetragonus high nitrogen treatment was correlated with a significant (P < 0.01) narrowing of solitary vessels but only a moderate (P < 0.06) narrowing of clustered ones.
Ratio of solitary to clustered vessels
The percentage of vessels that were solitary was extremely variable within each treatment in both species. In C. tetragonus, between 34 and 57% of all vessels occurred as solitary vessels (Table 1, column 6), but neither was statistically significant because of the high variability within each treatment. In C. peruvianus, the high light treatment had a significantly (P < 0.03) low percentage of solitary vessels (22%), but no other treatment was significantly different from the controls.
Vessel density
Vessel density was high in both species, with a grand mean of all treatments of 381 vessels/mm2 in C. peruvianus and 256 vessels/mm2 in C. tetragonus; in most treatments, density was quite variable with standard deviations being 10–30% of their respective means. In C. tetragonus, mean density varied from 224 to 297 vessels/mm2 (Table 1, column 7) but no treatment caused a significantly high or low density. In C. peruvianus, the range was greater, from 173 to 580 vessels/mm2, the low value differed significantly (P < 0.03) from the control, and both of these extremes occurred in light treatments: low vessel density in low light and high density in high light. High water treatment, which had induced greatly increased shoot elongation in four of five samples of C. peruvianus, did not cause increased vessel density.
Mean amount of wood per axial bundle
Interfascicular cambium develops only slowly in these species; consequently during the course of the experiment all wood was produced by fascicular cambia. Each sympodium remained a discrete bundle separated from adjacent bundles by primary rays. Mean amount of wood per bundle was calculated in transverse section from ten bundles per plant. Radial length of each bundle was measured from metaxylem to vascular cambium, and width was measured at midlength. In C. tetragonus, high nitrogen (P < 0.02) and low water (P < 0.04) were correlated with significant decreases in the mean amount of wood produced per axial bundle (Table 1, column 8). In C. peruvianus the mean amount of wood per bundle was not significantly affected by any treatment, even high water, and even the one plant in this set that was aberrantly short (see above) had an average amount of wood per bundle.
Estimated specific conductance
An approximate estimate of the potential conducting capacity per square millimetre of wood can be obtained by multiplying mean vessel density by mean vessel radius taken to the fourth power (conductance is proportional to r4; Zimmerman, 1983
); this is the estimated specific conductance. In C. peruvianus, low nitrogen (P < 0.01) and low phosphorus (P < 0.01) caused a reduction in estimated specific conductance due to a significant reduction in mean vessel diameter (see Table 1, columns 3, 7, and 9). Low light caused a significant (P < 0.03) reduction of estimated specific conductance due to a significant decrease in mean vessel density (Table 1, column 7) rather than diameter. A significant decrease in the estimated specific conductance values for C. tetragonus occurred with high nitrogen (P < 0.003), low nitrogen (P < 0.03), and low water (P < 0.03) treatments. High phosphorus (P < 0.04) produced a significant increase in estimated specific conductance. In all cases except low water, the significant effect on estimated specific conductance resulted from nonsignificant changes in vessel diameter and density.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Mauseth, 1988
), even cacti (Mauseth and Plemons-Rodriguez, 1997
, 1998
). It seems logical that environmental factors that increase growth rate, especially an abundance of water, should induce plants to produce broader vessels, especially because this would not involve production of a new type of cell but rather producing more of a cell type that it already produces (broad vessels) and producing fewer of another (narrow vessels). This was reported for Helianthus and Polygonum (Penfound, 1931
) and Fraxinus (Doley and Leyton, 1968
, 1970
) but not in cacti. For desert-adapted plants, water is available episodically as brief rainy periods that alternate with long droughts, so it may be more adaptive for their wood morphogenic mechanisms to respond to long-term average conditions rather than to transitory ones. If so, morphogenic mechanisms should be relatively self-controlling rather than be responsive to environmental conditions. Significant effects were seen primarily in treatments of deprivation. The low light treatment, 10% of ambient, almost certainly must have been a severe deprivation for these species whose natural habitat is full-light areas. However, none of the plants manifested signs of etiolation or even slightly abnormal growth. It is difficult to be certain of the true level of deprivation of nitrogen, phosphorus, and water: residual amounts would have remained in the plant bodies, although nutrient reserves should have dropped to extremely low levels after a full year of deprivation. The objective of this study was not to study wood morphogenesis in the absolute absence of these minerals but rather at low levels that might be encountered in nature. These results indicate that plants in nature or in cultivation are unlikely to experience such low levels of these factors that wood morphogenesis would be significantly affected.
In the presence of high amounts of light, nitrogen, phosphorus, and water, wood undergoes normal morphogenesis and develops characters almost indistinguishable from those of control plants, that is, plants receiving moderate amounts of these factors. Apparently once low or moderate amounts of these factors are present, wood develops normally.
In most woody plants, annual wood production is closely correlated with environmental conditions. Annual rings of trees in temperate forests are broader if produced during favorable years than if produced during times of stress. Many cacti, these included, produce so little wood each year that the production of even a few more cells should have been readily detectable.
While this study was in progress, other investigations revealed that whereas numerous types of highly modified wood have evolved in Cactaceae (Mauseth, 1993
; Mauseth et al., 1995
; Mauseth and Plemons, 1995
; Mauseth and Plemons-Rodriguez, 1997
, 1998
), fibrous woods such as those in C. peruvianus and C. tetragonus have been extremely stable and unchanging evolutionarily (Mauseth and Landrum, 1997
; Mauseth and Plemons-Rodriguez, 1998
). The fibrous woods of cacti adapted to extreme desert conditions, to mesic habitats, and even to rain forests are similar in terms of vessel diameter and density, whereas the percentage of vessels that are solitary varies greatly in no discernible pattern. Apparently the morphogenic mechanisms that control maturation of fibrous woods are extremely stable developmentally (as demonstrated here) and evolutionarily.
Several cactus species produce dimorphic wood, that is, they produce one type while young and another type while older (Mauseth and Plemons, 1995
; Mauseth and Plemons-Rodriguez, 1997
, 1998
). The experimental treatments here did not induce any type of wood dimorphism.
Even though wood anatomical characters appear stable despite environmental treatments, the functional capacity of the wood, as approximated by the estimated specific conductance, appears to change significantly in response to some treatments. In C. peruvianus, low light levels caused such a major reduction in vessel density that the estimated specific conductance decreased. Similarly, low nitrogen and low phosphorus produced a lower estimated specific conductance by inducing the formation of narrower vessels. However, other treatments reduced the estimated specific conductivity by inducing the formation of vessels that were only slightly narrower and slightly less abundant than those in control plants. If estimated specific conductance is a reasonably good estimator of a plant's capacity to conduct water, then a plant might be able to alter its hydraulic conductance by making statistically imperceptible changes to several characters simultaneously.
From these results, it seems that if global environmental change causes the habitat of these two cacti to become cloudier and wetter, the two species will be adversely affected. Most individuals do not undergo altered development that might make them more adapted to the new conditions. Assuming that their bodies are well-adapted for current climatic conditions, as the environment changes, they will continue to produce the same type of body, even though it is not adapted to the new conditions. Some individuals (such as sample no. 5) would possibly succumb quickly, altering the gene pool.
|
FOOTNOTES |
|---|
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Carlquist, S. 1988 Comparative wood anatomy. Springer-Verlag, Berlin.
Doley, D., and L. Leyton. 1968 Effects of growth regulating substances and water potential on the development of secondary xylem in Fraxinus. New Phytologist 67: 579–594.[CrossRef]
———, and ———. 1970 Effects of growth regulating substances and water potential on the development of wound callus in Fraxinus. New Phytologist 69: 87–102.[CrossRef]
Drew, M. C., M. B. Jackson, and S. Gifford. 1979 Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L. Planta 147: 83–88.[CrossRef][ISI]
Etherington, J. R. 1984 Comparative studies of plant growth and distribution in relation to water logging. Journal of Ecology 72: 389–404.[CrossRef]
Goryshina, T. K. 1980 Structural and functional features of the leaf assimilatory apparatus in plants of a forest-steppe oakwood. I. Leaf plastid apparatus in plants of various forest strata. Acta Oecologica 1: 47–54.
———. 1989 Fotosinteticheskii apparat rasteni I usloviya sredy. Izdatel'stvo Leningrad University, Leningrad.
Heathcote, C. A., M. S. Davies, and J. R. Etherington. 1987 Phenotypic flexibility of Carex flacca Schreb. New Phytologist 105: 381–391.[CrossRef][ISI]
Jackson, R. B., J. H. Manwaring, and M. M. Caldwell. 1990 Rapid physiological adjustment of roots to localized soil enrichment. Nature 344: 58–60.[CrossRef]
Kawase, M. 1979 Role of cellulase in aerenchyma development in sunflower. American Journal of Botany 66: 183–190.[CrossRef][ISI]
Larcher, W. 1995 Physiological plant ecology. Springer-Verlag, Berlin.
Mauseth, J. D. 1988 Plant anatomy. Benjamin/Cummings, Redwood City, CA.
———. 1993 Water-storing and cavitation-preventing adaptations in wood of cacti. Annals of Botany 72: 81–89.
———. 1996 Comparative anatomy of tribes Cereeae and Browningieae (Cactaceae). Bradleya 14: 66–81.
———, and J. V. Landrum. 1997 Relictual vegetative anatomical characters in Cactaceae: the genus Pereskia. Journal of Plant Research 110: 55–64.
———, G. Montenegro, and A. M. Walckowiak. 1984 Studies of the holoparasite Tristerex aphyllus (Loranthaceae) infecting Trichocereus chilensis (Cactaceae). Canadian Journal of Botany 62: 847–857.
———, and B. J. Plemons. 1995 Developmentally variable, polymorphic woods in cacti. American Journal of Botany 82: 1199–1205.[CrossRef][ISI]
———, and B. J. Plemons-Rodriguez. 1997 Presence of paratracheal water storage tissue does not alter vessel characters in cactus wood. American Journal of Botany 84: 815–822.[Abstract]
———, and ———. 1998 Evolution of extreme xeromorphic characters in wood: a study of nine evolutionary lines in Cactaceae. American Journal of Botany 85: 209–218.[Abstract]
———, Y. Uozumi, B. J. Plemons, and J. V. Landrum. 1995 Structural and systematic study of an unusual tracheid type in cacti. Journal of Plant Research 108: 517–526.[CrossRef][ISI]
Nobel. P. S. 1988 Environmental biology of agaves and cacti. Cambridge University Press, New York, NY.
———. 1996 Shading, osmoticum, and hormone effects on organ development for detached cladodes of Opuntia ficus-indica. International Journal of Plant Science 157: 722–728.
Penfound, W. T. 1931 Plant anatomy as conditioned by light intensity and soil moisture. American Journal of Botany 18: 558–572.[CrossRef][ISI]
Raschi, A., F. Miglietta, R. Tognetti, and P. R. van Gardingen [eds.] 1997 Plant responses to Elevated CO2 evidence from natural springs. Cambridge University Press, New York, NY
SAS. 1996 SAS for windows v6.11. SAS Institute, Cary, NC.
Tselniker, Y. 1978 Fiziologicheskie osnovy tenevynoslivosti drevesnykh rastenii. Nauka, Moskva.
Van Arendonk, J. J. C. M., G. J. Niemann, J. J. Boon, and H. Lambers. 1997 Effects of nitrogen supply on the anatomy and chemical composition of leaves of four grass species belonging to the genus Poa, as determined by image-processing analysis and pyrolysis-mass spectrometry. Plant, Cell and Environment 20: 881–897.[CrossRef]
Zimmerman, M. H. 1983 Xylem structure and the ascent of sap. Springer-Verlag, Berlin.
This article has been cited by other articles:
|
|
 |
|
  N. SCHMITZ, A. VERHEYDEN, H. BEECKMAN, J. G. KAIRO, and N. KOEDAM Influence of a Salinity Gradient on the Vessel Characters of the Mangrove Species Rhizophora mucronata Ann. Bot., December 1, 2006; 98(6): 1321 - 1330. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. D. MAUSETH Structure-Function Relationships in Highly Modified Shoots of Cactaceae Ann. Bot., November 1, 2006; 98(5): 901 - 926. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. L. Cooper and D. D. Cass Comparative evaluation of vessel elements in S alix spp. (Salicaceae) endemic to the Athabasca sand dunes of northern Saskatchewan, Canada Am. J. Botany, April 1, 2001; 88(4): 583 - 587. [Abstract] [Full Text]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
