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Ecology |
Department of Biology, Tufts University, Medford, Massachusetts 02155 USA
Received for publication May 24, 2001. Accepted for publication August 23, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: heterogeneity • IPU • Lycopersicon • phenolics • sectoriality • soil nutrients • tomato • vascular architecture
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Within-plant heterogeneity is commonly attributed to differences in tissue developmental stage (e.g., young vs. old leaves), to direct effects of the abiotic environment (e.g., sun vs. shade leaves) and to biotic interactions (e.g., presence or absence of previous damage by herbivores) (Denno and McClure, 1983
; Karban and Baldwin, 1997
). While these factors are important, vascular architecture combined with spatial variation in environmental factors such as soil nutrient availability can determine patterns of within-plant heterogeneity (Orians and Jones, 2001
).
Aboveground growth and development require the transport of resources within the plant. However, transport is generally restricted by vascular architecture to specific subunits, known as integrated physiological units (IPUs; coined by Watson and Casper, 1984
; and further discussed by Watson, 1986
; Sprugel, Hinckley, and Schaap, 1991
; Marshall, 1996
; Orians and Jones, 2001
). This restricted transport within IPUs is referred to as sectoriality. While sectoriality in the movement of signal molecules, photosynthate, and hormones within shoots is commonly recognized (e.g., Murray, Mauk, and Noodén, 1982
; Watson and Casper, 1984
; Sprugel, Hinckley, and Schaap, 1991
; Vuorisalo and Hutchings, 1996
), sectoriality in the transport of resources from shoots to roots (Cook and Stoddard, 1960
; Steiber and Beringer, 1984
; Singleton and van Kessel, 1987
; Murphy and Watson, 1996
) and from roots to shoots (Rinne and Langston, 1960
; Hay and Sackville Hamilton, 1996
) is also prevalent. For example, Rinne and Langston (1960)
performed split-root studies and showed that the movement of phosphorous isotope (P32) was confined to leaves and sides of leaves orthostichous to the labeled roots. These short-term isotope experiments suggest that spatial variation in the availability of soil nutrients might result in heterogeneity in plant growth and traits important to herbivores.
The availability of soil nutrients is one of the key determinants of plant–herbivore interactions (Mattson, 1980
; Bryant et al., 1987
; Hartley and Jones, 1997
). In general, an increase in nutrient availability increases herbivore abundance (Waring and Cobb, 1992
). Because there is extensive spatial variation in soil nutrient availability at scales relevant to individual plants (Lechowicz and Bell, 1991
; Jackson and Caldwell, 1993
; Robertson and Gross, 1994
; Stark, 1994
; Gross, Pregitzer, and Burton, 1995
), studies examining the consequences, if any, of sectorial transport of soil nutrients to aboveground plant parts are relevant. Although the effects of spatial variation in nutrients to the growth of clonal plants is well studied (i.e., Wijesinghe and Handel, 1994
), studies of nonclonal plants are lacking.
In this study, we used split-root techniques to determine the effects of spatial variation in nutrient availability to the growth, chemistry, and morphology of tomato (Lycopersicon esculentum Mill). Tomato is an excellent system to study for two reasons. First, the vascular architecture is well characterized (Dimond, 1966
). Orthostichous leaves are vertically aligned on the stem and have direct vascular connections with one another, and leaves positioned on opposite sides of the stem lack connections; leaves off to one side share partial connections. As a consequence, localized damage causes greater induction of proteinase inhibitors in leaves and leaflets with direct vascular connections (Orians, Pomerleau, and Ricco, 2000
). This sectoriality extends from roots to shoots: dye applied to specific lateral roots travels up to vertically aligned leaves and the proximal leaflets of leaves in adjacent sectors of the shoot (C. M. Orians, unpublished data). Therefore, we hypothesize that sectors with direct vascular connections to fertilized lateral roots differ from sectors without direct vascular connections to those roots.
Second, soil nutrient availability is known to affect chemical traits important to herbivores of tomato (Wilkens, Spoerke, and Stamp, 1996
; Stout, Brovont, and Duffey, 1998
). Stout, Brovont, and Duffey (1998)
found that nitrogen fertilization causes an increase in protein levels, a decrease in the concentrations of phenolics, and a decrease in the activity of polyphenol oxidase in tomato. Similarly, Wilkens, Spoerke, and Stamp (1996)
found that nitrogen availability causes an increase in plant growth and foliar nitrogen availability and a decrease in foliar phenolics (although severely nutrient-limited plants also had low levels of phenolics). These nutrient-induced changes in tomato traits may affect the performance of herbivores on tomato (Minkenberg and Ottenheim, 1990
; Wilkens, Spoerke, and Stamp, 1996
). Minkenberg and Ottenheim (1990)
found that many different indices of performance (e.g., feeding preferences, oviposition rates, growth, etc.) of a leafmining fly were higher on high nitrogen plants. Although not tested, Wilkens, Spoerke, and Stamp (1996)
reported that the differences in phenolic concentrations observed between the different nutrient treatments in their study were sufficient to deter herbivores. These studies suggest that chemical differences among sectors may affect herbivore foraging behavior and performance.
In our experiments, fertilizer was either applied to the main root (and all associated lateral roots) or to a subset of lateral roots from one sector of the root system (Fig. 1). In the short term, we expected increased nutrient uptake in fertilized lateral roots and hypothesized that sectors of the crown with direct vascular connections to these roots would differ in leaf size and chemistry. Specifically, we hypothesized that leaves and leaflets within the fertilized sector would be larger and contain lower concentrations of two phenolics, rutin and chlorogenic acid, since fertilization typically causes an increase in growth and a decrease in investment to these and other carbon-based defenses (e.g., Bryant et al., 1987
; Nichols-Orians, 1991
; Wilkens, Spoerke, and Stamp, 1996
). We focused on these two phenolics because both are known to deter feeding by larvae of Manduca sexta and Spodoptera exigua (Stamp and Yang, 1996
; Yang and Stamp, 1996
). Moreover we hypothesized that side-shoot production would be greater in these sectors.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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3 wk old), we washed the roots and used them in a series of split-root experiments. At this stage, there is a single main root from which clusters of lateral roots exit. These lateral roots are vertically aligned along the main root and are oriented in different directions. We isolated a cluster of 2–3 secondary lateral roots within the same orientation (hereafter termed lateral roots) and placed them in a separate pot from the main root with its attached lateral roots. These plants were then used to determine: (1) the patterns of resource (dye) flow from lateral roots to shoots in tomato; (2) the short-term consequences of belowground variation in nutrients to growth and chemistry; and (3) the long-term consequences of spatial variation in nutrient availability to the production of side shoots.
Experiment 1: mapping resource flow with dye
We quantified patterns of resource flow in tomato by following the movement of rhodamine-B dye. Rhodamine-B dye is a uv florescent dye that is commonly used to map xylem. Six seedlings were planted into separate paired pots (9.6 x 9.6 x 9.0 cm pots taped together with duct tape) containing the same potting soil with the tap root plus lateral roots in one pot and a subset of the lateral roots in the second pot. The split-root seedlings were randomly placed on a greenhouse bench and allowed to establish for 1 wk. Thereafter they were fertilized (20 mL of 0.5 g/L) via their isolated lateral roots and grown an additional 3 wk (seven-leaf stage). At this time, the lateral roots were washed, cut under water, and placed in a beaker with 0.25% rhodamine-B dye. After 12 h, the pattern of dye accumulation within and among leaves relative to the orientation of the lateral roots was determined by visualization under uv. Leaves were assigned to the nearest 45° angle relative to the lateral root (0°, 45°, 90°, 135°, and 180°), and when leaflets on both sides of the petiole received dye, we used relative intensity to determine which side received more dye.
Experiment 2: short-term responses in growth, morphology, and chemistry
Twenty-eight seedlings were each planted into separate paired 20 cm long conical pots (Stuewe and Sons, Corvallis, Oregon, USA) containing potting soil. The tap root (which includes lateral roots from all sectors) was planted into one main pot and isolated lateral roots from one sector were planted into an adjacent lateral pot. As above, seedlings were randomly placed on a greenhouse bench and allowed to establish for 1 wk prior to initiation of fertilization treatments. Once a week, 14 seedlings each received 10 mL fertilizer (0.5 g/L) into the main pot (MP fertilized), and 14 seedlings received equal amounts of fertilizer into the lateral pot (LP fertilized). All root systems were watered four times a day using an automatic watering system so that water would not be limiting. After 2 wk, various aspects of plant growth were measured, and leaf samples were harvested for chemical analyses (described below).
Whole-plant responses
We measured plant height (from the base of the stem) and the number and length of each leaf. We measured root biomass for a random subset of plants (N = 5/treatment). Roots were washed, separated into main and lateral roots, oven-dried for 48 h at 60°C and weighed (in grams). Differences in height, leaf number, leaf size, and root biomass were determined using a one-way ANOVA with fertilization treatment (MP vs. LP fertilized) as the main effect.
Morphology and chemistry of individual leaves
We determined whether fertilizer treatments differentially affected the near and far sides of each leaf (Fig. 1). Because of the selective movement of dye in Experiment 1 (see RESULTS below), we first recorded the position of each leaf as within 45° of that of the lateral root ("same" orientation), from 45° to 135° ("adjacent" orientation) and between 135° and 180° ("opposite" orientation) (Fig. 2). For all leaves, leaflets on the side proximal to the orientation of the lateral root were labeled "near" and those on the opposite side were labeled "far." (Note: since none of the leaves were considered to be directly above or opposite the lateral roots, all leaves had near and far leaflets.)
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We measured the concentrations of two phenolics, rutin and chlorogenic acid (CHA), in the leaflets of the top 2–3 leaves per plant using methods from Broadway et al. (1986) and English-Loeb, Stout, and Duffey (1997)
. Briefly, each excised leaflet (two leaflets per side per leaf) was weighed, placed in vials with 7 mL of 50% methanol : water, and incubated at 60°C for 24 h. After 24 h, extracts were cooled to room temperature and 0.083 mL of extract from the leaflets was added to 1 mL of diphenylborinate reagent (0.5% m : v in 50% ethanol)(N = 2 replicates/sample). We measured absorbance at 390 nm and 440 nm, used standard curves of commercial rutin and CHA to determine extinction coefficients at 390 nm and 440 nm, and then calculated concentration (micromoles per gram fresh leaf mass) of each. We averaged the two replicates per leaflet and then averaged the two leaflets per side to estimate phenolic concentration for the near leaflets and the far leaflets of each leaf.
To determine if near and far leaflets differed in area and chemistry, we performed paired t tests at the beginning (leaf area only) and at the end of the experiment (leaf area and chemistry) for MP- and LP-fertilized plants separately. We paired the mean leaflet area or chemical concentration for the near and far side of each leaf. Leaves were considered independent tests of the effects of orientation ("same," "adjacent," and "opposite") since no two leaves were in exactly the same position on the stem.
Experiment 3: long-term growth responses
Twenty seedlings (ten per treatment) were each planted in separate paired pots (9.6 x 9.6 x 9.0 cm pots taped together) containing the potting soil. Again, the tap root with its associated lateral roots were planted in one main pot, the isolated lateral roots into an adjacent lateral pot, and seedlings were randomly place on a greenhouse bench. We began fertilizing the plants 1 wk later and continued the fertilization treatments for 7 wk. In week 1 the plants received 50 mL of 0.5 g/L fertilizer, either via the main pot (N = 10) or lateral pot (N = 10). Each subsequent week, the dose of fertilizer was increased by 0.5 g/L. This dosage was higher than the short-term experiment because of the greater soil volume in the pots and to ensure the plants did not become nutrient-stressed during this long-term experiment. Plants were watered four times a day using an automatic watering system.
At the end of 7 wk, we determined the orientation ("same," "adjacent," or "opposite") of all side shoots on each plant, the number of side shoots, and the total length of each side shoot. We used a chi-square analysis to determine if the number of side shoots within each orientation deviated from an expectation of 1 : 2 : 1 (same : adjacent : opposite) as the adjacent orientation represents half the total area (Fig. 2). To estimate the effects of treatment (MP and LP fertilized) and orientation ("same," "adjacent," or "opposite") on side-shoot length we used a two-way ANOVA. Within each orientation, the length of all side-shoots was summed and natural log transformed because of a significant correlation between length and variance.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 8.19, df = 2, P < 0.03) (Fig. 6A). In contrast, the number of side shoots within each orientation was as expected for MP-fertilized plants (expected = 1 : 2 : 1, 2 = 0.33, df = 2, P = 0.28) (Fig. 6A).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Eissenstat and Caldwell, 1988
; Jackson, Manwaring, and Caldwell, 1990
; Caldwell, 1994
; Robinson, 1994
; van Vuuren, Robinson, and Griffiths, 1996
). In fact nutrient uptake was so effective that LP- and MP-fertilized plants did not differ in height or leaf number. Nonetheless, sectoriality in nutrient transport from roots to shoots could result in differential "fertilization" of aboveground plant parts.
Within-plant heterogeneity is typically attributed to differences between young and old leaves, sun and shade leaves, and damaged and undamaged leaves. As hypothesized, our results demonstrate that spatial variation in belowground nutrient availability and sectoriality generates predictable heterogeneity in leaf morphology, phenolic chemistry, and plant growth. Sectors with direct connections to the fertilized roots had larger leaves/leaflets, lower concentrations of phenolics, and greater production and growth of side shoots. This pattern of heterogeneity is consistent with published results and reviews describing the movement of isotopes and other tracers from roots to shoots of vascular plants (Rinne and Langston, 1960
; Watson and Casper, 1984
; Hay and Sackville Hamilton, 1996
). Although previous studies have shown that ramets of clonal plants with access to higher nutrient availability grow faster than other ramets (e.g., Wijesinghe and Handel, 1994
), this is the first study to show that sectoriality in nonclonal plants can lead to within-plant heterogeneity in aboveground growth and leaf traits.
Are nonclonal plants likely to encounter sufficient spatial variation in belowground nutrient availability? Several studies and reviews indicate that spatial variation in nutrient availability exists at scales relevant to individual plants (Robertson et al., 1988
; Lechowicz and Bell, 1991
; Jackson and Caldwell, 1993
; Robertson and Gross, 1994
; Stark, 1994
; Gross, Pregitzer, and Burton, 1995
). This variability is created by several factors: microclimatic conditions, microtopography, and the activities of plants and animals (reviewed by Stark, 1994
). For example, when plant cover is low and water is not limiting, an increase in temperature at the soil surface can generate hot-spots of microbial activity and therefore nutrient availability. Animals modify nutrient availability primarily by transporting material: animal matter, fresh plant material, organic debris, or soil (Huntly and Inouye, 1988
; Stark, 1994
; Inouye, Huntley, and Wasley, 1997
). Examples include the concentration of feces at particular sites, the collection of organic matter in the nests of ants and termites, and the movement of nutrient-poor subsoils to the soil surface by burrowing mammals.
Even if there is extensive spatial variation in soil nutrient availability, not all plants or species are expected to be sectorial (reviewed by Orians and Jones, 2001
). Watson and Casper (1984)
suggest that older plants are more sectorial than younger plants. However, our results clearly demonstrate that sectoriality is pronounced in young tomato plants. Sachs, Novoplansky, and Cohen (1993)
further argue that plants can develop new xylem connections in response to changing conditions. Therefore, over time, nutrients might flow from one root sector to the entire plant. Redistribution may also occur via phloem tissue. Finally, spatial variation in water availability also affects patterns of nutrient transport (reviewed by Orians and Jones, 2001
). Since the movement of nutrients is determined by the bulk flow of water through the xylem (Zimmermann, 1971
), patchy water availability may result in nutrient transport from a single root to the entire plant.
There are also differences among species in sectoriality. For example, monocots are less sectorial than dicots (Watson, 1986
). Even among dicots some species are less sectorial (e.g., Shea and Watson, 1989
; personal observation). For sectorial species, we suspect that within-plant heterogeneity will be common and may even increase over time. Once shoots begin to develop within an IPU, photosynthetic rates increase and these shoots become sinks for resources (Dickson, 1991
). The greater rates of carbon fixation in these shoots then increase export of photosynthate to connected roots (Barta, 1976
; Singleton and van Kessel, 1987
), thereby enhancing root growth and nutrient uptake. Therefore, spatial variation in nutrient availability could result in a positive feedback on carbon acquisition by the fast-growing connected shoots, further increasing the differences among sectors and therefore increasing within-plant heterogeneity.
Implications for plant–herbivore interactions
Heterogeneity in leaf morphology and chemistry and in side-shoot growth are likely to affect plant–herbivore interactions (Denno and McClure, 1983
; Price, 1991
; Jones et al., 1993
; Suomela and Nilson, 1994
; Barker, Wratten, and Edwards, 1995
; Suomela, Kaitaniemi, and Nilson, 1995
). Differences in leaf size, nutritional chemistry, and secondary chemistry are important determinants of the quality of leaf tissue to herbivores (reviewed by Hartley and Jones, 1997
). Therefore, nutrient-induced increases in leaf size (and probably nutritional content) together with decreases in secondary chemistry could enhance the growth of herbivores in those sectors. Suomela and colleagues have shown that the growth of Epirrita autumnata (Geometridae) larvae varies by as much as 30% within a single birch tree (Suomela and Nilson, 1994
; Suomela, Kaitaniemi, and Nilson, 1995
; Suomela, 1996
). Perhaps some of this variation is due to belowground variation in nutrient availability. Whitham (1983)
found that gall-forming insects prefer larger leaves of cottonwood, a plant species with documented sectorial control of resource transport (Davis, Gordon, and Smit, 1991
; Jones et al., 1993
; R. Dickson, USDA Forest Service, personal communication), and shoot galling insects generally prefer more rapidly growing shoots (Price, 1991
). These studies suggest that nutrient-induced heterogeneity in leaf size and shoot growth rates may affect the foraging behavior and distribution of herbivores.
At this point we do not know if the within-plant heterogeneity in chemistry and morphology observed in this study is sufficient to deter the behavior or growth of herbivores. We suspect it may for two reasons. First, the combination of CHA and rutin can reduce herbivore growth more than either alone (Stamp and Yang, 1996
). So, although the difference in concentration from one side of the leaf to the other was relatively small, the fact that both chemicals showed the same response increases the likelihood that these differences in chemistry have biological relevance. Second, although not measured in this study, fertilization typically increases foliar nitrogen levels (Minkenberg and Ottenheim, 1990
; Wilkens, Spoerke, and Stamp, 1996
), and small differences in foliar nitrogen can have big effects on herbivore behavior and growth (Minkenberg and Ottenheim, 1990
).
In conclusion, spatial variation in belowground nutrients can generate predictable heterogeneity in growth, morphology, and chemistry of sectorial species and this heterogeneity is likely to affect a plant's interactions with herbivores. We predict that aboveground plant sectors with connections to high nutrient soil patches will have increased foliar nitrogen, decreased foliar phenolics, and should generally be more suitable to herbivores. Future studies should examine these ecological interactions.
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FOOTNOTES |
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2 Author for reprint requests (Colin.Orians{at}tufts.edu
, Fax: 617-627-3805).
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 T. M. B. a. C. M. Orians Vascular pathways constrain 13C accumulation in large root sinks of Lycopersicon esculentum (Solanaceae) Am. J. Botany, June 1, 2006; 93(6): 884 - 890. [Abstract] [Full Text] [PDF]
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 C. M. Orians, S. D.P. Smith, and L. Sack How are leaves plumbed inside a branch? Differences in leaf-to-leaf hydraulic sectoriality among six temperate tree species J. Exp. Bot., August 1, 2005; 56(418): 2267 - 2273. [Abstract] [Full Text] [PDF]
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M. A. Zwieniecki, C. M. Orians, P. J. Melcher, and N. M. Holbrook Ionic control of the lateral exchange of water between vascular bundles in tomato J. Exp. Bot., May 1, 2003; 54(386): 1399 - 1405. [Abstract] [Full Text] [PDF]
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