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The effects of developmental stage and source leaf position on integration and sectorial patterns of carbohydrate movement in an annual plant, Perilla frutescens (Lamiaceae)¹

^a Department of Biology, Indiana University, Bloomington, Indiana 47405

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
A well-integrated plant shows extensive carbohydrate translocation through the plant body. Even in highly integrated plants, however, translocation patterns will be sectorial if vascular tissue restricts carbon movement to sectors along stems. Both integration and sectorial translocation patterns are sensitive to plant architecture and thus may change as a plant develops. These patterns should vary also with the position of the source leaf because leaves at each node are unique in age and vascular relationship to the rest of the plant. I measured the effects of developmental stage and location of the source leaf on integration and sectoriality in an annual plant, Perilla frutescens, by labeling plants with C at one of three leaves and four developmental stages. Stage and source leaf affected both integration and sectoriality. Most notably, integration declined and sectoriality increased during seed fill, when resource demand at each node was high. Furthermore, translocation was least extensive from the leaf supporting the largest number of seeds on its axillary branch. These results suggest that plants are not homogeneous collections of subunits; rather, the role of each leaf in a plant's carbon budget is a function of its age and location on the plant.

Key Words: allocation • carbohydrate translocation; • integration • Lamiaceae • module • Perilla frutescens • sectoriality

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Unlike most animals, plants grow and develop by producing new morphological subunits, or "modules" (e.g., branches, ramets), from meristems. White (1979) pointed out that viewing plants as assemblages of morphological subunits can enhance our understanding of the dynamics of entire plants and plant populations. It is important to remember, however, that plants are not homogeneous assemblages of subunits. Because modules are produced throughout the life of a plant, and each module arises from another, they are diverse in age and in their relationship to the rest of the plant (Harper and Bell, 1979; Diggle, 1994; Watson, Geber, and Jones, 1995).

Furthermore, the modules composing a plant are generally neither fully independent nor universally interdependent. Plants can be divided into Integrated Physiological Units (IPUs), groups of modules that function as a unit for carbon assimilation and use, but that together are relatively independent from the rest of the plant (Watson and Casper, 1984). The boundaries of these IPUs can change during growth as a plant's morphology becomes more complex (Watson and Casper, 1984). Many studies have sought to define the relationship between morphological subunits (modules) and physiological subunits (IPUs) in a variety of plants. These studies have explored two distinct types of physiological relationship: integration and sectoriality (Fig. 1).

View larger version (39K): [in this window] [in a new window]   Fig. 1. (a) Diagram of Perilla frutescens, illustrating the concepts of integration and sectoriality. The plant is said to be well integrated because CO2 assimilated by the labeled leaf (in black) is recovered from leaves and axillary branches at distant nodes (shaded areas), where it was translocated. Note that the amount of label, indicated by the intensity of shading, declines with distance from the labeled leaf. The distribution of labeled assimilate is sectorial, however, because it is restricted primarily to the same side of the stem (the same vascular bundles) as the labeled leaf. The labeled orthostichy has the highest activity, followed by the adjacent orthostichy (branches and leaves represented by squares and half circles), and in the opposite orthostichy only one node contains any label. Activity was recovered from the stem also, but it is not shown here. (b) Cross section of the main axis, showing the vascular bundles. Leaves and branches on each side of the square stem are supplied by the pair of bundles running through the corners on that side. One bundle supplies half of two adjacent sides, as illustrated in this diagram by the dark grey bundle containing the white star.

Of these two components of resource movement, integration has been the more intensively studied, particularly in clonal plants. Researchers have investigated the ecological consequences of resource movement between ramets under resource-poor (Jónsdóttir and Watson, 1997) or spatially heterogeneous conditions such as density (Williams and Briske, 1991; Hartnett, 1993), light availability (Tissue and Nobel, 1990; Kemball, Palmer, and Marshall, 1992; Stuefer, During, and de Kroon, 1994), and nutrient availability (Alpert, 1991; Hartnett, 1993; Wijesinghe and Handel, 1994). Even in a constant and homogeneous environment, however, the relationships among modules are likely to be complex because they change throughout development (Harper and Bell, 1979; White, 1979; Diggle, 1994). Thus, there is potentially significant spatial and temporal variation in resource movement among modules due simply to intrinsic changes in plant morphology.

Such developmentally based shifts in resource movement are of interest to agricultural researchers who want to determine which leaves assimilate most of the carbon used for seed fill and at what stages this occurs (Hale and Weaver, 1962; Pate, Atkins, and Perry, 1980; Watson and Casper, 1984; Ho, 1996). Others have sought to link seasonal patterns of movement to growth form (Ginzo and Lovell, 1973), branching structure (Chapman, Robson, and Snaydon, 1992), and evolved response to herbivory (Dyer et al., 1991) or damage (Landa et al., 1992). Compared to the number of studies on perennials, very few studies have examined temporal variation in integration in non-crop annuals (but see Lacey and Marshall, 1992).

Like integration, sectoriality has important ecological implications, including effects on competitive interactions among plant parts (Watson, 1986), growth following defoliation (Thomas and Watson, 1988; Price, Marshall, and Hutchings, 1992), and tolerance of marginal habitats (Larson, Doubt, and Matthes-Sears, 1994). Much of the ecological interest in sectoriality has been focused on changes in sectoriality under stress. Thlaspi arvense maintains sectorial translocation of C even when leaves supporting fruit growth are removed from an orthostichy (Benner, Fitzpatrick, and Watson, 1989). In some cases, defoliation or inflorescence removal weakens sectorial constraints (Garrish and Lee, 1989; Shea and Watson, 1989; Price, Marshall, and Hutchings, 1992). These results demonstrate that the vascular architecture of a plant does not absolutely determine patterns of carbohydrate translocation and that these patterns may be modified by manipulating modules. Therefore sectoriality, like integration, might also be sensitive to ontogenetic changes in module number and arrangement. Very few studies have addressed this question, but results from trees (Larson and Dickson, 1973; Barlow, 1979) indicate that sectoriality is sensitive to developmental stage and to the location of the source leaf relative to the tissues it supports.

The purpose of this study was to construct a profile of carbohydrate movement from various source leaves throughout the development of an annual plant, Perilla frutescens. I examined changes in both integration and sectoriality during development using source leaves at different positions along the plant's main axis. Perilla frutescens Britt. (Lamiaceae) is a short-day photoperiodic annual. A single upright axis bears opposite leaves and branches, each pair emerging at right angles to the last (decussate phyllotaxis). At floral induction, all active meristems produce indeterminate inflorescences. Perilla has a simple vascular architecture: leaves and branches on the same side of the square stem share vascular bundles, leaves and branches on adjacent sides share half of their bundles, and those on opposite sides have no bundles in common (Fig. 1).

	MATERIALS AND METHODS

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Field-collected seeds of Perilla were placed on wet filter paper, and those germinating within a week were transplanted into flats containing equal parts perlite and Metro-Mix 360. Twenty-one days later, the largest 120 seedlings were transplanted individually into 7.5-cm pots filled with Metro-Mix 360. Plants received ambient light supplemented with arc lights on a 1430/0930 light/dark schedule. Fertilizer was added weekly beginning day 31 (25 mL of standard Peter's solution). On day 81 the photoperiod was changed to induce flowering (1330/1030 light/dark). All plants opened their first flowers on day 106, 3.5 wk after induction. One month later all leaves had abscised. The experiment ended 23 wk after germination, when all seeds were mature.

Treatments
Plants were assigned randomly to treatment and arranged in randomized blocks along a greenhouse bench. On each plant, a single leaf either at the middle node (node 6) or near the base (node 3) or tip (node 9) of the plant was labeled once with C at one of four developmental stages (early and late vegetative, early and late reproductive). The limits of the first three developmental stages were based on the position of the youngest fully expanded leaf (leaves 3, 6, and 9, respectively). The late reproductive stage began when approximately half of all flowers on terminal inflorescences had opened. Because leaves 6 and 9 had not developed by the early labeling stages, not all combinations of leaf and stage were possible. I exposed leaves to 9.35 x 10 Bq of CO₂ for 15 min in a clear plastic enclosure, as in Landa et al. (1992). Plants were harvested either 1 wk after labeling ("early harvest") or when fully senesced ("mature harvest").

Aboveground portions of the harvested plants were separated into main stems and terminal inflorescences. Leaves and branches were removed and grouped by orthostichy; leaves and branches sharing the orthostichy of the labeled leaf ("labeled orthostichy") were further divided by node. Leaves and branches from the orthostichies adjacent to the labeled one had equivalent vascular relationships with the labeled leaf and so were consolidated into a single sector ("adjacent orthostichies"). Plants harvested at maturity no longer had leaves, so they were composed of fewer parts than the early-harvest plants.

Plant parts were dried at 60°C, weighed individually and ground in a Wiley mill fitted with a number 20 mesh. For each plant part, two subsamples of ground material were weighed and combusted at 900°C for 2 min in a biological oxidizer (model 4000, R. J. Harvey Instrument Corporation, Hillsdale, New Jersey). The CO₂ liberated from each sample was collected into 10 mL of C Cocktail (Harvey Instrument Corp., Hillsdale, New Jersey) and transferred into scintillation vials, which were counted for 5 min each in a scintillation counter (model LS230, Beckman Instruments, Fullerton, California).

Analysis
The mean specific radioactivity of a part [disintegrations per minute per milligram dry mass] reflects its ability to draw assimilate from the labeled leaf, independent of its size. Although specific activity is useful for comparing parts within a plant, between-plant comparisons can be problematic: specific activity depends on the amount of label taken up by the entire plant, which is sensitive to environmental conditions during labeling and the age of the labeled leaf. To minimize the effects of between-plant variation in total activity, I converted specific activity to relative specific activity (RSA) by dividing the specific activity of each part by the specific activity of the entire shoot (Mor and Halevy, 1979). If radioactive carbohydrates are distributed uniformly over a plant body, then the activity of each part is proportional to its mass and the RSA of each part will be one. Any part with an RSA greater than one contains more label than expected under the null model of uniform distribution. To estimate total activity of a plant part, I multiplied the specific activity of that part by its total mass. The total mass and total activity of all plant parts were summed for each plant, yielding total aboveground mass and activity by plant. Like specific activity, the total activity of a plant part depends on the amount of label assimilated by the plant; therefore, the total activity of each part was converted to a percentage of the total activity of the plant (%TA).

Temporal changes in carbon movement to stems were characterized using two-way analyses of variance with source leaf and labeling stage as independent variables (PROC GLM; SAS, 1985). The extent of carbon movement from the leaves was measured in several ways: the %TA retained in the axillary branch of the labeled leaf and not exported to other parts of the plant; the RSA of this axillary branch; and the %TA and RSA of the branches and leaves at each node as a function of distance from the labeled node. The first two measures were analyzed by ANOVA. Activity by node was used only to visualize the extent of carbon movement as an aid in interpreting the other results.

Repeated-measures ANOVA was used to characterize sectoriality, with orthostichy as the within-subject repeated measure and source leaf and stage at labeling as the independent variables. When leaves were analyzed, the labeled leaf was excluded from the total activity of the labeled orthostichy to prevent it from inflating the activity of its orthostichy. Both %TA and RSA were log transformed to equalize variances.

	RESULTS

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The plants in this study were both highly integrated for carbohydrates and markedly sectorial. The stage at which a plant was labeled and the location of the source leaf affected both the direction and extent of resource movement and the degree of sectoriality.

Extent of movement
The extent of carbohydrate translocation from leaves was measured as the amount of activity used locally—in the labeled leaf's axillary branch—and not exported to branches at other nodes. In both the early and mature harvests, leaf position and labeling stage affected activity at the labeled node, as measured by %TA (early harvest: leaf P = 0.0002, developmental stage P = 0.02; mature harvest: both leaf and developmental stage P < 0.0001) and relative specific activity (early harvest: leaf P < 0.0001, developmental stage P = 0.01; mature harvest: leaf P = 0.002, developmental stage P = 0.03) (Fig. 2). Plants were least extensively integrated at the late reproductive stage during seed fill (Tukey's studentized range test, P < 0.05). Plants labeled at leaf 6 retained the highest proportion of assimilate (%TA) in the axillary branch of the labeled leaf (dark grey bars in Fig. 6), whereas the axillary branch of the labeled leaf had the most activity for its size (RSA) in plants labeled at leaf 9 (Tukey's studentized range test, P < 0.05) (Fig. 2).

View larger version (36K): [in this window] [in a new window]   Fig. 2. Mean relative specific activity (RSA) ± 1 SE retained in the axillary branch of the labeled leaf for both the early and the mature harvest. Bars are grouped by the position of the labeled leaf. Note that within each group, RSA generally increases as plants are labeled later in development. Percentage total activity (%TA) retained in the labeled branch is shown as part of Fig. 6 (dark grey bars).

View larger version (90K): [in this window] [in a new window]   Fig. 6. Mean percentage of the total activity found in leaves (slants), branches (greys), stems (waves), and terminal inflorescences (solid black) for each harvest. Labeled leaves (right-leaning slants) are distinguished from all other leaves (left-leaning slants), and branches at the labeled node (dark grey) are distinguished from all other branches (light grey). Horizontal bars are grouped by labeling stage: V1 and V2 are early and late vegetative stages, respectively; R1 and R2 are early and late reproductive stages. The position of the labeled leaf is indicated to the left of each horizontal bar.

View larger version (25K): [in this window] [in a new window]   Fig. 3. Mean activity ± 1 SE of branches at each node within the labeled orthostichy for each labeling stage and leaf position. V1 and V2 are early and late vegetative stages, respectively; R1 and R2 are early and late reproductive stages. Lines are grouped by labeled leaf position. Graphs (a) and (b) show % total activity, and (c) and (d) show RSA of early- and late-harvest plants, respectively. The inset in Fig. 3c provides a magnified view of the right side of the graph. Note that the y -axis scale differs between the early- and late-harvest plants. In Fig. 3c and d , "T" indicates terminal inflorescence.

Sectoriality
Carbohydrate movement was highly sectorial (Fig. 4), however the degree of sectoriality varied significantly with labeling stage and the position of the labeled leaf (Table 1). Sectoriality of translocation to leaves declined between the first and second vegetative stages and was not evident during the reproductive stages, when no new leaves were being produced (Fig. 4, Table 1). By contrast, allocation to branches was most highly sectorial when plants were labeled late in development (Fig. 4). This increase in sectoriality was driven by an increase in the RSA of the labeled orthostichies, coupled with no significant change in the RSA of the adjacent and opposite orthostichies (ANOVA). The increase in RSA of the labeled orthostichy was not an artifact of increased activity solely at the labeled node. Instead, the enhanced concentration of activity occurred over several nodes in the labeled orthostichy (Fig. 3). In the mature-harvest plants, the variation in RSA among orthostichies was significantly greater among plants labeled at leaf 9 or leaf 6 compared to those labeled at leaf 3 (ANOVA, P = 0.003), indicating that resource movement was significantly more sectorial from these two leaves.

View larger version (31K): [in this window] [in a new window]   Fig. 4. Sectoriality of carbohydrate movement: mean RSA ± 1 SE of early-harvest leaves and branches and mature-harvest branches by orthostichy for each treatment combination. Black bars = labeled, grey bars = adjacent, and stippled bars = opposite orthostichies.

View larger version (31K): [in this window] [in a new window]   Fig. 5. Mean RSA ± 1 SE of stems for each harvest. Bars are grouped by labeling stage, as indicated above the bars. The position of the labeled leaf is given below each bar.

Allocation to roots was not examined in this experiment because roots had begun to disintegrate before plants were harvested and they could not be recovered completely. In another labeling experiment on Perilla, translocation to roots was greatest during vegetative growth, and leaf 3 supplied the most assimilate to roots (Preston, 1997, p. 108). If allocation to roots was similar in this study, then excluding the roots probably inflated the activity measured in the shoots of plants labeled at node 3 or during vegetative growth. Given that those were the plants with the lowest activity (Figs. 1–3), including roots in this study would not have changed the results and may even have accentuated the observed decline in integration during development.

	DISCUSSION

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Knowledge about integration and sectoriality of carbon translocation patterns can be used to predict plant responses to ecological interactions such as herbivory or competition (e.g., Marquis, 1992; Rosenthal and Welter, 1995). In this context, however, it is important to remember that translocation patterns are not necessarily static (Watson and Casper, 1984), and that the patterns observed at one point in development may not reflect translocation patterns at the time that herbivory or competition is most intense (Marquis, 1996). This experiment showed that both integration and sectoriality change throughout development and that each labeled leaf played a particular role in supporting plant growth.

Effects of developmental stage on translocation
Spatial patterns of carbohydrate movement in the shoot changed throughout development (Fig. 6). When plants were labeled early in vegetative growth, carbohydrates generally moved from the source leaves to newly developing leaves. When plants were labeled during the second reproductive stage, translocation was shifted to branches, where reproductive structures were being produced. As a result, patterns of translocation varied throughout development, driven by the spatial distribution of growing tissue at each labeling stage.

Temporal variation was evident not only in spatial patterns but also in the degree of integration; the amount of assimilate used locally, rather than exported to other nodes, varied between stages (Fig. 2). Most notably, plants were least integrated during the second reproductive stage when the inflorescences terminating each branch were maturing seeds. The distribution of label to each node confirms this shift towards reduced integration with the onset of reproduction (Fig. 3). Degree of sectoriality also varied with developmental stage (Fig. 4). Sectorial translocation to leaves declined with development, and allocation to branches became increasingly sectorial. Increasing sectoriality coincided with flowering and fruiting of the branch apices, and presumably was associated with increasing local demand for resources by these developing structures. Thus, the distribution of growing tissue over the plant body influenced not only where labeled assimilates went, but also how far. When local demand was high, resource use became highly localized, and translocation between nodes and orthostichies was reduced.

At first glance, the pattern of allocation to stems appears to contradict the trend of carbohydrate movement to actively growing tissue (Fig. 5). In the early harvest, labeled assimilate moved into stems at all labeling stages, including the reproductive stages when stem growth should have been reduced. The mature harvest showed, however, that carbohydrates translocated to the stems during seed fill did not stay in the stems. The fate of this "lost" assimilate cannot be determined from these data. It is possible that the stems respired at an unusually high rate at the second reproductive stage, releasing C into the atmosphere. It seems more likely, however, that stems accumulated assimilates for short-term storage, as happens in some annuals (Chiariello and Roughgarden, 1984; Chapin, Schulze, and Mooney, 1990). This carbon might then have been remobilized to support seed fill, which would be most consistent with the patterns observed elsewhere in the plant. The roots, which were not measured in this experiment, may also have served as temporary storage (Preston, 1997)

The results of this experiment are similar to those of Lacey and Marshall (1992) who found that during fruiting, integration in Plantago virginica was reduced and the amount of assimilate retained at the labeled node doubled. Up until seed fill, however, carbohydrate translocation in Perilla was extensive within the labeled orthostichy. This result contrasts with studies that have found little integration in annuals (Singh and Pandey, 1980; Marshall, 1989; Kemball, Palmer, and Marshall, 1992; Horton and Lacey, 1994). For example, in Galium aparine, a shaded branch was not supported by leaves from the main stem (Kemball, Palmer, and Marshall, 1992), whereas in Perilla, even unshaded branches with mature leaves imported carbon from leaves on the main stem. Marshall (1996) has suggested that annual plants are typically subdivided into small separate physiological subunits (IPUs), but my results indicate that some annual plants are indeed well integrated.

Variation in degree of integration is found also among clonal perennial species, and this variation has allowed ecologists to look for the conditions that favor integration and those that favor module (ramet) independence (e.g., Pitelka and Ashmun, 1985; de Kroon and van Groenendael, 1990; Caraco and Kelly, 1991; Jónsdóttir and Watson, 1997). Current theories about the adaptive value of integration in clonal plants cannot be applied appropriately to annuals, however, because annuals and perennials differ in their allocation to different life-history functions (Harper, 1977). For example, the benefits of integration to establishing new vegetative offspring (Caraco and Kelly, 1991) or maintaining storage structures and meristems between seasons (Landa et al., 1991) do not pertain to annual plants.

Therefore, an ecological theory of integration in annual plants must explore factors that affect resource deployment in annuals. For example, annuals do not maintain storage tissue between seasons, but some do store resources within a season (Chiariello and Roughgarden, 1984; Chapin, Schulze, and Mooney, 1990), and translocation of stored carbohydrates to flowering branches would require some integration. Results from this experiment suggest that Perilla uses stem tissue as temporary storage in this way. Another trait involving resource use in annuals is the timing of reproduction relative to vegetative growth. Species that show multiple switches (King and Roughgarden, 1982a) or a graded transition (King and Roughgarden, 1982b) to reproductive growth might require a different degree of integration than determinate annuals like Perilla, which make a single switch to reproduction.

Although plants in this experiment were well integrated, carbohydrate movement was largely confined to one orthostichy. This result is consistent with many other studies reporting sectoriality in annual species (Prokofyev, Zhdanova, and Sobelev, 1957; Shiroya et al., 1961; Singh and Pandey, 1980; Zeevaart, 1985; Benner, Fitzpatrick, and Watson, 1989; Garrish and Lee, 1989; Shea and Watson, 1989; and Ho, 1996). Much of the ecological interest in sectoriality has been focused on stress-induced changes in sectoriality; this experiment showed, however, that extreme artificial manipulations are not always necessary to alter sectorial patterns. In Perilla, sectoriality changed along with the normal shifts in carbohydrate demand that accompany seed production.

Effects of source leaf on translocation
In this experiment, each labeled leaf played a particular role in the carbon economy of the plant. Harper (1989) has argued that one leaf's contribution to the growth of a plant goes beyond the amount of carbon it assimilates in its lifetime. A leaf increases the photosynthetic capacity of an entire plant by supporting the growth of new leaves. Chapin, Schulze, and Mooney (1990) term this "compounding the interest." The value of a leaf declines with age, partly because its photosynthetic capacity declines, but also because fewer future leaves depend on it (Harper, 1989).

The results of the present experiment demonstrate that the value of a leaf is influenced not only by its age, but also by its position on the plant. At all four labeling stages, leaves differed in the number and location of the leaves that they supplied and thus were not equal in the contribution they made to future carbon gain. To illustrate this point, it is useful to compare the translocation patterns of leaves 3 and 6 (Fig. 3b, d). In plants labeled at the first reproductive stage, leaf 3 supplied assimilates to the uppermost branches, but leaf 6 primarily supported its own axillary branch rather than the upper branches. Similarly, more assimilates were translocated beyond the labeled orthostichy when they originated from leaf 3 than from leaf 6 (Fig. 4). Thus, leaf 3 likely enhanced the total carbon gain of the plant more than leaf 6 did, by supporting the growth of a larger number of branches. Leaf 3 also appeared to contribute more than leaf 6 to the ultimate reproductive capacity of the plant because each branch it supported carried meristems capable of giving rise to inflorescences.

Given that both sectoriality and integration changed over the growing season and with the location of the source leaf, it is likely that the consequences of losing a leaf to herbivory or other damage also would depend on timing and location. For example, if plants in this experiment had been damaged, they might have suffered severe but localized losses from damage to leaf 6 and more diffuse effects from damage to leaf 3. It is possible that translocation patterns would be altered when Perilla was defoliated, mitigating these losses, but there may be metabolic costs associated with translocation across orthostichies, or a fitness cost to those undamaged orthostichies or branches from which resources were diverted. Any such costs should depend on the normal degree of integration and sectoriality at the time of defoliation and would thus also be sensitive to the timing and location of defoliation.

	FOOTNOTES

 
¹ The author thanks M. A. Watson, R. L. Anderson, K. Clay, L. Delph, C. Lively, C. Marshall, and Robert Turgeon for helpful criticism of the manuscript, M. Hutchings for useful comments on an early draft, J. Lemon for customizing the greenhouse bench for this experiment, all of the Indiana University greenhouse staff for care of the plants, and H. A. Mooney and D. D. Ackerly for generously providing space and a supportive atmosphere in which to complete the manuscript. This work was supported by a grant from the Indiana Academy of Sciences and by the Indiana University Department of Biology.

² Current address: Department of Biological Sciences, Stanford University, Stanford, CA 94305 (e-mail:kap1{at}leland.stanford.edu ).

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