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Structure and Development |
2Department of Horticulture, Estación Experimental La Mayora (CSIC), Algarrobo-Costa 29750, Malaga, Spain; 3Department of Plant Breeding, Cornell University, Ithaca, New York 14853 USA; 4Department of Biological and Environmental Engineering, Cornell University, Ithaca, New York 14853 USA; 5Department of Plant Biology, Cornell University, Ithaca, New York 14853 USA
Received for publication August 14, 2003. Accepted for publication October 7, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: cellulose microfibrils • epidermis • fruit cracking • plant biomechanics • Solanaceae • strain-hardening • tomato fruit
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Following the terminology of Wattendorf and Holloway (1980)
, Holloway (1982)
, and Jeffree (1996)
, it typically consists of an external layer of epicuticular waxes (ECW) overlying a comparatively thin layer of saponifiable lipids (the cuticle proper, CP) that covers an inner layer of waxes and fibrous polysaccharides embedded in a cutin matrix (the cuticular layer, CL). The CP and CL comprise the cuticular membrane (CM), which sensu stricto develops within cell walls (Esau, 1977
). The structure of the CM and the extent to which it extends beneath the epidermis vary among and sometimes within species (Jeffree, 1996
). For example, although it is frequently confined to the outer periclinal and anticlinal walls of the epidermis, the CM may develop in subepidermal cell walls (Fig. 1). Significant ultrastructural and chemical differences in the CM also exist across and within species (see Kolattukudy, 1980
, 1996
; Jeffree, 1996
; Wiedemann and Neinhuis, 1998
).
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; Schönherr, 1982
; Eller, 1985
; Riederer, 1990
; Juniper, 1991
; Riederer and Schreiber, 2001
). Likewise, chemical and anatomical differences may affect the mechanical function of the CM (see Petracek and Bukovac, 1995
; Wiedemann and Neinhuis, 1998
). Nevertheless, because the walls of the epidermis and adjoining cells are placed in tension when primary organs are turgid (Kutschera, 1989
; Niklas and Paolillo, 1997
, 1998
), the CM can function as a tensile "skin" depending on its thickness and material properties. In this paper, we report the tensile properties and anatomy of peels from the fruits of two Lycopersicon esculentum cultivars, which differ in their susceptibility to cracking, i.e., the crack-resistant Inbred 10 and the crack-prone Sweet 100. We also report the mechanical properties and anatomy of their cellulase/pectinase-isolated CM. Our objective is to determine the extent to which the CM contributes to the ability of fruit walls to resist tensile failure. Because the outer fruit wall is composed of different anatomical constituents, some of which could not be isolated and tested individually (subcuticular cell layers), the volume fractions of various peel constituents were used to determine their relative mechanical contributions.
Based on this study, we propose a simple rheological model for the tomato fruit wall that attributes strain-hardening to the passive realignment of fibrils in the CM and its associated cell walls. This model is discussed in the context of the mechanical and anatomical features of Inbred 10 and Sweet 100 fruits and their susceptibility to cracking when ripe.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Sample preparation
Rectangular paradermal segments of the outer fruit wall (aligned either longitudinally or equatorially with respect to the pedicle–style fruit axis) were removed using two parallel razor blades bonded to a metal block to assure uniform segment width (5.25 mm) and depth of cut (230 ± 35 µm). Segment length varied due to differences in fruit size and shape. The outer fruit wall was peeled off by hand, placed in a petri dish subepidermal side downward on filter paper, and hydrated with the liquid and soft pulp of the fruit from which it was removed to reduce desiccation, maintain tissue osmolarity, and prevent direct wetting of the CM. A small portion of the outer fruit wall next to each peel was also removed and preserved in FAA for anatomical study. Microscopic measurements of peel and CM thickness were used to determine the cross sectional areas of samples tested mechanically (see Mechanical tests).
Duplicate peels were removed from each fruit for enzyme treatment following the protocol of Orgell (1955)
as modified by Yamada et al. (1964
; see Petracek and Bukovac, 1995
). Excised samples were suspended in a fungal origin mixture of cellulase and pectinase (0.2% m/v and 2.0% m/v, respectively; Sigma) and 1 mmol/L NaN3 (to prevent microbial growth) in sodium citrate buffer (50 mmol/L, pH 4.0). Suspensions were aspirated to aid enzyme penetration before incubation at 35°C for 7–10 d (during which suspensions were agitated by hand daily). Samples were then rinsed in citrate buffer and inspected microscopically before testing.
Mechanical tests
Peels and their enzyme-isolated CM were mounted for tests using two small metal rods suspended by stirrups between the cross heads of a model 4502 Instron testing machine (Fig. 2). A dab of fast-drying super glue was spread over the middle of each rod and the external surface of the ends of each sample, which were then folded over each of the two rods before aligning the stirrups parallel to the Instron cross-head axis. Samples were continuously hydrated during each test with the liquid extracted from their corresponding fruits by means of a micropipette applied to their subepidermal surface. A small piece of hydrated tissue paper was placed on this surface to maximize uniform hydration and further reduce desiccation during testing. Unless otherwise noted, a 2.0 mm/s strain rate (i.e., cross-head displacement rate) was used in loading-unloading and uniaxial tension tests. This high rate of extension was used to mimic rapid fruit swelling due to diurnal water influx. In this context, preliminary tests using slower strain rates (e.g., 0.2 mm/s) gave results that were qualitatively indistinguishable from those reported here.
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Three general types of mechanical tests were performed: (1) transient creep tests to determine the rate of creep and the instantaneous elastic strain upon loading, (2) successive loading-unloading (cyclical) tests to determine the sum of plastic strains resulting from repeated applications of varying tensile forces (strain history) and the affects of repeated load applications on the Young's modulus of a sample (strain-hardening or -softening), and (3) uniaxial tension tests to determine breaking stress, breaking strain, and the work of fracture. Because no sample could be tested each way, the data from all three tests were juxtaposed to determine the mechanical properties of peels and their isolated CM. The protocols for each of the three types of tests were as follows.
Secondary (transient) rates of creep and instantaneous elastic strains were determined by sustaining samples in uniaxial tension under a constant load for 
20 min during which the longitudinal extension of each sample was recorded every 2 s. The rate of creep was determined from the slope of the log-log linear regression curve of strain vs. time for the secondary phase of creep (Fig. 3A). The instantaneous elastic strain was taken as the strain recorded 4 s after the application of each tensile load. Each peel was tested repeatedly using either an ascending sequence of sustained tensile forces (from 0.10 N to 0.65 N in 0.05 N load increments) or a descending sequence (from 0.65 N to 0.10 N with 0.10 N load increments between 0.60 N and 0.10 N).
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Successive loading-unloading (cyclical) tests were used to determine the effects of prior mechanical loadings on sample stiffness and the sum of plastic strains. Each peel was increasingly extended (using an increasing sequence of forces from 0.10 N to 0.65 N in 0.05 N increments) and allowed to relax before reloading (Fig. 3B–C). Equivalent stress forces Pe exerted on peels were used for loading-unloading tests of corresponding enzyme-treated samples. Stresses and strains were continuously monitored during each loading cycle every 0.5 s. Plastic deformations were recorded at the end of each loading cycle; sample stiffness (Young's modulus E) was determined from the slope of the linear portion of the stress 
vs. strain 
plot after compensating for the plastic strains in each previous loading cycle, i.e., E = 
/.
Uniaxial tensile tests to failure were performed using the aforementioned protocol. The maximum stress b and strain b were recorded as the breaking stress and the breaking strain, respectively. These tests were also used to determine the work of fracture W (the energy per unit cross section required to propagate a crack) by making a small cut of specified length 
on one edge of a sample before testing. The Young's modulus E and the breaking stress of each sample were then used to compute W using the formula W = 
2b/2E (see Kraemer and Chapman, 1991
; Niklas, 1992a
; Anderson, 1995
). The dimension of was established for each cultivar from preliminary notch-sensitivity analyses (data not shown).
Anatomical protocols
Materials were washed in 50% ethanol, rehydrated, and sectioned at a thickness of 10 µm, frozen in water, and using a cryostat. The sections were observed unstained or stained in zinc-chlor-iodine for detection of cellulosic walls (Peacock, 1966
). Unstained sections were also observed between crossed polarizers, with and without the insertion of a rose plate, which develops a color image that allows for the determination of the net orientation of unstained cellulose wall microfibrils (Bennett, 1950
). Stained sections were also examined using a single polarizing filter beneath the specimen and a rotating stage to detect dichroism, which allows the determination of the net orientation of stained cellulose wall fibrils (Roelofsen, 1959
). Photographs were obtained using an image capture program under the control of a microcomputer.
Statistical analyses
All analyses were performed using the JMP software package (SAS Institute, Cary, North Carolina, USA). The mean values for reported mechanical properties are based on 10 samples (one from 10 different fruits) from a minimum of four different plants (n = 10 peels or CM; n 4 plants). With the exception of the data from tensile tests to failure (see below), ordinary least squares regression and correlation analyses were performed based on 12 means (one for each tensile force used in either a creep or a loading-unloading test). Statistical differences in the slopes of regression curves were determined on the basis of the 95% confidence intervals of slopes; regression curve fits were rejected if P > 0.0001. All pair-wise comparisons (Tukey-Kramer HSD; 
= 0.05) among means of E, b, or W were used to determine whether these properties differed between the cultivars (n = 4 means, one mean for the fruits produced by each of four plants).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Mechanical properties of peels
The rate of creep decreased when peels were tested with progressively larger tensile forces (Fig. 4A). With a 0.1-N force, the rate of creep for Sweet 100 peels was, on average, 40% faster than that of Inbred 10 (i.e., 0.106 s–1 and 0.076 s–1, respectively). However, with progressively larger forces, all pair-wise comparisons of mean values (n = 4) indicated that the difference in the rate of creep between the peels from the two cultivars deceased and became statistically indistinguishable for forces 0.20 N. Likewise, when peels were initially loaded with 0.60 N, the rate of creep for the two cultivars differed significantly (based on all pair-wise comparisons of means), decreased sharply for 0.60 N, and remained approximately unchanged for progressively smaller tensile forces (Fig. 4B).
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b, and W (Fig. 6C). The E of Inbred 10 was, on average, 20% larger than that of Sweet 100 peels (i.e., 43.5 ± 4.83 MPa and 27.1 ± 1.93 MPa, respectively), whereas the b of Inbred 10 peels was, on average, 15% greater than that of Sweet 100 (i.e., 1.16 ± 0.105 MPa and 0.97 ± 0.052 MPa, respectively). The average W for Inbred 10 and Sweet 100 peels was 154.7 ± 12.7 J/m2 and 127.8 ± 16.6 J/m2, respectively. The average b of Inbred 10 was significantly larger than that of Sweet 100 (i.e., 0.17 ± 0.02 and 0.10 ± 0.02, respectively). Therefore, before failing in tension, Inbred 10 peels sustained, on average, significantly larger tensile forces and deformed more compared to Sweet 100. Inbred 10 peels also required, on average, almost 65% more energy per unit area to tear than Sweet 100 walls.
Mechanical properties of isolated CM
With increasing equivalent tensile forces Pe, the rate of creep decreased log-log linearly for both cultivars (Fig. 4C). The rate of creep of Inbred 10 CM was significantly slower than that of Sweet 100 CM. All pair-wise comparisons between the rates of creep observed for peels and their corresponding CM indicated no significant statistical differences. Creep tests using descending equivalent tensile forces indicated that the CM of both cultivars strain-hardened (data not shown), which was corroborated by sequential loading-unloading tests.
A strong linear relationship was observed between the magnitudes of instantaneous elastic strains and applied equivalent tensile forces; these strains increased more rapidly for Inbred 10 CM compared to Sweet 100 CM (Fig. 5C). Plastic strains accumulated less rapidly for Inbred 10 CM than for Sweet 100 (Fig. 5D), i.e., the total strains and the plastic (permanent) component of these strains observed for Sweet 100 CM exceeded those of Inbred 10.
Sequential loading-unloading tests indicated that the CM of both cultivars strain-hardens initially. The average E of Inbred 10 CM exceeded that of Sweet 100 CM for each loading-unloading cycle and the difference between the two increased with each successive cycle. Visual inspection and regression analyses of mean E vs. Pe indicated that the degree of strain-softening was more pronounced for Sweet 100 CM compared to Inbred 10 CM (Fig. 6B).
Tensile tests to failure showed that Inbred 10 CM is stiffer and has a higher work of fracture (but an equivalent breaking stress) compared to Sweet 100 CM (Fig. 6D). Specifically, the E of Inbred 10 and Sweet 100 CM was 70.3 ± 2.95 MPa and 51.3 ± 4.83 MPa, respectively; the W of Inbred 10 and Sweet 100 CM was 95.4 ± 10.4 J/m2 and 70.9 ± 7.09 J/m2, respectively. Thus, the CM stiffens the fruit walls of both cultivars, subepidermal cells increase the work of fracture, and Inbred 10 CM is substantially stiffer and more energy "absorbent" than Sweet 100 CM.
Peel and CM anatomy
The peels of both Inbred 10 and Sweet 100 consisted of a cuticularized surface layer underlain by collenchyma. Figures 7 and 8 represent peels from the two cultivars at the same magnification, showing a marked difference between cultivars in peel thickness and in thickness of the cuticularized outer periclinal epidermal wall. In addition, the cuticularized anticlinal walls of the Sweet 100 epidermis appeared in sectional view as "pegs" that were only tenuously attached to relatively thin, cuticularized inner periclinal epidermal walls (Fig. 8). In Inbred 10, the cuticle extended 2–3 cell layers into the interior (Fig. 7), thereby involving hypodermal cell walls. (A similar arrangement is illustrated by Petracek and Bukovac [1995]
for tomato variety Pik Red, and for certain other tomato varieties by Chu and Thompson [1972]
.) The interior cuticularized periclinal walls of Inbred 10 cuticle were all thicker than the cuticularized inner periclinal epidermal walls found in Sweet 100. The cuticularized anticlinal walls of the epidermis in Inbred 10 had broad attachments to the inner cuticularized periclinal walls of the epidermis and even into the hypodermal cell layers (Fig. 7).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). To the best of our knowledge, no prior study of the tomato fruit has examined the mechanical and anatomical relationships between the isolated CM and intact samples of the outer fruit wall, nor has any other study employed the spectrum of mechanical tests used here to quantify the mechanical behavior of these structures. Our tests indicate that the outer fruit wall and the CM of Inbred 10 and Sweet 100 cherry tomatoes are isotropic, viscoelastic, and, to different degrees, strain-hardening structures. The rheological behavior of the outer fruit walls of both cultivars mirrors that of their CM, which serves as a "tensile skin" whose mechanical properties and behavior are highly correlated with thickness.
The rheological behavior of the CM and the magnitudes of its mechanical properties we report are consistent with previous studies. For example, Wiedemann and Neinhuis (1998
: table 1) show that the Young's modulus and breaking stress of hydrated tomato CM are on the order of 60 MPa and 2 MPa, respectively. Likewise, the viscoelasticity of the CM has been observed previously, whereas inspection of the data graphed by Thompson (2001
: e.g., fig. 3) from sequential loading-unloading cycle tests indicates that the CM rate of creep decreases with successive cycles, which is consistent with strain-hardening. Finally, Petracek and Bukovac (1995)
, who also show that the CM is viscoelastic, report as we do that elastic strains typically exceed plastic strains when the hydrated CM is modestly extended. Thus, a general mechanical phenomenology can be adduced for the tomato CM, although significant variation exists regarding the manifestation of this phenomenology and the absolute magnitudes of material properties (see Fig. 6).
That the mechanical properties of the CM mirror in large part those of the fruit wall peels is not surprising. The average CM work of fracture for both cultivars is comparable to that of polyesters and some epoxy resins (i.e., W 
100 J/m2; see Gordon, 1978
). Because the peripheral cells of a hydrostatically inflated organ sustain the largest tensile stresses (see Kutschera, 1989
; Niklas and Paolillo, 1997
, 1998
), the CM is ideally positioned to cope with mechanical stresses. However, our data indicate that the mechanical role of subepidermal tissues cannot be neglected, principally because a material's work of fracture is inversely proportional to its Young's modulus. Thus, if the fruit subepidermal cells have a lower E than the CM, they are capable of "absorbing" strain energy such that significantly more energy is required to propagate a crack through the fruit wall than through its isolated CM. The effect of the tomato fruit subepidermis is evident from comparisons of the W between the isolated CM and peels.
Unfortunately, the subepidermis E of tomato fruits can only be inferred, because we were unable to enzymatically isolate this tissue for mechanical tests. However, a Voigt-model (see Niklas, 1992b
) indicates that this tissue has an E on the order of 24 MPa, which is significantly less than that of the CM of either cultivar. This model assumes that the Young's modulus of the outer fruit wall EOFW equals the CM Young's modulus ECM (times the decimal volume fraction fCM of the CM) plus the Young's modulus of the subepidermis ESC (times its decimal fraction fSC contribution), i.e., EOFW = ECMfCM + ESCfSC. For Sweet 100 peels, on average, EOFW = 27.1 MPa, ECM = 51.3 MPa, and fCM = 0.20 such that fSC = 0.80 for which the Voigt model gives ESC = 21.5 MPa. For Inbred 10, on average, EOFW = 43.5 MPa, ECM = 70.3 MPa, and fCM = 0.25 such that fSC = 0.75 and ESC = 25.9 MPa. The range of values predicted by this model (i.e., 21 MPa and 26 MPa) is numerically consistent with the E reported for collenchyma from Apium graveolens and Levisticum officinale leaves, i.e., 22 MPa (data from Esau [1936]
and Ambronn [1881]
, respectively; see Niklas, 1992a
).
The physical attachment of the CM to collenchyma suggests that strain incompatibility may occur when peels are extended beyond the CM breaking strain, i.e., the bilaminate structure of the outer fruit wall may debond. This phenomenon was observed during some of our tensile tests to failure. Micro-cracks developed on the CM surface and the collenchymatous subepidermis increasingly supported the applied mechanical loads. This strain incompatibility, which was far more pronounced for Sweet 100 than for Inbred 10 peels, is likely biologically important. If a fruit imbibes water and expands rapidly, its CM may experience tensile forces that exceed its capacity to extend elastically, producing micro-failures that expose underlying cells to dehydration.
This scenario may explain why the fruits of Sweet 100 crack when attached to plants, whereas those of Inbred 10 do not. Nevertheless, equally plausible (and nonexclusive) scenarios for cracking exist. For example, the CM of Sweet 100 ultimately strain-softens when extended and relaxed repeatedly (see Fig. 6C). Mechanical "fatigue" may cause a fruit wall to rupture during repeated diurnal cycles of fruit expansion-contraction. In contrast, the CM of Inbred 10 continues to strain-harden during equivalent loading-unloading cycles, thereby increasing its capacity to sustain larger tensile forces. Likewise, the large plastic strains exhibited by Sweet 100 CM may result in rapid dehydration of the underlying subepidermis due to the thinning of the CM. If the inner fruit volume is conserved, the outer portions of the fruit will shrink and crack.
We believe that strain-hardening and strain-softening reflects the response of microfibrils in the CM to tensile forces. Prior work indicates that fibrillar components in cell walls can progressively align in the direction of applied tensile forces such that the effective Young's modulus increases (see Köhler and Spatz, 2002
). However, when excessively extended, the fibrils may slip past one another (as their matrix deforms) and the Young's modulus decreases. Although speculative, this phenomenology suggests a simple rheological model for the behavior of the tomato CM—one that accounts for the relative abundance of CM fibrils as well as the anatomical differences between Inbred 10 and Sweet 100 fruit (Fig. 12).
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Importantly, the epidermis of a hydrostatically inflated spherical fruit wall experiences equivalent orthogonal biaxial tensile forces (see Henry and Allen, 1974
; Haman and Burgess, 1986
) such that strain-hardening is unlikely to occur if fibrils are randomly oriented. However, basic engineering theory indicates that any departure from a spherical geometry or any bias in the net orientation of CM fibrillar components will produce some degree of strain-hardening. For example, an internally pressurized prolate geometry will experience circumferential tensile stresses that are larger than their corresponding longitudinal stresses (see Gordon, 1978
; Niklas, 1992a
). Even if the fibrils in its outer "tensile skin" are randomly oriented, such a geometry is predicted to rupture longitudinally when excessively pressurized from within. In this regard, Sweet 100 fruits are prolate and they invariably crack longitudinally.
In summary, our data indicate that a strong positive relationship exists between the anatomy of the tomato outer fruit wall (particularly CM thickness) and its mechanical properties (e.g., stiffness and work of fracture). But it is premature to suggest that any particular suite of anatomical features provides a reliably consistent qualitative diagnostic for the rheology of the tomato fruit wall because the fruit wall and its CM have a complex cellular and subcellular infrastructure (and chemistry) that cannot be canonically characterized across all species or even across the cultivars of a single species (see Hankinson and Rao, 1979
; Jeffree, 1996
; Kolattukudy, 1996
; Wiedemann and Neinhuis, 1998). It is nevertheless clear that the mechanical behavior of the CM is intimately linked to anatomy and that the CM is a biologically important component of the primary plant body for mechanical as well as physiological reasons.
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FOOTNOTES |
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6 kjn2{at}cornell.edu
; Phone: 607-255-8727; FAX: 607-255-5407
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Anderson T. L. 1995 Fracture mechanics—fundamentals and applications. CRC Press, Boca Raton, Florida, USA
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