IAWA Journal, Vol. 31 (2), 2010: 203–216

OCCURRENCE OF REACTION XYLEM IN THE OF GUIANENSIS AND PINNATA

Pramod Sivan, Preeti Mishra and K. S. Rao* BR Doshi School of Biosciences, Sardar Patel University, Vallabh Vidyanagar 388 120, Gujarat, *Corresponding author [E-mail: [email protected]]

SUMMARY The anatomy of the secondary xylem and distribution pattern of gelati- nous fibres (G-fibres) have been studied in the developing and heavy bearing mature peduncles of Kigelia pinnata and Couroupita guianensis. The peduncle in both the developed reaction xylem as a result of growth stresses caused by development of large . In Couroupita peduncles which are originally horizontal, G-fibre distribution was uni- lateral and similar to that of typical tension wood whereas the hanging Kigelia peduncles have uniformly distributed gelatinous fibres throughout the xylem. The tension xylem severity was higher in the basal region and decreased towards the terminal region of the current year’s peduncle but after fruit development a drastic increase in tension wood severity was observed in the terminal region. In the Kigelia peduncles, tension wood severity in terms of G-layer proportion to lignified wall was found to be less than in Couroupita. The abundance of vessels decreased with high frequency of gelatinous fibres inCouroupita . The peduncle of Kigelia is characterized by high vessel frequency, thin normal fibre walls, and thick outer walls with thin gelatinous layer in tension wood fibres. Dimensional variations were also noticed in the mechanical and conducting elements varying with tension wood severity. Key words: Reaction xylem, peduncle, Kigelia pinnata, Couroupita guia- nensis, G-fibres.

Introduction

Tree stems maintain their orientation (vertical for trunks, oblique for branches) by gen- erating asymmetrical (from one side of the stem to the other) stresses in wood, during cell wall maturation, i.e. formation of secondary cell wall and lignification (Archer 1986; Fournier et al. 1994). Angiosperms generate stronger tension stresses on the upper side of stem (Wardrop 1964; Fisher & Stevenson 1981) leading to the formation of tension wood on the upper part of leaning or bending branches. The most distinguishing feature of tension wood is the occurrence of fibres with a particular morphology and chemi- cal composition due to the development of so-called gelatinous layer or the G-layer (Evert 2006). This layer is essentially made up of strongly crystalline cellulose (Côté et al. 1969), with a very low microfibril angle (Chaffey 2000). G-fibres are commonly found on the upper side of the leaning stems and branches. In species where tension wood exhibits a typical G-layer, its occurrence is always correlated with high tensile

Downloaded from Brill.com09/30/2021 01:04:16AM via free access 204 IAWA Journal, Vol. 31 (2), 2010 growth stress. (Clair et al. 2003; Washusen et al. 2003). On the other hand, tension wood may also develop in stems free from any bending stress (Berlyn 1961). The occur- rence of tension wood has been studied widely in stems, branches and of many dicots (Patel 1964; Fisher & Stevenson 1981) and in non vascular tissues of monocot leaves (Staff 1974). However, the information available on tension wood formation in the peduncles ( or fruit stalks) of tropical is meagre. The present work, therefore, was undertaken to study the distribution of tension wood in peduncles of two fruit bearing tropical species, Couroupita guianensis and Kigelia pinnata. In the former peduncles grow horizontally from the surface of the main stem, while in the latter peduncles hang vertically downward from the tips of branches, exhibiting positive gravitropism.

Materials and Methods materials Peduncles showing different developmental stages were collected from the trees of Kigelia and Couroupita growing at the University Botanical garden, Sardar Patel University, Gujarat, India. Peduncles representing three developmental stages of Couroupita, i.e.: from young , from mature without, and with heavy fruit (c. 1 kg), and two developmental stages of Kigelia, i.e.: from young inflorescences, and from mature inflorescences with heavy fruit (2–5 kg) were selected. For each developmental stage, three peduncles were collected from each of the species. Samples were collected from basal, middle and terminal regions of each peduncle. Samples were also collected from current year’s and one year old branches with di- ameters similar to those of peduncles, and growing at an angle of about 60° from each tree trunk. All material was fixed along in FAA (Berlyn & Miksche 1976).

Light microscopy Transverse sections of 8–10 μm thick were cut on a sliding microtome (Leica SM 2000R) and stained overnight in safranine O and counter-stained with fast green FCF (Berlyn & Miksche 1976). G- fibres in the reaction xylem of peduncles were identified by their red-stained lignified walls and green-stained gelatinous layer. After dehydration in ethanol-xylene series the sections were mounted in DPX. Tension wood severity at different regions of the peduncle was determined according to Washusen and Evans (2001). The proportion of gelatinous wall area to lignified wall area in transverse section was measured with an ocular micrometer. Thickness of the normal fibre walls was also measured and vessel frequency was counted with a grid ocular micrometer. Percent- age of eccentricity was measured from transverse sections of peduncles of different ages. The radial extent of secondary xylem on upper (UX) and lower side (LX) of the xylem cylinder was measured using an ocular micrometer at a 10× magnification. The percentage of eccentricity was then calculated using the formula, % of eccentricity = UX–LX + UX+ LX × 100, Where UX = Radial extent of secondary xylem on upper side of xylem cylinder and LX = Radial extent of secondary xylem on the lower side of the xylem cylinder.

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Maceration Peduncle xylem from each developmental stage was macerated by using Jeffrey’s fluid (Berlyn & Miksche 1976). The length and width of fibres and vessel elements were recorded. One hundred random measurements were taken for each dimension to obtain mean values.

Scanning Electron Microscopy Samples were cut into blocks of 2–3 mm thickness, dried and coated with gold using planner magnetron sputtering unit (Model 12 MSPT) and observed with a Philips XL 30 ESEM (Philips).

Statistical analysis Analysis of variance (ANOVA) was used to determine statistically significant dif- ferences of anatomical parameters at a 0.05 confidence level using Sigmastat software (Version 3.5, San Jose, CA, USA).

RESULTS Both Couroupita guianensis and Kigelia pinnata are cultivated in India and semi- in the local climate of alternating dry and wet season. In Couroupita, one year old mature peduncles were about one metre long bearing 6–8 round fruits each weighing about 1 kg (Fig. 1A). In Kigelia, one year old peduncles were about 3.5 m long carrying 1–2 oblong fruits, each with a weight ranging from 2 to 5 kg (Fig. 1B). The young peduncles from both species show similarity in length to that of the mature peduncles and carry an inflorescence with more than 10 .

Figure 1. – A: Fruits of Couroupita guianensis hanging from the main trunk. – B: Pendulous long peduncles with fruit in Kigelia pinnata.

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Table 1. Percentage of eccentricity in different regions of peduncles in Couroupita and Kigelia. Species Age Region Radial extent of UX + LX UX + LX %*) secondary xylem Upper (UX) Lower (LX)

CYI Basal 55 36 91 19 21 Middle 24 21 45 3 6 Terminal 21 16 37 5 13 OYI Basal 101 71 172 30 17 Couroupita Middle 62 50 112 12 11 Terminal 37 25 62 12 19 OYF Basal 210 130 340 80 24 Middle 135 98 233 37 16 Terminal 118 40 158 78 49

CYI Basal 34 31 65 3 5 Middle 32 30 62 2 3 Kigelia Terminal 25 24 49 1 2 OYF Basal 78 62 140 16 11 Middle 58 52 110 6 5 Terminal 56 42 98 14 14

*) = Percentage of eccentricity (UX – LX + UX + LX × 100). Note: Measurements are given in µm. CYI, current year’s peduncle bearing inflorescence; OYI, one year old peduncle bearing inflorescence; OYF, one year old peduncle bearing fruit.

Reaction xylem in the peduncle of Couroupita guianensis Tension wood was more strongly developed in the fruit bearing peduncles than in young inflorescences with no fruits. Within the same peduncle the distribution of G- fibres varies from the basal to terminal region. Peduncles do show eccentric secondary growth with more xylem on the upper side (Table 1). In both current and one year old peduncles, G-fibres were more abundant in the basal region (about 60% of the total radius of secondary xylem) closer to the main trunk. In this area, G-fibre distribution extended radially from the periphery to the centre of the xylem cylinder (Fig. 2A). At the middle region of peduncles, G-fibres were less abundant (about 30% of the total radius) representing as 2–3 tangential bands (Fig. 2B) separated by a wide zone of normal fibres. The terminal region of the peduncles showed heterogeneity in G-fibre distribution at various development stages. G-fibres were found to be less abundant in the current year’s peduncle whereas the one year old peduncles have a narrow band of gelatinous fibres near the cambial zone (Fig. 2D) and their abundance was maximal after fruit development (Fig. 2C). The vessels distributed in the basal and middle region of the peduncle were mostly solitary (Fig. 2A & B) whereas the terminal region showed radial multiples of 2–5 vessels (Fig. 2C & D). The SEM studies showed the shrinkage and detachment of the gelatinous layer from the inner fibre cell wall layer (Fig. 2E). The detachment of the G-layer can be due to artefacts during sample preparation and sectioning (Clair et al. 2005). The thickness of the gelatinous layer was greater in the one year old fruit bearing peduncles compared to those of current year’s peduncles.

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Figure 2. – A– G: Transverse sections of Couroupita peduncle at different developmental stages. – A: Basal region of one year old fruit bearing peduncle showing G-fibre distribution. – B: Middle region of the one year old inflorescence bearing peduncle showing tangential bands of G-fibres (vertical bars). – C: Terminal region of one year old peduncle bearing fruit showing distribution of G-fibres with thick gelatinous layer and multiple vessels (arrow). – D: Terminal region of the one year old inflorescence bearing peduncle showing multiple vessels (arrow) and narrow band of G-fibres (vertical bar) in xylem close to cambium. –E : SEM image of G-fibres in Couroupita peduncle showing thick gelatinous layer detached from fibre wall (arrow). – F: G-fibre showing thick gelatinous layer (arrow) at basal region of the one year old peduncle bearing fruit. – G: G-fibres at middle region of one year old fruit bearing peduncle showing G-layer with medium thickness (arrow). – H: Terminal region of one year old peduncle bearing fruit showing G-fibres with thick gelatinous layer (arrow). — Scale bar = 50µ m.

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The thickness of the G-layer also varied at different regions of the same peduncle (Fig. 2F, G & H). G-fibres in leaning branchwood were similar to those found in the basal region of the one year old peduncle. G-fibres with thick gelatinous layers were found in the branch xylem close to the cambium (Fig. 3F).

Reaction xylem in the peduncle of Kigelia pinnata The xylem cylinder along the entire length of the peduncles showed little eccentric growth (Table 1). The basal, middle and terminal regions of both current year and one year old peduncles have a uniform pattern of G-fibre distribution, throughout the xylem cylinder (Fig. 3B & C). However, in the basal region of one year old peduncles a small area of xylem remained with thick-walled normal fibres. The gelatinous layer was thin and remained attached to the inner wall layer (Fig. 3D). The majority of vessels was solitary in the basal and middle region of the peduncle (Fig. 3B & C) but the terminal region had radial multiples of 2–3 vessels. In all three regions gelatinous fibres were uniformly distributed throughout the xylem cylinder. A few thin-walled normal fibres were observed in the xylem area adjacent to the pith. G-fibre abundance was less in branchwood compared to that of the peduncle (Fig. 3E). G-layers were thicker in the one year old peduncle with heavy fruit than in young peduncles (Fig. 3G).

Figure 3. Transverse sections of branchwood of Couroupita (A) and peduncles of Kigelia (B–G). – A: G-fibres in the branchwood showing thick gelatinous layer (arrow). – B: Basal region of the current year’s peduncle bearing inflorescence showing uniform distribution of G-fibres. – C: Middle region of one year old fruit bearing peduncle showing G-fibre distribution. – D: Basal region of the one year old peduncle bearing fruit showing G-fibres with a thin layer of gelatinous layer attached to inner cell wall layer (arrow). – E: Branchwood showing G-fibre distribution as a tangential band (arrows). – F: SEM image of G-fibres in basal region of one year old peduncle showing gelatinous layer remained attached with the fibre wall (arrow). — Scale bar = 50 µm.

Downloaded from Brill.com09/30/2021 01:04:16AM via free access Pramod, Mishra & Rao — Reaction wood in developing fruit stalks 209 0.118 0.511 0.094 0.331 0.438 0.716 0.039 0.087 0.775 0.860 0.165 0.216 0.030 0.337 0.297 0.128 0.043 0.029 0.086 0.023 0.030 0.025 M × T M × < 0.001 . 0.011 0.081 0.025 0.033 0.001 0.571 0.310 0.493 0.100 0.923 0.004 0.827 0.023 0.008 0.001 B × M p -value < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001

, current year’s , peduncle bearing current inflo - year’s 0.008 0.210 0.013 0.306 0.005 0.026 0.146 0.006 0.097 CYI 0/289 B × T B ×

< 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 < 0.001 Couroupita guianensis Couroupita SD 172 14.5 67 3.6 92.6 3.1 342 3.2 86 3.5 12 9.6 594 0.7 0.4 0.4 86 66.7 11.9 1.8 522 0.2 0.2 p -value, probability value; Terminal (T) Terminal 642 56.3 304 15.7 389 18.8 1643 17.6 658 16.1 70 51.6 2484 2.05 1.75 3.6 652 295.3 76 42.8 2657 1.5 1.7 Mean SD 119 9.4 54 2.7 97.2 3.0 580 3.4 91 2.9 15 9.8 489 0.4 0.43 0.57 94 60.4 20 9.49 565 0.2 0.4 Middle (M) 706 59.6 317 17.37 338 22.2 1704 17.7 759 15.1 73 47.6 2159 1.91 2.68 3.5 787 315 85.4 43.3 2132 1.3 2.6 Mean , one year old peduncle bearing fruit. O YF SD 205 11.4 54 3.6 62.5 6 496 4.5 70 3.3 13 4.8 630 1 0.2 0.5 72 59.6 10.5 4.9 412 0.5 0.4 Base (B) 1086 65.6 282 15.4 275 30 1844 21.1 730 14.4 76 35 1721 3.5 1.0 3.4 734 283 66.2 25.9 1986 2.6 1.3 Mean ) 2 µ m) µ m) 2 µ m) µ m)

, one year old peduncle bearing inflorescence; O YI O YF CYI O YF CYI O YI O YI O YF CYI O YI O YF CYI O YI O YF O YI O YF O YI O YF O YF CYI O YI O YF CYI

Length

Width ( µ m) Width

Width Frequency/mm G-layer thickness Length ( Fibre wall thickness Total lumen area (mm Total thickness ( Wall

O YI 1. 2. 2. 3. 1. 1. 2. 4. 1.

N ormal fibre characteristics

Table 2. Comparison of anatomical characteristics between different regions of same age peduncles 2. Comparison of anatomical characteristics between different Table Variable A. Fibre characteristics ( rescence;

B. characteristics Vessel C. G-fibre characteristics ( test ( a = 0.05) are indicated in bold. SD, standard deviation; A NO VA N ote: following Significant differences D.

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0.030 0.945 0.322 0.001 0.684 0.103 0.874 0.094 0.914 0.378 0.078 0.030 0.282 0.945 M × T M × < 0.001 < 0.001 < 0.001 < 0.001 0.311 0.036 0.001 0.013 0.008 0.037 0.323 0.031 0.765 0.778 0.686 0.253 0.012 0.131 B × M p -value < 0.001 < 0.001 < 0.001 < 0 .001 .

0.925 0.752 0.143 0.391 0.162 0.682 0.032 0.692 0.011 0.456 0.004 0.375 0.004 0.138 0.006 B × T B ×

< 0.001 < 0.001 < 0.001 Kigelia pinnata 372 54 2.07 307 127 3 0.2 2.8 0.4 3.0 0.37 0.7 34 0.6 49 0.69 10.8 15.9 SD p -value, probability value; CY I , current year’s peduncle bearing Terminal (T) Terminal 2794 612 31.9 2049 702 26.8 0.46 16.1 0.65 17.9 28 2.5 196 2.79 211 3.38 72 87.5 Mean SD 690 92 3.7 377 127 6.2 0.1 3.4 0.3 3.4 0.5 0.5 42 0.6 39 0.69 21 22.8 Middle (M) 3285 716 32 2206 78.4 27.6 0.38 16.0 0.86 15.6 2.9 3.2 237 3.1 230 3.2 85 109 Mean SD 262 91 3.57 412 117 2.8 0.2 5.8 0.3 3.3 0.6 0.5 43.7 0.6 35 0.6 14.1 17.1 Base (B) 2815 722 23.9 1997 721 20.6 0.54 17.5 0.75 17.0 2.5 2.5 220 3.05 193 3.92 84 89 Mean ) 2 µ m) µ m) 2 µ m) µ m) CY I Length CY I CY I O YF O YF O YF G-layer thickness CY I Width CY I lumen area (mm Total O YF O YF Fibre wall thickness CY I O YF Length ( CY I Wall thickness ( Wall CY I O YF O YF Width ( µ m) Width CY I O YF Frequency/mm 1. 1. 2. 4. 2. 1. 1. 2. 3.

N ormal fibre characteristics

Table 3. Comparison of anatomical characteristics between different regions of same age peduncles 3. Comparison of anatomical characteristics between different Table Variable A. Fibre characteristics (

C. G-fibre characteristics (

B. characteristics Vessel D.

YF, one year old peduncle bearing fruit. inflorescence; O YF, N ote: Significant differencestest following A NO VA ( a = 0.05) are indicated in bold. SD, standard deviation;

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Fibre dimensions In Couroupita, fibres were longer towards the terminal region of the peduncle and the fibre diameter was inversely proportional to fibre length. There was a significant difference in fibre dimensions between different regions of peduncles of all the three developmental stages (Table 2). In Kigelia, fibre length showed significant differences among all the regions (Table 3). In both the plants, branchwood fibres were shorter and narrower than those of the peduncles. In one year old peduncles they were wider in the terminal region and narrowest in the middle region (Table 3).

Vessel dimensions In Couroupita, in both inflorescence and fruit bearing peduncles the vessel element length and width differed significantly among all three regions (Table 2). In Kigelia, in both current year’s and one year old peduncles, vessel element length increased significantly from basal to terminal region (Table 3). The increase in vessel element length is followed by a decrease in width of vessel elements. Compared to peduncles, branchwood showed shorter and wider vessel elements (Table 4).

Vessel frequency In Couroupita, significant differences in vessel frequency were observed between basal and middle and basal and terminal regions of peduncles in all three developmental stages (Table 2). Low frequency of vessels was evident in the regions with a high in- cidence of G-fibres.I n Kigelia, peduncles showed higher vessel frequency, compared to that of Couroupita. Vessel frequency increased from basal towards the terminal region of current year’s and one year old peduncles irrespective of G-fibre frequency (Table 3). Compared to that of peduncles, branchwood had a lower vessel frequency in both species (Table 4).

Table 4. Tension wood characteristics of one year old branchwood in Couroupita and Kigelia.

Couroupita Kigelia ––––––––––––––– –––––––––––––––– Mean SD Mean SD

Fibre length (µm) 734 114 672 65 Fibre width (µm) 15 15 15 3 Vessel element length (µm) 217 90 171 32 Vessel element width (µm) 59 30 107 16

Vessel frequency/mm2 area 30 4 18 2 G-layer thickness (µm) 2.98 0.5 1.2 0.5 G-fibre wall thickness (µm) 0.864 0.1 2.04 0.7 Tension wood severity (%) 77 36

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A Tension wood severity 90 - 80 - ● 70 - ◆ 60 - ◆ OYI ● 50 - ◆ ● OYF 40 - ● 30 - ◆ 20 - 10 - 0 - | | | Base Middle Terminal

B Tension wood severity 25 - ● ● ● 20 - ▲ ▲ CYI 15 - ▲ ● OYF

10 - ▲

15 -

G-layer proportion (%) G-layer proportion (%) 0 - | | | Base Middle Terminal

Figure 4. Tension wood severity in different regions of peduncles of Couroupita (A) and Kigelia (B). - -▲- - = current year’s peduncle with inflorescence, - -◆- - = one year old peduncle with inflorescence; ––●–– = one year old peduncle with fruit..

Gelatinous layer thickness and tension wood severity In Couroupita, G-fibres are restricted to the basal part of the current year’s peduncle while thickness of the gelatinous layer decreases from basal towards terminal regions of one year old peduncles (Table 1). Thinner gelatinous layers and thick lignified fibre walls were found in the middle region. Tension wood severity was relatively high in one year old fruit bearing peduncles (Fig. 4A). The tension wood severity in peduncles of Couroupita was much higher than that of Kigelia peduncles (Fig. 4A & B). In Kigelia, in the middle region of the peduncle, fibres have thinner G-layers than those of the basal and terminal regions of both current year’s and one year old peduncles (Table 2). The G-layer thickness in current year’s branchwood was similar to that found in the basal region of the peduncle (Tables 2 & 3). Thickness of the lignified wall layers in G-fibres was inversely proportional to that of the G-layer. The proportion of gelatinous layer thickness to that of the lignified fibre wall revealed that tension wood severity was greater in all the three regions of one year old peduncles than in younger ones (Table 2). In one year old peduncles the tension wood severity was greater in the basal and terminal region than in the central part (Fig. 4B).

Thickness of normal fibre walls Normal fibres with highly lignified walls were found distributed in the lower region of the xylem cylinder in Couroupita peduncles (Table 2). There was no significant dif-

Downloaded from Brill.com09/30/2021 01:04:16AM via free access Pramod, Mishra & Rao — Reaction wood in developing fruit stalks 213 ference in the wall thickness of normal fibres at different regions of the same peduncle (Table 2). The peduncle of Kigelia also showed normal fibres to be more thick-walled than G-fibres including its G-layer (Table 3). The fibre wall thickness varies significantly in all the three regions of one year old fruit bearing peduncles (Table 3).

DISCUSSION

Growth stresses result from the superposition of two kinds of stress: support stress and maturation stress, the former is an elastic response to the increasing load of the wood and shoots supported by the tree, and the latter originates during wood formation (Clair et al. 2006). Maturation stress allows the tree to adapt to various mechanical constraints. The stresses are formed in three dimensions (longitudinal, radial, and tan- gential). The tension wood formation in maturing peduncles could be supportive stress response because of increasing fruit weight. The great abundance of gelatinous fibres on the tension side of both young and old peduncles in Couroupita is not only due to the weight of the fruits but may also be due to maturation stresses as diameter growth has occurred which can exert tangential and radial growth stress (Huang et al. 2001). The heterogeneity in G-fibre distribution may be a response to varying intensity of stressing forces at various regions of the peduncle. The formation of thick G-layers at the basal region of the current year’s peduncles with inflorescences can be due to the bending force developed by the growing peduncle and weight of the flower buds which generates more internal growth stress at the basal region. Along with the fruit develop- ment, the terminal region of the peduncle is also subjected to the bending force of fruit weight whereas the middle region of the peduncle of both the developmental stages presumably experiences comparatively less stress. In the peduncle of Kigelia uniform distribution of G-fibres is comparable with the G-fibre distribution in the upright poplar stem due to the uniform distribution of growth stresses in all radii (Berlyn 1961). The increment in gelatinous layer thickness in older peduncles is due to the weight of the fruit, increasing the internal tensile stress. Gravity is one of the most formative factors in plants because of its continuity, uni- form intensity and constant direction (Zimmermann & Brown 1971; Linden 2005). The severity of tension wood formation in peduncles of Couroupita is due to their horizontal growth angle to gravity similar to that of branches. Therefore, the reaction mechanism in Couroupita peduncles is similar to that occurring in lateral branches. The mechanism of reorientation of leaning stems has been explained as the expansion of tension wood, pulling the stem into a vertical position (Huang et al. 2001). The gelatinous fibre dis- tribution in Kigelia peduncles is similar to stress responses found in the vertical stems of Fagus, Populus (Isebrands & Bensend 1972), Eucalyptus (Washusen et al. 2002), and Quercus (Burkart & Cano Capri 1974). The bending impact of gravity upon the peduncle of Kigelia can be negligible as it grows vertically from the onset. This leads to uniform distribution of G-fibres in various regions of the peduncle and absence of pronounced eccentric growth as observed in Couroupita. Our observation suggests that the pattern of G-fibre distribution in the Kigelia pe- duncle may be due to the more complicated internal strain distribution (Huang et al.

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2001) as an adaptive mechanism to withstand environmental factors such as wind. G-fibres enhance the elasticity of the xylem (Bamber 2001; Donaldson 2008) that helps the stem to withstand the wind force. The peduncles of Couroupita are short and thick. The considerable diameter growth provides strength and rigidity to the peduncles (Can- nel et al. 1988; Kervella et al. 1994) which helps them to carry several heavy fruits. The dimensional changes of fibres and vessels at various regions of the peduncle are closely associated with developmental stage and distribution of gelatinous fibres. Several au- thors described G-fibres as being longer with narrower compared to normal fibres (Polge 1984; Janin et al. 1990; Jourez et al. 2001). The lower mean width of the G-fibres is associated with higher cambial activity (Jourez et al. 2001). The present study confirms that the dimensional changes of elements in different regions of peduncles are related to the distribution of tension wood fibres. Gartneret al. (2003) reported that severe tension wood may not have any effect on vessel frequency. However, our results indicate that vessel frequency also has a close relation with tension wood severity. Ollinmaa (1956), in his investigations of birch, underscored differences in vessel frequency which can be 50–75% lower in tension wood. On the other hand, increased frequency of vessels at the terminal region of the peduncle in both Couroupita and Kigelia may be due to the multiple vessel formation to meet the demand of water supply to the developing fruits. A similar cause can be attributed to high vessel frequency in peduncles compared to that of branchwood. The high tension wood severity may be the reason why the tension wood in Couroupita peduncles shows a lower vessel frequency compared to that of Kigelia. An increased gelatinous fibre formation is typically accompanied by a significant reduction in size and number of vessel elements produced in the xylem tissue of tension wood (Niklas 1992; Krishnamurthy et al. 1997) as priority is given to the support elements responsible for mechanical strength (Timel 1969). Pitard (1899) pointed out that the fruit weight induces an increase of the mechanical system but the tissue developed in response to fruit weight depends on the plant family in question: the current study shows that the vessel frequency is higher in the secondary xylem of Kigelia, whereas the Couroupita peduncle is characterized by low vessel frequency and a high tissue proportion of thick-walled fibres. So the difference in tissue compo- sition of the mechanical system may also have a relation with the taxonomic distance between Kigelia and Couroupita. In conclusion, the present study reveals the heterogeneity in distribution and sever- ity of gelatinous fibres and structural changes of xylem elements in various regions of the peduncle during two different developmental stages of the peduncle in Kigelia and three developmental stages in Couroupita. The major reason is found to be the posi- tional change of the peduncle which controls the distribution of internal growth stress. It would be interesting to relate the pattern of reaction xylem formation in peduncles with the size of fruits in fruit bearing tree species.

ACKNOWLEDGEMENTS

The authors are thankful to the University Grant Commission, New Delhi for financial assistance under the major research project programme.

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REFERENCES

Archer, R.R. 1986. Growth stresses and strains in trees. Springer series in wood science. Springer- Verlag, Berlin, Heidelberg, New York. 240 pp. Bamber, R.K. 2001. A general theory for the origin of growth stresses in reaction wood: how trees stay upright. IAWA J. 22: 205–212. Berlyn, G.P. 1961. Factors affecting the incidence of reaction tissue in Populus deltoides Bartr. Iowa State J. Sci. 35: 367–424. Berlyn, G.P. & J.P. Miksche. 1976. Botanical microtechnique and cytochemistry. Iowa State University Press, Ames, Iowa. Burkart, L.F. & J. Cano Capri. 1974. Tension wood on southern red oak Quercus falcata Michx. Univ. Tex. For. Papers 25: 1–4. Cannell, M.G.R., J. Morgan & M.B. Murray. 1988. Diameters and dry weights of tree shoots: effects of Young’s modulus, taper, deflection and angle. Tree Physiol. 4: 219–231. Chaffey, I. 2000. Microfibril orientation in wood cells: new angles on an old topic. Trends in Plant Sciences 5: 360–362. Clair, B., T. Almeras, H. Yamamoto, T. Okuyama & J. Sugiyama. 2006. Mechanical behavior in tension wood, in relation with maturation stress generation. Biophysical J. 91: 1128–1135. Clair, B., J. Gril, K. Baba, B. Thibaut & J. Sugiyama. 2005. Precautions for the structural analysis of the gelatinous layer in tension wood. IAWA J. 26: 189–195. Clair, B., J. Ruelle & B. Thibaut. 2003. Relationship between growth stresses, mechano-physical properties and proportion of fibre with gelatinous layer in chestnut (Castanea sativa Mill.). Holzforschung 57: 189–195. Côté, W.A.J., A.C. Day & T.E. Timell. 1969. A contribution to the ultrastructure of tension wood fibres. Wood Sci. & Technol. 3: 257–271. Donaldson, Ll. 2008. Microfibril angle: measurement, variation and relationships. A review. IAWA J. 29: 345–386. Evert, R.F. 2006. Esau’s plant anatomy: Meristems, cells and tissues of the plant body - their structure, function and development. John Wiley and Sons Inc., Hoboken, New York. Fisher, J.B. & J.W. Stevenson. 1981. Occurrence of reaction wood in branches of dicotyledons and its role in tree architecture. Bot. Gaz. 142: 82–85. Fournier, M., H. Baillères & B. Chanson. 1994. Tree biomechanics: growth, cumulative pre- stresses and reorientations. Biomimetics 2: 229–252. Gartner, B.L., J. Roy & R. Huc. 2003. Effects of tension wood on specific conductivity and vul- nerability to embolism of Quercus ilex seedlings grown at two atmospheric CO2 concentra- tions. Tree Physiol. 23: 387–395. Huang, Y.S., S.S. Chen, T.P. Lin & Y.S. Chen. 2001. Growth stress distribution in leaning trunks of Cryptomeria japonica. Tree Physiol. 21: 261–266. Isebrands, J.G. & D.W. Bensend. 1972. Incidence and structure of gelatinous fibres within rapid- growing eastern cotton wood. Wood Fibre 4: 61–71. Janin, G., J.M. Ory & V. Bucur. 1990. Les fibres du bois de reaction. A.T.I.P. 44: 268–375. Jourez, B., A. Riboux & A. Leclercq. 2001. Anatomical characteristics of tension wood and oppo- site wood in young inclined stems of Poplar (Populus euramericana cv ‘Ghoy’. IAWA J. 22: 133–157. Kervella, J., L. Pages & M. Genard. 1994. Genotypic differences in the length relationship of branches of one-year-old peach and nectarine trees. J. Amer. Soc. Hort. Sci. 119: 616– 619. Krishnamurthy, K.V., N. Venugopal, V. Nandagopalan, Y. Hariharan & A. Sivakumari. 1997. Tension phloem in some legumes. J. Plant Anat. Morph. 7: 20–23.

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Linden, A.W. 2005. An investigation into mechanisms of shoot bending in a clone of Populus tremuloides exihibiting ‘crooked’ architecture. MSc thesis: 13–15. Department of Plant Science, University of Manitoba, Winnipeg. Niklas, K.J. 1992. Plant biomechanics: an engineering approach to plant form and function. Plant Biomechanics, Chicago Press, Chicago. Pp. 420–423. Ollinmaa, P. 1956. On the anatomic structure and properties of the tension wood in birch. Acta. For. Fennica 64: 157–263. Patel, R.N. 1964. On the occurrence of gelatinous fibres with special reference to root wood. J. Inst. Wood. Sci. 12: 67–80. Polge, H. 1984. Essai de caractérisation de la veine verte du Merisier. Ann. Sci. For. 41: 45–58. Pitard, J. 1899. Recherches sur I’anatomie comparée des pédicelles floraux et fructifères. Fac. Sci. Paris (Imp. J. Durand, Bordeaux). Staff, I.A. 1974. The occurrence of reaction fibres inXanthorrhoea australis R.Br. Protoplasma 82: 61–75. Timel, T.E. 1969. The chemical composition of tension wood. Svensk Papperstidn. 72: 173– 181. Wardrop, A.B. 1964. The reaction anatomy of arborescent angiosperms. In: M.H. Zimmermann (ed.), The formation of wood in forest trees: 405–456. Academic Press, New York. Washusen, R. & R. Evans. 2001. The association between cellulose crystallite width and tension wood occurrence in Eucalyptus globulus. IAWA J. 22: 235–243. Wahusen, R., P. Ades & P. Vinden. 2002. Tension wood occurrence in Eucalyptus globulus Labill. I. The spatial distribution of tension wood in one 11-year-old tree. Austral. For. 65: 120–126. Washusen, R., J. IIic & G. Waugh. 2003. The relationship between longitudinal growth strain and the occurrence of gelatinous fibres in 10 and 11-year-old Eucalyptus globulus Labill. Holz Roh- Werkstoff 61: 299–303. Zimmermann, M.H. & C.L. Brown. 1971. Tree structure and function. Springer-Verlag, New York.

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