Compression-Wood-Like Reaction Wood” in Gardenia Jasminoides

Home , Buxus microphylla, Hebe (plant), Pseudowintera, Pseudowintera colorata

Aiso et al. – Compression-wood-likeIAWA Journal 34 (3), reaction2013: 263–272 wood in angiosperms 263

ANATOMY AND LIGNIN DISTRIBUTION OF “COMPRESSION-WOOD-LIKE REACTION WOOD” IN GARDENIA JASMINOIDES

Haruna Aiso, Tokiko Hiraiwa, Futoshi Ishiguri*, Kazuya Iizuka, Shinso Yokota and Nobuo Yoshizawa Faculty of Agriculture, Utsunomiya University, Utsunomiya 321-8505, Japan *Corresponding author; e-mail: [email protected]

ABSTRACT Anatomical characteristics and lignin distribution of ‘compression-wood-like reaction wood’ in Gardenia jasminoides Ellis were investigated. Two coppiced stems of a tree were artificially inclined to form reaction wood (RW). One stem of the same tree was fixed straight as a control, and referred to as normal wood (NW). Excessive positive values of surface-released strain were measured on the underside of RW stems. Anatomical characteristics of xylem formed on the underside of RW and in NW stems were also observed. The xylem formed on the underside exhibited a lack of S3 layer in the secondary fibre walls, an increase of pit aperture angle in the S2 layer, and an increase in lignin content. Some of the anatomical characteristics observed in the underside xylem resembled compression wood in gymnosperms. These results suggest that the increase of microfibril angle in the secondary wall and an increase in lignin content in angiosperms might be common phenomena resembling compression wood of gymnosperms. Keywords: Gardenia jasminoides, compression-wood-like reaction wood, microfibril angle, guaiacyl lignin.

INTRODUCTION

Stems can be accidentally inclined by various environmental factors such as soil move- ment, strong wind exposure, felling of a neighbouring tree etc. In order to restore the required geometry of the trees, reaction wood (RW), which is known as tension wood (TW) in case of angiosperm trees, is formed on the upper side of the stems (Côté & Day 1965; Du & Yamamoto 2007; Déjardin et al. 2010). In many cases TW is char- acterized by the presence of a gelatinous layer (G-layer) in the wood fibres (Onaka 1949). However, angiosperm trees do not always form gelatinous fibres (G-fibres) in the RW (Onaka 1949; Baba 1983; Yoshizawa et al. 2000; Hiraiwa et al. 2007; Sultana et al. 2010). Formation of ‘compression-wood-like reaction wood’ has been observed in some genera of angiosperm trees, such as Pseudowintera, Buxus and Hebe (Onaka 1949; Kučera & Philipson 1978; Meylan 1981; Timell 1983; Yoshizawa et al. 1993a, b, 1999; Baillères et al. 1997; Kojima et al. 2012).

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It is well documented that compression wood (CW) is formed on the underside of inclined stems or branches in gymnosperm trees (Timell 1983; Déjardin et al. 2010). Excessive compressive growth stresses, eccentric growth and higher lignin content have been found in CW. Similarly, ‘compression-wood-like reaction wood’ in angiosperm trees also exhibits excessive compressive growth stress and eccentric growth, and forms highly lignified wood fibre walls on the underside of inclined stems or branches. In Pseudowintera colorata, the microfibril angle (MFA) in the S2 layer of tracheids increased by the formation of RW (Kučera & Philipson 1978; Meylan 1981; Kojima et al. 2012). Kojima et al. (2012) reported that, in Hebe salicifolia, the MFA of fibre walls increased by RW formation, whereas other morphological features and monosaccharide composition of the cell walls in the RW fibres remained unchanged. In some species of the genus Buxus, anatomy and chemical composition of RW has been thoroughly investigated (Yoshizawa et al. 1993a, b, 1999; Baillères et al. 1997). RW of B. microphylla Sieb. et Zucc. var insularis Nakai lacked the S3 layer in vessel and fibre walls. In addition, RW fibres in B. microphylla had a rounded outline in transverse section and the S2 layer of the fibres had a lignin-rich layer (S2 (L)). Furthermore, guaiacyl lignin was increased by the formation of RW in B. sempervirens. It is notable that the characteristics of RW in Buxus species resemble those of CW tracheid in gymnosperm trees. Onaka (1949) reported that Gardenia jasminoides Ellis exhibited eccentric growth on the underside of inclined stem or branches. However, there is no current description of anatomy and lignin RW distribution of G. jasminoides. It has been long thought that ‘primitive’ woody angiosperms cannot form typical G-fibres in RW (Chow 1947; Timell 1969; Baba 1983; Yoshizawa et al. 2000). For instance, some Magnolia species (Magnoliales) do not form G-layers in wood fibres (Yoshizawa et al. 2000). It is debatable whether or not the species forming ‘compression- wood-like reaction wood’ are ‘primitive’. The present study investigated anatomical characteristics, lignin content and lignin distribution in G. jasminoides forming ‘compression-wood-like reaction wood’. In addition, the relationship between the formation of RW in angiosperm species forming ‘compression-wood-like reaction wood’ and their phylogenetic position is discussed.

MATERIALS AND METHODS

A three-year-old tree of Gardenia jasminoides Ellis was planted in the nursery of Ut- sunomiya University, Japan, in early April, 2011. Three coppiced stems from that tree were used in the present study. Two nearly straight stems were artificially inclined at the angles of 50 (sample A) and 70 (sample B) degrees from the vertical to form the RW. The remaining stem (control) which was originally almost straight and vertical, was fixed at 0 degrees from the vertical, and referred to as normal wood (NW). In early September, 2011, all stems were cut down after measuring the diameter at ground level, tree height and surface-released strain. Released strain of the xylem surface was measured on the underside of the inclined stems (about 20 cm above the ground) and on randomly selected sections of the periphery of the straight stem (about 40 cm above the ground) using the strain gage method (Sasaki et al. 1978, Okuyama et al. 1981). After

Downloaded from Brill.com10/04/2021 03:33:27AM via free access Aiso et al. – Compression-wood-like reaction wood in angiosperms 265 measuring the surface-released strain, discs (1 cm in thickness) were collected from positions near those for measuring surface-released strain in the straight and inclined stems, the discs were subsequently fixed in 3% glutaraldehyde in phosphate buffer (pH 7.0). Small wood blocks containing the current annual ring were collected from the underside of the inclined stems and random positions along the straight stem. Cross sections (15 µm in thickness) including the current annual ring were obtained from the underside of the small wood blocks with a sliding microtome (ROM-380, Yamatokohki). Safranine (1% in 50% ethanol) stained and non-stained sections were prepared as described in our previous report (Sultana et al. 2010). Width of the current annual ring at upper and undersides of the inclined stem was measured using cross-sectional images obtained by a microscope (BX51, Olympus) equipped with a digital camera (E-P3, Olympus) and ImageJ software (National Institute of Health). Eccentric growth ratio was defined as the ratio of current annual ring width at the upper side of inclined stem to that of the underside of the inclined stem. In the case of NW, the growth ratio was calculated as the ratio of width of the current annual ring at two random positions. Cross-sectional images were captured using a digital camera and microscope equipped for observing cell morphology (cell wall thickness, cell diameter and frequency of vessels). Cell wall thickness of wood fibres was measured in 100 cells, whereas 50 cells were used for measuring cell wall thickness of vessel elements. Vessel frequency and vessel diameter were determined by capturing15 images from each sample from each of the 30 cells. For measuring the cell length, small blocks were macerated with Schulze’s solution at 70 °C for 2 h. Subsequently, the lengths of 50 wood fibres and 30 vessel elements in each sample were measured using a microprojec- tor (V12, Nikon). A polarizing microscope (BX51, Olympus) was used to observe the secondary wall structure in the wood fibres. The angle of the bordered pit aperture of the wood fibres was measured by using a scanning electron microscope (JCM-5000, JEOL) to estimate the microfibril angles of the S2 layer (Cockrell 1974; Donaldson 1991). Pit aperture angle was measured for 30 cells in each sample. Cross sections were stained with Mäule and Wiesner reagents to observe lignin distribution. Mäule and Wiesner colour reactions were carried out according to the methods described by Yoshizawa et al. (2000). Visible-light (VL) absorption spectra of secondary walls in wood fibres and vessels, and the middle lamellae of cell corners were measured at 450 to 600 nm wavelength for every 5 nm by a microspectrophotometer (UMSP50, Carl Zeiss, spot diameter: 0.5 mm, band width: 5 nm). Measurements were repeated 10 times for each wavelength. Due to the temporary nature of these colour reactions, all measurements were performed within 10 min. Absorption in this range (450 to 600 nm) was measured 5 times for each cell type. Mean values of absorbance were calculated at 515 and 570 nm for Mäule and Wiesner reactions, respectively. Lignin content was determined with the acetyl bromide method (Iiyama & Wallis 1988; Lin & Dence 1992).

RESULTS

Surface-released strain determined in NW had a negative value, −143 µε. In contrast, the released strain indicated positive values on the undersides of inclined stems A

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Table 1. Surface-released strain and eccentric growth ratio in normal wood (NW) and reaction wood (RW) in Gardenia jasminoides.

Surface-released Current annual ring width (mm) Eccentric growth Sample strain (µε) –––––––––––––––––––––––––– ratio upper under NW -143 1.4 1.4 1.0 A 225 0.6 1.4 2.4 B 1228 0.5 0.7 1.4

Note: Inclination angles of stem A and B were 50 and 70 degrees from the vertical, respectively. Eccentric growth ratio was calculated by dividing the current annual ring width on the underside by that on the upper side. and B (Table 1). A positional difference in current growth increment was not observed in NW, while a large difference was observed for the current growth increment on the under and upper sides; the eccentric growth ratio was determined to be 2.4 and 1.4 for A and B, respectively (Table 1). Changes in anatomical characteristics were determined by comparing the underside of the inclined stems to the NW. Vessel frequency, vessel wall thickness and fibre pit aperture angles significantly increased in the xylem on the underside of inclined samples A and B (Table 2). Conversely, vessel diameter, fibre length and fibre wall thickness significantly decreased in the xylem on the underside of inclined samples (Table 2). However, no significant difference in vessel element length was found among the three samples. Figures 1 to 3 illustrate polarizing microphotographs of the cross sections from NW and underside of inclined stems A and B. A three-layered structure of fibre walls was observed clearly in NW, whereas in sample A, almost all wood fibres lacked an S3 layer. A complete absence of the S3 layer was observed in wood fibres on the underside of sample B.

Figure 1–3. Polarizing microphotographs of unstained cross sections in Gardenia jasminoides. – 1: Normal wood (NW). – 2: Underside of inclined stem in sample A. – 3: Underside of inclined stem in sample B. — A = axial parenchyma cell; R = ray; V = vessel; Wf = wood fibre. — In NW (Fig. 1), an S3 layer (arrowheads) is present in the secondary fibre walls. In sample A (Fig. 2), an S3 layer was present or absent. In sample B (Fig. 3) all wood fibres lacked an 3S layer.

Downloaded from Brill.com10/04/2021 03:33:27AM via free access Aiso et al. – Compression-wood-like reaction wood in angiosperms 267 – 1.5 1.9 CC

– 1.9 2.6 Vcw

24.5 ± 4.9 a 42.8 ± 5.5 b 42.6 ± 5.6 b WF (degree)

Wiesner reaction Wiesner – 7.5 8.2 Pit aperture angle in WFcw ––––––––––––––––––––

–

0.8 0.8 CC

Ratio (RW/NW)

m) µ V

– 1.0 0.9 2.0 ± 0.4 a 2.2 ± 0.4 b 2.4 ± 0.4 b Vcw

Mäule reaction

–

0.9 0.9 WFcw –––––––––––––––––––– ––––––––––––––––––––––––––––––––––––––––––

WF Cell wall thickness (

2.4 ± 0.3 a 2.3 ± 0.3 a 3.2 ± 0.5 b –––––––––––––––––––––––––– CC

0.53 ± 0.04 c 1.01 ± 0.09 a 0.79 ± 0.04 b

Vcw V

0.30 ± 0.08 c 0.79 ± 0.02 a 0.56 ± 0.09 b 0.44 ± 0.09 a 0.43 ± 0.09 a 0.43 ± 0.08 a

Wiesner reaction (570 nm) Wiesner .

WFcw

Cell length (mm) –––––––––––––––––––––––––––––––––––– 0.71± 0.12 a 0.77 ± 0.04 a 0.09 ± 0.02 b WF

0.77 ± 0.07 a 0.78 ± 0.15 a 1.11 ± 0.14 b –––––––––––––––––––––––––––

Absorbance (log Io/I) 0.79 ± 0.01 c 0.66 ± 0.01 b 0.65 ± 0.03 b

Gardenia jasminoides Gardenia

m) Vcw µ VD ( 0.49 ± 0.03 ns 0.50 ± 0.10 ns 0.46 ± 0.04 ns 36.6 ± 3.0 e 26.9 ± 2.6 a 32.7 ± 3.7 b

Mäule reaction (515 nm)

) WFcw 2 ––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––––– –––––––––––––––––––––––––––––––––––– 0.55 ± 0.01 a

0.47 ± 0.04 b 0.48 ± 0.03 ab

115 ± 19 a 154 ± 40 b 156 ± 32 b (No./mm

Lignin content (%) 23.9 ± 3.7 ns 28.5 ± 3.7 ns 29.1 ± 3.3 ns

A B

NW A B Sample NW Sample Note: WFcw = wood fibre cell wall; Vcw = vessel cell wall; CC = A, middle and lamellaTable B of 1. The refer cell same to corner; letters, NW, followed by means TukeyHSD test (p in the and standard deviations indicate no significant difference < 0.05). Note: VF = vessel frequency; VD = vessel diameter; WF = wood fibre;V A, = and vessel; BTable NW, refer 1. to The same letters followed by means and standard TukeyHSD test (p in the deviations indicate no significant difference < 0.05). Table 3. Lignin content and absorbance measurements of different types and parts of cells stained with Mäule and Wiesner reagents. Wiesner types and parts of cells stained with Mäule 3. Lignin content and absorbance measurements of different Table

Table 2. Cell morphology in NW and RW of and RW 2. Cell morphology in NW Table

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Table 3 illustrates lignin contents and absorbance measurements at 515 nm and 570 nm after Mäule and Wiesner reactions. Figures 4 to 7 illustrate cross sections of NW and underside of sample B after Mäule and Wiesner colour reactions. Although the lignin content in RW was higher than that in NW, no significant differences among the three samples were found in the lignin content determined by the acetyl bromide method. By observing the photomicrographs, almost no colour difference was found between NW and the underside of inclined stems after the completion of Mäule staining. However, the absorbance at 515 nm after Mäule reaction measured by microspectrophotometry

Figure 4–7. Microphotographs of the cross sections in NW and sample B of Gardenia jasminoides after Mäule and Wiesner reactions. – 4: NW after Mäule reaction. – 5: Underside of inclined stem in sample B after Mäule reaction. – 6: NW after Wiesner reaction. – 7: Underside of inclined stem in sample B after Wiesner reaction. — Similar colour intensities were observed in the secondary wall of fibres, vessels and middle lamella of cell corners after the Mäule reaction. Colour intensity after the Wiesner reaction significantly increased on the underside of sample B compared to NW.

Downloaded from Brill.com10/04/2021 03:33:27AM via free access Aiso et al. – Compression-wood-like reaction wood in angiosperms 269 significantly decreased in the secondary fibre walls and the middle lamella of cell corners in the underside of A and B samples. No significant differences in the absorbance measured at vessel cell walls were found between the three samples. On the other hand, in the Wiesner reaction, secondary walls of wood fibres, vessels and cell corners in the underside of the inclined stems were more strongly stained compared to those in NW. On the underside of samples A and B, the absorbance at 570 nm following the Wiesner reaction was significantly higher in the secondary wall of fibres and vessels and middle lamella of cell corners than in NW.

DISCUSSION

It is well known that growth eccentricity and occurrence of excessive compressive growth stresses on the underside of inclined stems or branches are considered typical characteristics of CW in gymnosperm trees and several angiosperm trees belonging to the genera Pseudowintera, Buxus and Hebe (Onaka 1949; Kučera & Philipson 1978; Meylan 1981; Timell 1983; Yoshizawa et al. 1993a; Baillères et al. 1997; Déjardin et al. 2010; Kojima et al. 2012). In this study, negative surface-released strain was observed in NW (Table 1), suggesting that weak tensile growth stress occurred on the xylem surface of NW. On the other hand, positive surface-released strains were observed on the underside of both A and B samples (Table 1), suggesting that excessive compressive growth stress was generated on the underside of inclined stems. Frequency and diameter of vessels decrease in many angiosperm trees, which form G-fibre in TW (Côté & Day 1965; Jourez et al. 2001). This is also true for RW in Buxus microphylla (Yoshizawa et al. 1993a). However, Kojima et al. (2012) reported that vessel morphology in Hebe salicifolia remained unchanged in RW. RW formed in Gardenia jasminoides showed an increase in vessel frequency, whereas vessel diameter decreased compared to NW (Table 2). In contrast, CW tracheids formed in gymnosperms are shorter and have thicker cell walls and a rounded outline in transverse section (Timell 1983). Kojima et al. (2012) reported that both opposite wood (OW) and RW show approximately the same fibre lengths in RW of Hebe salicifolia. Tracheids in RW of Pseudeowintera colorata are longer than in the OW (Kučera & Philipson 1978). Furthermore, a decrease in fibre tracheid length was observed in RW of Buxus microphylla (Yoshizawa et al. 1993a). Therefore, changes of fibre length due to RW formation in G. jasminoides (Table 2) are similar to those in Buxus microphylla. Secondary walls of NW fibres show a three-layered structure (S1 + S2 + S3), while TW fibres show S1 + G, S1 + S2 + G, or S1 + S2 + S3 + G (Onaka 1949; Nakagawa et al. 2012). Some species which do not form typical G-fibres also lack the S3 layer (Okuyama et al. 1994; Yoshizawa et al. 2000). Recently, Sultana et al. (2010) reported that some Japanese angiosperm species do not change the layered structure of secondary fibre walls in RW. The RW of ‘compression-wood-like reaction wood’ species, Buxus microphylla, shows the lack of an S3 layer (Yoshizawa et al. 1993a). In the present study, wood fibres on the underside of sample B also lacked an S3 layer in the secondary wall. The increase of MFA in

Downloaded from Brill.com10/04/2021 03:33:27AM via free access 270 IAWA Journal 34 (3), 2013 tracheids is a typical characteristic of CW in gymnosperms (Côté & Day 1965; Timell 1983). This is also true for ‘compression-wood-like reaction wood’ in several angiosperm tree species (Kučera & Philipson 1978; Meylan 1981; Yoshizawa et al. 1993a; Kojima et al. 2012). For instance, in Hebe salicifolia, MFAs of S2 layers of the RW and OW fibres were 30.2±6.4 and 21.7± 3.4 degrees, respectively (Kojima et al. 2012). This study also demonstrated that the pit aperture angle in the wood fibres dramatically increased with the formation of RW. Therefore, we conclude that the lack of S3 layer and increase in MFA of tracheids or fibres in RW may be a common phenomenon occurring in angiosperm trees which form ‘compression-wood-like reaction wood’. In gymnosperm trees, lignin content increases due to the formation of CW (Côté & Day 1965; Timell 1983). Angiosperm trees which form ‘compression-wood-like reaction wood’ also have an increased lignin content (Yoshizawa et al. 1993a, b, 1999; Baillères et al. 1997). Baillères et al. (1997) reported that lignin content in the RW and OW of Buxus sempervirens increased to 31.0 %, and 27.9 %, respectively. The present study exhibited a tendency of increased lignin content due to the formation of RW in Gardenia jasminoides (Table 3); however, no significant differences were observed in the lignin content between NW and RW. Lignin in angiosperms is composed of syringyl and guaiacyl units (Lin & Dence 1992; Takabe et al. 1992). Yoshizawa et al. (1993b, 1999) reported that the guaiacyl units in lignin increased in the secondary wall of wood fibres, vessels and the middle lamella of cell corners with the formation of RW in Buxus microphylla, while the content of syringyl units decreased. In the present study, microspectrophotometry revealed that lignin stained with Wiesner reagent remarkably increased in the secondary wall of fibres, vessels and the middle lamella of cell corners in RW, whereas lignin stained with Mäule reagent slightly decreased among all samples (Table 3 and Figures 4–7). These results suggest that formation of RW causes a change in the S/G ratio in G. jasminoides. In general, the cell wall lignin of tracheids in gymnosperms is almost entirely composed of guaiacyl units (Lin & Dence 1992) and an increase of guaiacyl units occurs in the formation of CW (Parhan & Côté 1971). An increase in the guaiacyl units due to the formation of RW was also observed in G. jasminoides. Angiosperm species, such as Pseudowintera colorata, Trochodendron aralioides and Sarcandra glabra are considered ‘primitive’ as vessels are absent in them (Kučera & Philipson 1978; Meylan 1981; Kuo-Huang et al. 2007). These species are located at different places in the phylogenetic tree of angiosperms reconstructed on the basis of molecular analysis (Bremer et al. 2009), suggesting that these species are not very closely related. It has been proposed that ‘compression-wood-like reaction wood’ is also found in ‘primitive’ angiosperm species (Kučera & Philipson 1978; Meylan 1981; Yoshizawa et al. 1993a, b, 1999). However, some of the orders of species which form ‘compression-wood-like reaction wood’ (Pseudowintera colorata in Canellales, Buxus in Buxales, G. jasminoides in Gentianales and Hebe salicifolia in Lamiales) are found at the ‘advanced’ positions in the phylogenetic tree, suggesting that functions similar to CW may have been acquired by parallel evolution in angiosperms with ‘compression- wood-like reaction wood’.

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Accepted: 15 March 2013 Associate Editor: Lloyd Donaldson

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