Characterization of Schinopsis Haenkeana Wood Decayed by Phellinus Chaquensis (Basidiomycota, Hymenochaetales)

IAWA Journal, Vol. 33 (1), 2012: 91–104

CHARACTERIZATION OF SCHINOPSIS HAENKEANA WOOD DECAYED BY PHELLINUS CHAQUENSIS (BASIDIOMYCOTA, HYMENOCHAETALES)

María Luján Luna1, 2, *, Mónica A. Murace3, Gerardo L. Robledo4 and Mario C. N. Saparrat5,6,7

SUMMARY Schinopsis haenkeana is a native tree to the Chaco Serrano Forests in Argentina. The white-rot fungus Phellinus chaquensis degrades its wood, causing a white- rot type of decay. The objective of this study was to investigate the structural alterations caused by P. chaquensis in S. hankeana decayed naturally and in vitro. Sound living branches with decay and basidiocarps of P. chaquensis were sampled from the field and in vitro decay tests were performed according to the ASTM D-2017-81 standard method. Naturally decayed branches exhibited an innermost discolored zone with white-rot decay and an outer yellowish-white portion of sound sapwood. Using LM and SEM, degraded tissue displayed diagnostic characters of selective delignification and simultaneous decay. Findings indicate that P. chaquensis causes a mottled pattern of decay (selective delignification plus simultaneous decay) inS. haenkeana wood. Other features such as accumulation of extractives, profuse deposition of crystals and tyloses, typical of Schinopsis spp. heartwood, were additionally observed. In laboratory degraded material, signs of selective delignification and incipient stages of simultaneous decay were noticeable only microscopically. Chemical analysis revealed an oxidative alteration of aromatic moieties in naturally decayed samples which might be related to the accumulation of phenols as a response to fungal attack when compared to sound samples. Naturally degraded sapwood exhibits anatomical and chemical modifications that indicate the development of discolored wood derived from the host-pathogen interaction. Key words: Schinopsis haenkeana, Phellinus chaquensis, anatomy, white-rot decay, pathological heartwood, Fourier transform infrared spectroscopy, aromatic moieties.

1) Cátedra Morfología Vegetal, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, (1900) La Plata, Argentina. 2) Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC-BA). 3) Cátedra Protección Forestal, Facultad de Ciencias Agrarias y Forestales, UNLP, CC 31, (1900) La Plata, Argentina. 4) Laboratorio de Micología, IMBIV, CONICET, Universidad Nacional Córdoba, CC 495, (5000) Córdoba, Argentina. 5) INFIVE, UNLP- CCT La Plata CONICET, CC 327, (1900) La Plata, Argentina. 6) Instituto Spegazzini (FCNyM-UNLP) 53 # 477, (1900) La Plata, Argentina. 7) Cátedra Microbiología Agrícola, Facultad de Ciencias Agrarias y Forestales, UNLP, 60 y 119, (1900) La Plata, Argentina. *) Corresponding author [E-mail: [email protected]]. Associate Editor: Susan A. Anagnost

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INTRODUCTION

Schinopsis haenkeana Engl. (“orco quebracho”, “quebracho del cerro”) is a native tree, belonging to the Anacardiaceae, characteristic of the Chaco Serrano forests from central Argentina and considered vulnerable because of a decline in area of occupancy and the potential levels of exploitation (IUCN 2011). In this country the timbers of Schinopsis spp. are widely utilized because of their hardness and high durability, which are associated with high tannin contents (Roth & Giménez de Bolsón 1997). The most common uses are: fence posts, telegraph poles, bridges, railways, as well as tannin extraction and fire-wood. The white-rot fungus Phellinus chaquensis (Iaconis & J. E. Wright) J. E. Wright & J. R. Deschamps (Basidiomycota, Hymenochaetales) has been reported growing on Caesalpinia paraguariensis (D. Parodi) Burkart and Schinopsis spp. wood in the Chaco Forests (Iaconis & Wright 1953) and is the only heart-rot agent known for Schinopsis haenkeana (Robledo & Urcelay 2009). As a consequence of decay, infected trees are often hollow. Although fungal attack negatively impacts the potential applications of this wood by humans, it is considered an important factor in ecosystem dynamics, because many birds and mammals utilize the cavities formed during decay as a refuge and for nesting (Robledo & Urcelay 2009). Several species of Phellinus are known to cause white heart-rot in hardwoods as well as softwoods around the world (Blanchette 1980; Larsen & Cobb-Poulle 1990; Allen et al. 1996; Callan 1998; Ryvarden 2004). In Argentina, some Phellinus species are reported to have a wide range of substrates, i.e. Phellinus rimosus complex on Cedrela fissilis, Acacia spp., and Prosopis spp., meanwhile other species are only found on a few or one substrate, i.e. P. andinopatagonicus on Nothofagus spp. and Phellinus tabaquilio on Polylepis australis (Wright & Blumenfeld 1984; Deschamps & Wright 2000; Vizcarra Sánchez 2004; Rajchenberg 2006; Robledo & Urcelay 2009). The term white rot has been traditionally used to describe a type of decay where lignin, cellulose and hemicelluloses are degraded and the wood assumes a bleached appearance. Two patterns of white rot are generally recognized: selective delignification and simultaneous decay (Blanchette 1980; Schwarze et al. 2000). In selectively decayed woods, lignin and hemicellulose are preferentially removed causing delignification and separation among cells at the middle lamella. In simultaneous decay, all cell wall components are degraded (i.e. lignin, cellulose and hemicelluloses) thus causing the erosion of the cell wall adjacent to hyphae (Blanchette & Reid 1986; Anagnost 1998). Wood degradation may be dependent on the fungal species and its variation among strains, particular substrate characteristics (wood), nutrient availability and enviromental conditions (Blanchette 1991; Perestelo et al. 1999). Since information about the type of decay caused by P. chaquensis in “orco-quebracho” wood is very limited (Luna et al. 2007; Robledo & Urcelay 2009), this study was done to investigate the structural alterations caused by P. chaquensis in S. hankeana samples from natural forests and in-vitro decayed wood.

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Figure 1–3. Schinopsis haenkeana attacked by Phellinus chaquensis. – 1: General view of a specimen in the Chaco Serrano Forest. – 2: Detail of trunk with basidiomata. – 3: Detail of basidioma.

MATERIALS AND METHODS

Living branches (15–20 cm diameter) of Schinopsis haenkeana, both with basidiomata of Phellinus chaquensis and without fungal fructifications (Fig. 1–3), were collected at Punilla Department, Córdoba Province, Argentina (30º 49' S, 64º 32' W). Sound branches were used as controls and to conduct in-vitro decay testing according to the ASTM D-2017-81 standard method. Laboratory decay tests on dead wood were undertaken in order to distinguish host (living wood) response to fungal attack.

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All the materials (sound, naturally decayed and in-vitro decayed woods) were used for the anatomical and chemical analysis.

Fungal isolation, growth and oxidative enzyme activity on agar plates Fungal mycelium was isolated from the context tissues of P. chaquensis basidioma by inoculating on 2% (w v-1) selective malt extract agar (MEA) medium supplemented with chloramphenicol (50 mg l-1) and benomyl (1–3 mg l-1) and adjusted to pH 7. The strain obtained in axenic culture was subcultured on MEA slants as stock cultures, being deposited in the Culture Collection of Instituto Spegazzini, Universidad Nacional de La Plata, Argentina (LPSC 1087). The strain was identified on the basis of its cultural features, such as growth and oxidative enzyme activity on modified Czapek Dox agar (2%, w v-1) basal media with low (1.1 mM) and high (10.9 mM) ammonium tartrate levels, supplemented with guaiacol (1 mM) according to Saparrat et al. (2009). Description of the fungus and its in-vitro cultural features were based on Iaconis & Wright (1953) and Robledo & Urcelay (2009).

Anatomical study Materials were analyzed under stereomicroscopy, light microscopy (LM) and scanning electron microscopy (SEM). For LM, samples were fixed in formaldehyde-acetic acid-alcohol (FAA), dehydrated through an ethanol series and embedded in paraffin. Sections (8–12 μm thick) were double stained with safranin-fast green (D’Ambroggio de Argüeso 1986). Some sections were left unstained and viewed between crossed polar- izing filters. LM studies were made employing a Nikon Photolab 2 light microscope. For SEM, transverse and longitudinal sections were obtained. Samples were at- tached without pretreatment to aluminum stubs using double sticky tape, air dried and sputter-coated with gold-palladium. Observations were made in a JEOL, JSM-35 CF scanning electron microscope. The anatomical features were described according to Roth and Giménez de Bolsón (1997) and Giménez et al. (2000). The types of decay were identified following the diagnostic characters proposed by Anagnost (1998) and Schwarze (2007).

Fourier transform infrared (FT-IR) spectroscopy The chemical composition of sound and decayed samples was analyzed by means of the potassium bromide (KBr) method on a Bruker Fourier-transform IR spectro- photometer. Wood samples were ground to sawdust (< 0.4 mm) in a refrigerated Janke and sieved in a Kunkel mill. Pellets, consisting of 200 mg KBr and c. 3 mg ground wood, were pressed and scanned from 4,000 to 400 cm-1 averaging 64 scans at 1 cm-1 interval with a resolution of 4 cm-1. The spectra obtained were processed according to Saparrat et al. (2010). Bands selected as index peaks reflecting functional groups, associated with the cell walls and/or chemical changes in the lignocellulosic matrix, were assigned according to Saparrat et al. (2009, 2010).

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RESULTS

Growth and oxidative enzyme activity of Phellinus chaquensis on agar plates When grown on media with low or high N (as ammonium), the isolate developed a dense aerial mycelium with golden-brown color. It exhibited a slow growth, revealing colonies with diameters < 3.0 cm in 15 days at 28 °C. The strain showed extracel- lular oxidative activity only on agar cultures supplemented with guaiacol at high N level.

4 5 6

7 8 9

10 11

Figure 4–11. Schinopsis haenkeana sound wood. – 4: TS. General view showing tissue without secretion products. – 5: LS. Vessel with tyloses (asterisks). – 6: LS. Vascular tracheid on the right. – 7: TLS. General view showing rays uni-multiseriate. – 8: TLS. Secretory canal in ray. – 9 & 10: LS. Rhombic crystals in rays (arrowheads). – 11: RLS. Ray with upright and procumbent cells. – Scale bars in 6 = 10 μm, in 4, 5, 8, 10 & 11 = 50 μm, in 7 & 9 = 100 μm.

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Anatomical observations Sound wood — In transverse sections (TS) sound branches displayed a yellowish-white coloration to the naked eye, characteristic of Schinopsis haenkeana sapwood. Under LM and SEM the following features were observed: diffuse porosity with vessels solitary or in radial multiples of 2–4, occasionally in short tangential multiples, some of them with tyloses; axial parenchyma paratracheal, vasicentric-confluent, scanty (Fig. 4 & 5). Vascular tracheids were evident in longitudinal sections (Fig. 6). Rays uni- or multiseriate, heterogeneous, containing secretory canals with tannins and rhombic crystals (Fig. 7–10), and with two types of cells: upright and procumbent (Fig. 11).

Natural decayed wood — Macroscopically decayed branches showed in TS two dis- tinct zones: a) an innermost red-brownish portion with irregular peripheries and visual evidence of decay, and b) an outer whitish-yellowish portion of sound wood (Fig. 12). The decayed zones displayed an external ring rot pattern and an internal zone with a spongy consistency (Fig. 13). Under LM the altered wood appeared compartmentalized by dark secretions deposited in axial/radial parenchyma and in vessel and fiber lumina, thus creating the uniform red-brownish coloration (Fig. 14 & 15). Vessels were also occluded by tyloses and profuse crystal deposition (Fig. 16). The ring rot pattern consisted of bright whitish fibrillar material intermingled with yellowish to tan mycelia that filled small voids in the wood and had characteristics of selective and simultaneous white rot (Fig. 17 & 18). In longitudinal sections, degraded zones appeared like spindle-shaped areas running parallel to the grain. Under SEM, areas with defibration occurred in zones adjacent to simultaneously decayed cells (Fig. 19). In the former separation among cells (mainly fibers) at the middle lamella was evident, while secondary walls remained free from degradation (Fig. 20). Areas with simultaneous pattern of white rot showed small voids filled with mycelium and all cell walls (mainly in vessels and fibers) were degraded (Fig. 21 & 22). Parenchyma cells appeared chiefly unaltered and filled with phenolic materials (Fig. 22), althought in some portions degradation also reached them (Fig. 20). The central spongy portion displayed a more advanced stage of simultaneous decay. Observations with a light stereoscope showed that abundant mycelia masses were

Figure 12–22. Schinopsis haenkeana wood naturally decayed by Phellinus chaquensis. – 12: General view of decayed branch showing compartmentalization by dark secretions. – 13: De- tail of degraded portion displaying an external mottled pattern (arrow) and an internal spongy zone (asterisk). – 14 & 15: LM views of discolored zone with deposits of secretion products and crystals (arrowheads). – 16: Polarized light micrograph showing profuse deposition of crystals in vessels. – 17: General aspect of fibrillar zones. – 18: General view of pockets filled with mycelium. –19: SEM micrograph showing a zone where selective delignification (left) and simultaneous decay (right) coexisted. – 20: SEM micrograph. Detail of selectively decayed portion showing separation among fibers. – 21: SEM micrograph illustrating a vessel filled with mycelium. – 22: LM micrograph from a zone where generalized cell wall erosion is evident in fibers (arrowheads). Ray cells apparently unaltered (right). The vessel torn at left seems to be an artifact. — Scale bars in 12 & 13 = 5 cm; in 14–16, 20 & 22 = 50 μm; in 21 = 100 μm, in 17–19 = 200 μm; h = hyphae.

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12 13

14 15 16

17 18 19

20 21 22

Figure 12–22 — Legends on the previous page.

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23 24

25 26

27 28 29

Figure 23–29. Schinopsis haenkeana wood naturally decayed by Phellinus chaquensis. SEM micrographs from spongy portion samples. – 23: Holes in vessel elements and profuse erosion of fiber walls. – 24: RLS showing hyphal spread and degradation of rays. – 25 & 26: Details of rounded pit erosion in vascular tracheids, axial parenchyma and fibers. – 27: Erosion troughs in fibers and vascular tracheids. – 28: Inner portion showing abundant mycelia and generalized attack. – 29: A more advanced stage of decay, where fibers and vessel elements appeared almost completely degraded. — Scale bars in 25 & 27 = 10 µm, in 24 & 26 = 20 µm, in 23 & 28 = 50 µm, in 29 = 100 µm.

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Other evidence of simultaneous white rot, like erosion troughs, was present in fibers and vascular tracheids (Fig. 27). Hyphae colonized the whole tissue although they were more abundant in the vessel lumina (Fig. 28). At more advanced stages of decay cells appeared almost completely degraded (Fig. 29).

30 31

32 33

34 35 36

Figure 30–36. Schinopsis haenkeana wood in-vitro decayed by Phellinus chaquensis. SEM micrographs. – 30 & 31: Characteristics of selective delignification: 30: Vessel elements separation at the perforation plates; 31: Separation among fibers caused by ML degradation. – 32 & 33: LS showing hyphae colonization via vessels and unaltered parenchyma rays. – 34: Bore holes in vessel wall. – 35: Hyphae running through tyloses. – 36: Detail of a bore hole (right) and crystals asociated with hyphae. — Scale bars in 36 = 10 µm, in 34 & 35 = 20 µm, in 31 & 33 = 50 µm, in 30 & 32 = 100 µm.

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In-vitro decayed wood — After 12 weeks, P. chaquensis caused a 9–10% weight loss in S. haenkeana wood blocks. Macroscopically no signs of decay were observed. Under SEM separation among cells (mainly vessel elements and libriform fibers) was evident (Fig. 30 & 31). In vessels, cells appeared detached from each other at the perforation plates (Fig. 30). Fibers separated at the compound middle lamellae (ML) conferring a fibrillar appearance to the tissue (Fig. 31). No signs of degradation were found in ray parenchyma cells (Fig. 32). The first stages of simultaneous white rot were also seen in some areas of the wood with abundant mycelium in the vessel lumina and bore holes (Fig. 32–34, 36). Hyphae colonized the tissue mainly through vessels (Fig. 34). When tyloses were present hyphae were observed penetrating through them (Fig. 35). In some samples, crystals associated with the hyphae surface were observed (Fig. 36). Some authors have identified them as calcium oxalate (Tait et al. 1999; Fernandes et al. 2005), though in the present work no analysis was done to identify their chemical composition.

FT-IR spectroscopy analysis on wood Several typical bands were recognized in FT-IR spectroscopy analysis on sound wood as well as degraded wood, the latter being a mixture of material derived from areas with both simultaneous and selective decay (Fig. 37). The bands identified corresponded to stretch of OH groups (3423-30 cm-1), -O-CH3 and -CH2- groups and C–H stretch in aliphatic compounds (2924-6 cm-1), non-conjugated carbonyl groups probably associated with pectins (1726-38 cm-1), conjugated double bonds (C=C and C=O; C=O in the composition of secondary amines and C-C bonds conjugated with benzene rings e.g. in aryl ketones in lignin; absorption band around 1625 cm-1, including N-H bending), aromatic skeletal vibrations in lignin (1509-11 cm-1), alkyl bending vibration of

80 a b

40 Percentage T

0 4000 2000 1000 400 Wave number (cm-1) Figure 37. Fourier transform infrared (FTIR) transmission spectra of samples of Schinopsis haenkeana wood associated with basidiomata of Phellinus chaquensis: a, sound wood; b, decayed wood.

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DISCUSSION AND CONCLUSION

Phellinus chaquensis caused two micromorphological patterns of white rot decay in Schinopsis haenkeana wood: selective and simultaneous. The occurrence of areas with selectively delignified wood interspersed among areas of simultaneously rotted wood with abundant hyphal masses correspond to the mottled pattern described by Otjen and Blanchette (1986) and Blanchette (1991). A similar type of mottled decay was observed by Otjen and Blanchette (1982) in conifer wood attacked by other species of Phellinus, such as P. pini (Brot.) Bondartsev & Singer. In S. haenkeana naturally decayed wood, features such as the demarcation of a discolored zone due to extractives accumulation, together with the occlusion of vessels by tyloses and the profuse deposition of crystals is evidence for a reaction of the living sapwood to fungal attack. The production of coloured sapwood as a response to injury has been called discolored wood, woundwood, false heartwood, or pathological heartwood (Shigo & Hillis 1973; Shigo & Marx 1977; Bamber & Fukazawa 1985; Hillis 1987). Shigo (1979) considered discoloured wood as a barrier tissue developed by the plant to confine the spread of micro-organisms such as wood rotting fungi CODIT( model of Shigo & Marx 1977). One of the plant’s strategies to restrain pathogen pro- gression is to occlude axial and radial cells with tyloses and crystals, as seen in this study, such that the cell lumen is no longer a path of least resistance (Rayner & Boddy 1988; Schwarze et al. 2000). A similar host response was reported by Giménez et al. (2000) in fire-damaged S. quebracho-colorado trees, where sapwood was infiltrated with gummy substances derived from parenchyma cell metabolism. Recently Bravo (2010) described the same phenomenon in Schinopsis lorentzii fire-damaged wood.

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The absence of anatomical evidence of wood defense reactions in laboratory decayed samples (dead wood) reinforces the hypothesis of a pathological heartwood development in living S. haenkeana branches that are attacked by the fungus. Chemical data also suggested discolored wood (pathological heartwood formation) in naturally decayed wood of S. haenkeana. The FT-IR spectroscopy analysis on naturally decayed samples suggests an oxidative alteration of aromatic moieties when compared to sound samples, as similarly seen by Dorado et al. (1999) who investigated other ligninolytic basidiomycetes on wheat straw. Our findings suggest that discoloration of naturally decayed wood appears related to the accumulation of antifungal phenolic substances such as tannins, which are synthetized de-novo by the living parenchyma cells in response to the fungal attack, together with the fungal manufacturing of oxidative detoxifying enzymes to coun- teract the plant defense mechanisms. Fungal oxidases catalyze the transformation of aromatic acids and phenols such as guaiacol type-compounds to quinone products and other chromophores, which are then polymerized to insoluble non-toxic melanins causing the discoloration around the perimeter of infection (Hinds 1981). Since most of the wood-decay Basidiomycota have powerful oxidative enzyme complexes, they can probably detoxify compounds such as tannins found in infected wood over time (Boddy 1992). In conclusion, Phellinus chaquensis caused in Schinopsis haenkeana wood a mottled pattern of decay, consisting of selective delignification and simultaneous decay. Naturally degraded sapwood exhibits anatomical and chemical modifications that indicate the development of discolored wood derived from the host-pathogen interaction.

ACKNOWLEDGEMENTS

We thank Dr. E. Nouhra and Dr. L. Domínguez for field assistance; Rafael Urréjola for his technical assistance during SEM analyses. The reviewers Robert Blanchette and Susan Diehl, and Associate Editor Susan Anagnost are acknowledged for their valuable comments that led us to improve the manuscript. Gerardo Robledo and Mario Saparrat are researchers on the National Research Council of Argentina (CONICET); G. Robledo kindly acknowledges Idea Wild for support with the technical equipment.

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