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South African Journal of Botany 81 (2012) 71–78 www.elsevier.com/locate/sajb

Formation and function of aerenchyma in baldcypress (Taxodium distichum (L.) Rich.) and Chinese tallow tree (Sapium sebiferum (L.) Roxb.) under flooding ⁎ G.-B. Wang, F.-L. Cao

College of Forest Resources and Environment, Nanjing Forestry University, Nanjing 210037, Jiangsu Provence, PR China

Received 5 February 2012; received in revised form 3 April 2012; accepted 22 May 2012 Available online 28 June 2012

Abstract

To understand flooding adaptation mechanisms of baldcypress (Taxodium distichum (L.) Rich.) and Chinese tallow tree (Sapium sebiferum (L.) Roxb.), we designed field experiments to examine the changes of morphology, growth, aerenchyma formation, porosity and root O2 consumption of one-year-old seedlings of both species. Both trees were divided into two groups. One group was not flooded (NF, soil water content was 75% of field capacity), while the other group was treated with flooding (FL, water level was 5 cm above soil surface) for 95 days. We found that flooding inhibited growth of both baldcypress and Chinese tallow tree, and biomass increment of baldcypress and Chinese tallow tree under FL decreased 36.4% and 74.5%, respectively, indicating that baldcypress was more tolerant to flooding. Root/shoot ratio of the two tree species increased significantly under flooding, which was primarily due to the decrease of stem and leaf biomass. Flooding also stimulated aerenchyma formation in the roots (lateral and adventitious), stems and leaves of baldcypress and roots of Chinese tallow tree. Porosity in the roots, stems and leaves of the two tree species increased significantly under flooding. The aerenchyma formation and increased porosity enhanced O2 diffusion to the roots. Our results indicate that baldcypress and Chinese tallow tree exhibit a number of adaptive mechanisms in response to flooding, including formation of adventitious roots and new lateral ones, aerenchyma formation, increased porosity of the roots, stems and leaves, and increased O2 release into the rhizosphere. © 2012 SAAB. Published by Elsevier B.V. All rights reserved.

Keywords: Adaptation; Flooding; Lateral and adventitious roots; Porosity; Root O2 consumption

1. Introduction with anaerobiosis. It is reported that not only root but also stem and leaf can develop aerenchyma (Xiao et al., 2009). This gas transport Effects of lack of oxygen in the plant root zone have been well system allows plants to transport atmospheric O2 to the documented to explain flooding stresses (Armstrong and Drew, underground organs to maintain aerobic respiration and to oxidize 2002; Gibbs and Greenway, 2003). Flooding causes oxygen various reductant compounds in the rhizosphere (Kolb and Joly, deprivation in the root system of plants. Since oxygen is essential 2009; Pezeshki, 2001). In some species, poor aeration increases for mitochondrial respiration, this process cannot be maintained aerenchyma formation and hence porosity (Li et al., 2006; under anoxic conditions and must be replaced by other pathways Shimamura et al., 2003). Two mechanisms of aerenchyma (Kreuzwieser et al., 2004). Flood-tolerant plants use several formation have been described: the first one is schizogeny, in strategies to cope with the stress. Aerenchyma development has which development results in the cell separation, and the other is been considered a mechanism critical to a plant's ability to cope lysigeny, in which cells die to create the gas space (Evans, 2004). A lot of adventitious roots also contain aerenchyma cells, which ⁎ Corresponding author. Tel.: +86 25 85427099; fax: +86 25 85427099. rapidly take over the oxygen supply (Glenz et al., 2006). After E-mail address: [email protected] (F.-L. Cao). death of the original roots due to flooding, lateral and adventitious

0254-6299/$ -see front matter © 2012 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2012.05.008 72 G.-B. Wang, F.-L. Cao / South African Journal of Botany 81 (2012) 71–78 roots are produced on the original root system and on the timber and other forestry products in China. However, their submerged portions of the stems. These flood-induced roots are different responses on aerenchyma formation and ROL to generally negatively geotropic and are usually thicker and have flooding between the two species largely remain unknown, and larger intercellular spaces than roots growing in well-aerated soils thus more research is needed. Baldcypress is a deciduous, woody (Polomski and Kuhn, 1998). Furthermore, they are better adapted conifer that can tolerate hydrological regimes ranging from well- to anoxic conditions as they can tolerate higher CO2 concentrations drained to 3 m depth of flooding for its entire growing season or are able to maintain respiration, despite the lack of oxygen. (Vann and Megonigal, 2002). Chinese tallow tree is a deciduous, Adventitious roots also increase water absorption by the roots, they broad-leaved tree that can tolerate seasonal inundation for only oxidize the rhizosphere and transform some soil-borne toxins into 40% of its growing season (Cao et al., 2010). less harmful compounds, and finally they increase the supply of root-synthesized gibberellins and cytokinins to the leaves 2.2. Experimental procedures (Kozlowski, 1997). Increase of radial oxygen loss (ROL) from the roots is another One hundred and eighty seedlings of each species were important adaptive response to flooding in flood-tolerant plants randomly assigned to no flooding (NF) and another 180 seedlings (Li et al., 2006). Rhizosphere oxygenation by ROL is very subjected to continuous flooding (FL). Twelve experimental important for waterlogged plants to overcome anaerobic condi- pools, each of which was 3 m (length)×2.3 m (width)×1.5 m tions. ROL from some plants has been shown to increase soil (depth), were built at Xiashu Forestry Centre of Nanjing Forestry reduction potential (Eh), which enables those plants to survive in University, Jiangsu Province, in November of 2007. The pools an otherwise anoxic condition (Tessnow and Baynes, 1978). It had holes at different heights on the walls for controlling the water also supports aerobic nitrifying or nitrogen fixing bacteria in the level. The pools were filled with surface soil (pH 5.10, organic rhizosphere (Ueckert et al., 1990). The potential for nitrification in matter 22.5 g/kg, hydrolyze nitrogen 155.6 mg/kg, available the rhizosphere is a major consideration underlying the current phosphor 21.6 mg/kg, available potassium 102.3 mg/kg) collect- use of wetlands for purification in both natural and artificial ed from a local farm. Thirty one-year-old seedlings of baldcypress effluents (Armstrong et al., 1994). In addition, ROL from roots to (1.5 cm in diameter and 60 cm in height) and thirty Chinese rhizosphere inhibits methanogenesis, promotes methane (CH4) tallow tree (2 cm in diameter and 80 cm in height) were separately oxidations and thus reduces potential efflux of CH4 from the transplanted in each pool in December of 2007. The treatments – plants. Wetlands contribute 40 50% of total emission of CH4 to were started in June of 2008, and lasted for 95 days. The holes on the atmosphere (Armstrong and Armstrong, 2001). the pool walls were opened in order to get rid of overfilled water Most flood-tolerant tree species are more inclined to develop before treatments, and the seedlings were watered to achieve field aerenchyma in roots than in shoots, and species not responding capacity when it was dry. After treatments, the holes on the pools directly to soil anaerobiosis by enlarging their internal air spaces of the flooded treatments were closed, and the water level was typically undergo anoxia in their roots (Polomski and Kuhn, maintained at 5 cm above the soil surface, while the holes on 1998). Aerenchyma tissues were observed in many tree species, pools of well-watered controls were left opened. such as Avicennia marina (Forsk.) Vierh. (Glenz et al., 2006), Salix nigra Marshall (Li et al., 2006), and Bruguiera gymnorrhiza (L.) Lamk. (Wang et al., 2007). Li and colleagues have 2.3. Morphological observation investigated the effects of flooding on root aerenchyma formation and ROL of plants (Li et al., 2006) and Xiao and colleagues have Three trees in each group were randomly sampled at investigated the effects of flooding on leaf and stem anatomical 16 days, 25 days, 46 days and 82 days after the treatments to responses (Xiao et al., 2009). However, little is known about the check the morphology of the roots and leaves. Photographs flooding effects on adventitious roots, stems and leaves of both were taken on the spot. baldcypress (Taxodium distichum (L.) Rich.) and Chinese tallow tree (Sapium sebiferum (L.) Roxb.). The baldcypress and Chinese 2.4. Formation of aerenchyma tallow tree have different flood tolerance. In this study, we investigated growth, morphological and anatomical processes of The root, stem and leaf segments were taken from the flooded aerenchyma formation of baldcypress and Chinese tallow tree and non-flooded plants on day 82 after treatments, with three under flooding conditions, and its function as an oxygen pathway replicates per treatment per species. The choice of day 82 of from the aerial parts to flooded roots. We also describe the treatment was to ensure that there was a sufficiently long duration relationship between aerenchyma formation and flooding toler- of response, while avoiding a heavy workload on other ance of baldcypress and Chinese tallow tree. measurements on day 95. For the flooded plants, the root segments were taken from the lateral roots (about 2 cm from the 2. Materials and methods taproot) and the adventitious roots (about 0.5 cm from the root- shoot junction), and stem segments were taken from 1 to 3 nodes 2.1. Plant materials from the stem apex, while leaf segments (0.5 cm×0.5 cm) were taken from veins and midribs in the middle of the leaves. As for Baldcypress and Chinese tallow tree are the most common the control (NF), plants segments were taken only from the leaf, tree species used to restore wetland ecosystems while providing stem and lateral root. The standard anatomical method (the G.-B. Wang, F.-L. Cao / South African Journal of Botany 81 (2012) 71–78 73

NF FL NF FL

A B

Fig. 1. The root system of baldcypress and Chinese tallow tree subjected to flooding for 82 days. (A) baldcypress; (B) Chinese tallow tree. Scale bars=2 cm. paraffin cut method; Wei et al., 2008) was followed to study consumptions were determined by sealing an intact plant root formation of aerenchyma. into a flask of nitrogen (N2)-flushed water with initial O2 concentration of 3 mg/L, within the flask measured using a 2.5. Porosity dissolved O2 meter (Multi 350i, Germany). After 2 h, the subsequent decrease in flask O2 concentration was recorded to The samples of lateral root, adventitious root, stem and leaf assess O2 consumption by the roots. Background rates of O2 flux under NF and FL treatment were collected at 90 days after were also determined in a flask with N2-flushed water without a treatment, and their porosities were determined using the plant to adjust O2 measurements. There was a significant change method similar to Visser and Bögemann (2003). A nylon wire in O2 concentration in the blank flask; hence, this was used to was connected to an electronic balance (Sartorius T-214, correct O2 consumption readings of the flask with suspended Germany). A small 40-mL flask was then filled with tap water roots. Shoots were then removed by cutting at the stem base, and at room temperature and closed with a rubber stopper with a the cut surface was immediately sealed with thick parafilm. O2 metal screw hook attached. Subsequently, the flask and stopper consumption from the flask was then measured again after 2 h to were entirely submerged in a tap water-filled 800 mL beaker determine the changes in root O2 consumption. Differences of and the flask was suspended using the nylon wire. After that the root O2 consumption between plants with and without shoots balance was tared for the under-water weight of the flask and indicate the contribution of aerenchyma to atmospheric O2 stopper. Root samples were then dried with tissue paper, cut transportation to the roots under O2 deficiency. into segments of approximately 25 mm and weighed (fresh weight, FW) on an electronic balance (Sartorius T-214, 2.7. Shoot and root growth Germany) to an accuracy of 0.1 mg. Subsequently, the root sample was placed in the water-filled flask, and the flask was Six plants per species were collected to determine biomass again closed and weighed under water (W1). After this, the as baseline before treatment. Ninety five days after treatment, roots were infiltrated with tap water by placing the open flasks eighteen plants (six plants per replicate) per treatment per with root segments under near vacuum conditions twice for species were randomly selected and harvested at the end of the 5 min. The water in the flask was then replaced by tap water at experiment. Roots, stems and leaves were dried and weighed, room temperature, and again the root sample was weighed and the data were used to calculate the total biomass increment under water (W2). The porosity of the tissue was calculated as: and root/shoot ratio. Porosity=100×(W2 −W1)/(FW−W1). 2.8. Statistical analyses 2.6. Root oxygen consumption Data are expressed as the means±SD (standard deviation) of Root oxygen consumption was determined at 92 days after three replicates. Data were tested using an analysis of variance treatment using a method similar to Suralta and Yamauchi and when the F value was significant; the mean of each group (2008). Intact plants with shoots and roots were sampled from the was further tested using Duncan's multiple range test at a 5% pots and washed to remove soil and other dirt. Root O2 significance level.

Table 1 Growth of baldcypress and Chinese tallow tree under NF and FL condition (mean±S.D., n=3), the examples were collected at the end of treatments (95 days). Tree species Treatment Root mass (g) Stem mass (g) Leaf mass (g) Biomass increment (g) Root/shoot Baldcypress NF 26.6±1.8 35.5±2.1 19.1±1.1 70.9±4.2 0.50±0.04 FL 27.1±1.3 22.9±1.3* 5.3±0.4* 45.1±2.6* 0.96±0.05* Chinese tallow tree NF 42.7±2.6 133.7±11.7 26.2±1.6 194.6±9.8 0.27±0.02 FL 26.4±1.1* 29.6±1.2* 1.6±0.1b* 49.6±3.1* 0.84±0.04* Note: the numbers with a star (*) indicate significantly difference between NF and FL within the same species. 74 G.-B. Wang, F.-L. Cao / South African Journal of Botany 81 (2012) 71–78

A: lateral root (NF) B: lateral root (FL) AR CT CT VC

SX VC AR SX

C: adventitious root(FL) D: stem (FL) AR

L CT CT VC SX VC SX

E: leaf midrib(NF) F: leaf midrib (FL) ME

VE VE L ME AR

leaf (FL) G: H: leaf (FL) ME AR ME VE

AR

VE L

Fig. 2. Transverse sections of lateral root, adventitious root, stem, leaf midrib and leaf of baldcypress at 82 days after treatments. CT, cortex; VC, vascular cambium; SX, secondary xylem; ME, mesophyll; VE, vein; AR, aerenchyma; L, lysigenous aerenchyma. Scale bar=110 μm.

3. Result occurred in the submerged segments appeared 46 days after treatment (Fig. 1B). Though both baldcypress and Chinese 3.1. Morphological responses tallow tree seedlings in the NF group also developed adventitious roots and lateral roots, the number of roots was White adventitious roots and white lateral roots began to far less and the size of roots larger in Chinese tallow tree appear after 25 days of flooding in the submerged part of (Fig. 1B). In comparison, baldcypress developed more white baldcypress seedlings, but hypertrophied lenticels did not adventitious and white lateral roots (Fig. 1A). occurred in baldcypress (Fig. 1A). Flooding induced the formation of hypertrophied lenticels, white adventitious roots 3.2. Growth responses and white lateral roots in Chinese tallow tree seedlings (Fig. 1B). The lenticels were already present 16 days after the Flooding significantly affected growth of both baldcypress start of the treatments, and the white adventitious roots that and Chinese tallow tree (pb0.001; Table 1). Total biomass G.-B. Wang, F.-L. Cao / South African Journal of Botany 81 (2012) 71–78 75

A: lateral root (NF) B: lateral root (FL)

CT CT CC

AR VE PR L VE

C: adventitious root (FL) D: lateral root (FL)

L CT AR AR CT PE PE XY L XY

E: stem (NF) F: stem (FL)

CT

CT

VE

G: leaf (NF) H: leaf (FL)

Fig. 3. Transverse sections of lateral root, adventitious root, stem and leaf of Chinese tallow tree at 82 days after treatments. CT, cortex; XY, xylem; AR, aerenchyma. CC, cork cambium; PR, periderm; VE, vessel; PE, pericycle, L, lysigenous aerenchyma. Scale bar=110 μm.

increment of baldcypress and Chinese tallow tree under 3.3. Anatomical responses flooding decreased 36.4% and 74.5%, respectively. Leaf mass declined by 71.5% for baldcypress and 74.5% for Chinese In comparison with the seedlings in the NF group (Fig. 2A tallow tree. Stem biomass decreased by 35.5% for baldcypress and E), flooding induced the development of aerenchyma in and 77.5% for Chinese tallow tree. Root biomass of Chinese adventitious roots, lateral roots, stems, leaf main veins and tallow tree decreased by 38.2%. However, root mass of leaves of baldcypress seedlings (Fig. 2B, C, D, F, G and H). baldcypress was not significantly affected under flooding The aerenchyma of roots and stems formed in the cortex, while conditions. Flooding increased the root/shoot ratio significantly the aerenchyma of the leaf main vein and leaves occurred in the by 92.0% for baldcypress and 211.1% for Chinese tallow tree. mesophyll. The aerenchyma displayed a lysogen pattern. 76 G.-B. Wang, F.-L. Cao / South African Journal of Botany 81 (2012) 71–78

50 50 * Baldcypress Chinese tallow tree NF * 40 FL 40

30 30 * * * * 20 20 Porosity (%) * * * * 10 10

0 0 Leaf Leafstalk Stem Lateral root Adventitious root Leaf Leafstalk Stem Lateral root Adventitious root Tissues

Fig. 4. Porosity of different tissues of baldcypress and Chinese tallow tree under low O2 concentration. At the end of the treatments (90 days), plants were extracted from the soil and different tissues were sampled for porosity. Data shown are means±S.D. of three replicates.

Compared to the seedlings in the NF group (Fig. 3A, E and G), 3.5. Root oxygen consumptions flooding also induced the development of aerenchyma in the cortex of adventitious roots and lateral roots of Chinese tallow The root O2 consumption of Chinese tallow tree was higher tree seedlings (Fig. 3B, C and D), but no aerenchyma was than baldcypress. Removal of shoots led to significantly higher found in the stems and leaves (Fig. 3F and H). The aerenchyma root O2 consumption of baldcypress and Chinese tallow tree in in the adventitious roots and lateral roots of Chinese tallow tree both FL and NF groups (Fig. 5), but to a different extent. In the NF also displayed a lysogen pattern. Although aerenchyma did not group, the root O2 consumption of baldcypress and Chinese tallow form in the stem and leaf of Chinese tallow tree, the tree increased 28.3% and 24.8% respectively, but in the FL group, intercellular spaces increased. the consumption increased 133.3% and 74.6% respectively. The difference in total O2 consumption rate between the seedlings with and without shoots was used to estimate the 3.4. Porosity amount of O2 supplied to the roots via the aerenchyma. The estimated contribution of aerenchyma for O2 transport in flooded Flooding significantly increased the porosity of different roots was 57.4% for baldcypress and 42.7% for Chinese tallow organs of Chinese tallow tree and baldcypress including the tree, and under the control condition, it was only 27.6% for leaf, petiole, stem, lateral root and adventitious root (Fig. 4). baldcypress and 19.8% for Chinese tallow tree (Table 2). Porosity of the leaves, petioles, stems, lateral and adventitious roots of flooded Chinese tallow tree increased by 69.1%, 4. Discussion 50.5%, 43.0%, 30.3% and 92.1%, respectively, and flooded baldcypress increased by 31.1%, 73.5%, 17.4%, 24.0% and Our study demonstrated that flooding restricted the growth of 99.2% respectively. In both FL and NF groups, porosity of our two studied species (Table 1). However, there were different different organs in baldcypress was significantly higher than growth responses between the two species. For examples, the that in Chinese tallow tree (pb0.001). total biomass decreased by 36.4% for the baldcypress tree as

Treatments NF FL NF FL 0

) -1 -1

-2 * root DW hr consumptions -1 2 -3 * * Root O (umol.g -4 with shoot without shoot Baldcypress Chinese tallow tree * -5

Fig. 5. Root oxygen consumption rates under low O2 concentration. At the end of the treatments (92 days), plants were extracted from the soil and transferred to low O2 hydroponics medium for root O2 consumption measurement. Data shown are means±S.D. of three replicates. G.-B. Wang, F.-L. Cao / South African Journal of Botany 81 (2012) 71–78 77

Table 2 The formation of aerenchyma is also reflected by the fact that Effect of flooding on the contribution of aerenchyma to atmospheric O2 the porosity of baldcypress and Chinese tallow tree in different transport to the roots under low O conditions a. 2 organs (root, stem and leaf) increased significantly under Tree species Treatments flooding. The porosity, or relative volume of internal gas spaces, NF b FL in the organs of a plant is an important factor determining a Baldcypress 27.6 57.4* plant's tolerance to flooding (Visser and Bögemann, 2003). Gas Chinese tallow tree 19.8 42.7* diffusion in water is much slower than in air, leading to an Note: the numbers with a star (*) indicate significantly difference between NF extremely limited exchange of gas between submerged plant and FL within the same species. organs and their environment (Jackson and Drew, 1984). Under a The increases or decreases in respiratory oxygen consumption are expressed such conditions, oxygen depletion in plants due to respiration as percentages of the total respiration measured with the roots excised. b may occur within hours (Rijnders et al., 2000). Intercellular air O2 consumption of plants without shoot gave a measure of total O2 demand due to respiration of the plant, i.e. consumption not supplemented by the channels that spatially connect all plant parts allow rapid aerenchyma supply. The rate of oxygen transport through the plant's diffusion of air into the submerged plant parts, as long as some aerenchyma system was calculated from the difference of O2 concentration stems or leaves are above the water surface and the porosity of the between plants with and without shoots (see Fig. 5 for the values). diffusion pathway is sufficiently high (Armstrong, 1972; Armstrong, 1979). We speculate that it was due to the increase compared to 74.5% for Chinese tallow tree; root biomass was not of intercellular spaces under flooding. The increase of tissue significantly altered for baldcypress tree while a reduction of porosity in plants under flooding conditions was correlated with 38.2% was found for Chinese tallow tree. Those different growth both aerenchyma formation and an increase of intercellular responses clearly demonstrate that the baldcypress tree has higher spaces. We also found in this study that tissue porosity of stability in dry matter production (root, stem, leaf) than Chinese baldcypress under no flooding and flooding were both greater tallow tree under waterlogged conditions. Such differences in the than that of Chinese tallow tree. It indicates that more flooding- dry matter production between the two trees under flooding tolerant species might have greater porosity itself, and this result indicate that baldcypress is more flooding-tolerant. In response to may be useful in gauging the flooding-tolerance of species. the flooding treatment, net photosynthesis was reduced signifi- Functional aerenchyma can be assessed by the root O2 cantly in baldcypress, however, this species began to recover consumption without shoots. The removal of shoots limited O2 within 2 weeks of treatment initiation (Pezeshki et al., 1996), diffusion into the roots and root porosity could be used as which also shows that baldcypress is more flooding-tolerant. indicator for the functionality of roots under O2 deficiency. The Different growth responses between the two study species enhanced porosity or aerenchyma in flooded plants effectively have also led to changes in the biomass allocation pattern. As facilitates atmospheric O2 diffusion into the roots. In flooded shown in Table 1, there was an increase in the root/shoot ratio for baldcypress and Chinese tallow tree, shoot removal led to higher both tree species. However, such an increase must have been root O2 consumption, indicating the presence of functional primarily due to the decrease of stem and leaf biomass under aerenchyma. The pattern of increase in root O2 consumption after flooding conditions because root biomass was either insignifi- shoot removal, however, differed between species. Aerenchyma cantly changed for baldcypress tree or less changed as compared in baldcypress had a higher ability of facilitating O2 diffusion to to those in other organs of the Chinese tallow tree. the roots than Chinese tallow tree. Flooding-enhanced aerenchyma formation was different be- In conclusion, flooding restricted growth of both studied tween the baldcypress and Chinese tallow tree. Aerenchyma species. However, it was most visible in Chinese tallow tree. formation was found in the lateral roots, adventitious roots, stems Flooding facilitated the formation of aerenchyma in the roots and leaves of baldcypress, whereas it was found only in the lateral (lateral roots and adventitious roots), stems and leaves of and adventitious roots of Chinese tallow tree. Enhanced aerenchy- baldcypress and the roots of Chinese tallow tree, and this result ma formation is one of the most common adaptive responses of was consistent with the increased porosity in the roots, stems and plants to soil hypoxia and anoxia (Colmer, 2002; Ferreira et al., leaves in both trees. The formation of consecutive aerenchyma in 2009; Jackson and Armstrong, 1999; Pezeshki, 1991). Many the roots, stems and leaves was very important for plants to reports have shown that root aerenchyma forms in plants under survive under flooding condition. The aerenchyma formation and flooding conditions, but only a few studies have been done to show increased porosity enhanced O2 diffusion to the roots. Our results that flooding also facilitates aerenchyma formation in the stem and have shown that baldcypress and Chinese tallow tree exhibit a leaf (Pezeshki et al., 1996; Suralta and Yamauchi, 2008). number of adapting mechanisms in response to flooding. Enhancements of aerenchyma under O2 deficient conditions are commoninsometreespecies(Li et al., 2006; Xiao et al., 2009), but the type of aerenchyma formation is different among different Acknowledgments species (Kong et al., 2008). There are two types of aerenchyma formation: lysigenous (cells die to create the gas space) and The authors thank the following colleagues for their assistance schizogenous (development results in the cell separation) forma- with data collection in this study: Wangxiong Zhang, Wangwen tion (Schussler and Longstreth, 1996). The aerenchyma formation Yu, and Zengfang Yin. This study was funded by the National in baldcypress and Chinese tallow tree is both lysigenous, because Nature Science Foundation of China (30771706) and the Ministry the residual cell walls are found in the aerenchyma. of Science and Technology of China (2006BAD03A0104). 78 G.-B. Wang, F.-L. Cao / South African Journal of Botany 81 (2012) 71–78

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Edited by JS Boatwright