Springer-VerlagTokyo102650918-94401618-086030669031Journal
of Plant Research J
Plant Res18110.1007/s10265-004-0181-3
J Plant Res (2004) 117:465–472 Digital Object Identifier (DOI) 10.1007/s10265-004-0181-3
© The Botanical Society of Japan and Springer-Verlag Tokyo 2004
ORIGINAL ARTICLE
Hery Purnobasuki • Mitsuo Suzuki
Aerenchyma formation and porosity in root of a mangrove plant, Sonneratia alba (Lythraceae)
Received: June 28, 2004 / Accepted: September 28, 2004 / Published online: November 5, 2004
Abstract Aerenchyma gas spaces are important for plants that grow in flooded and anaerobic sites or habitats, because these gas spaces provide an internal pathway for oxygen transport. The objective of this study is to characterize the development of aerenchyma gas spaces and observe the porosity in roots of Sonneratia alba. Tissue at different developmental stages was collected from four root types, i.e. cable root, pneumatophore, feeding root and anchor root, of S. alba. In S. alba, gas space is schizogenously produced in all root types, and increases in volume from the root meristem to mature root tissues. The aerenchyma formation takes place immediately, or 3–5 mm behind the root apex. At first, cortical cells are relatively round in cross sections (near the root apex); they then become two kinds of cells, rounded and armed, which combine together, forming intercellular spaces behind the root apex. The average dimensions of cortical cells increased more than 1.3 times in the vertical direction and over 3.3 times in the horizontal direction. At maturity, aerenchyma gas spaces are long tuberous structures without diaphragms and with numerous small pores on the lateral walls. Within the aerenchyma, many sclereids grow intrusively. Root porosity in all root types ranged from 0–60%. Pneumatophores and cable roots had the highest aerenchyma area (50–60%). Key words Aerenchyma · Cortical cells · Porosity · Roots · Sclereids · Sonneratia alba
Introduction Prolonged seawater flooding leads to an anaerobic root environment for mangrove plants. Wetland species of plants, however, have adapted to the anaerobic conditions
H. Purnobasuki (*) · M. Suzuki Botanical Garden, Graduate School of Science, Tohoku University, Kawauchi, Aoba-ku, Sendai 980-0862, Japan Tel. +81-22-2176789; Fax +81-22-2176761 e-mail:
[email protected]
either by rooting superficially in order to take advantage of the oxygen available in the upper soil or in water, or by developing aerenchyma, an extensive network of gas spaces throughout the root cortex (Armstrong 1979; Justin and Armstrong 1987; Laan et al. 1989; Jackson and Armstrong 1999; Visser et al. 2000b). Aerenchyma is plant tissue that is permeated by gas spaces. Aerenchyma reduces flooding stress by allowing an internal pathway for oxygen to the root zone to aid in respiration and oxidation (Armstrong et al. 1994; Schussler and Longstreth 2000). Despite the importance of aerenchyma to the survival of wetland species, little is known about the processes that lead to its formation in mangrove plants. Most the research on aerenchyma has taken place in other plants, i.e., the crops Zea mays (Campbell and Drew 1983) and Oryza sativa (Webb and Jackson 1986) and the grass Spartina alterniflora (Maricle and Lee 2002); or is related to aerenchyma formation in the shoots of Scirpus validus, petioles of Sagittaria lancifolia, and leaves of Sparganium eurycarpum, Sagittaria lancifolia and Typha latifolia (Kaul 1971, 1974; Schussler and Longstreth 1996). All of these investigations have been of herbaceous plants and the lifespan of the anaerobic organs is rather short. In trees, the root system is more persistent. Therefore, it is expected that roots of trees growing in anaerobic conditions develop a more persistent aerenchyma system than those of the herbaceous plants. The importance of aerenchyma and the physiology of root aeration to the survival of mangrove species has been described (Scholander et al. 1955; Curran 1985; Curran et al. 1986; Hovenden and Allaway 1994; Ashford and Allaway 1995; Skelton and Allaway 1996; Allaway et al. 2001), but very little is known about the development and organization of aerenchyma tissue in mangrove root systems. Developmental study from the root apex to the mature parts would be required to understand this conclusively (Allaway et al. 2001). Sonneratia alba is a pioneering mangrove species of Lythraceae and often grows in newly formed sand or mud flats in the outer fringe of the mangrove forest, and sometimes even constitutes a pure and sparse forest in the seaward zone. This species is fast-growing and can grow up to
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4–5 m tall; at maturity, in Japan, it rarely exceeds 6 m. This species develops a highly specialized root system of four main types (cable root, feeding root, anchor root and pneumatophore) (Troll and Dragendorff 1931; Tomlinson 1986). Anatomical knowledge of Sonneratia roots is scanty. There have been some previous investigations dealing with the structure of Sonneratia’s pneumatophores as aerating organs (Troll and Dragendorff 1931) and as waterconducting systems (Sun et al. 2004). The objective of this study was to examine and compare the characteristics of the structure and arrangement of cortical cells in four root types of Sonneratia alba to better understand how aerenchyma gas spaces are formed.
Materials and methods Material All root samples were taken from adult trees of Sonneratia alba J. Smith, which grow naturally in Komi estuary (24°19¢N, 123°54¢E), Iriomote Island, Okinawa Prefecture, Japan. The sampled trees were sparsely distributed in the outer fringes (seaward) of a mangrove forest where the plants were flooded by all high tides and easily influenced by strong winds and tidal forces. Around the sampled trees, we excavated root systems during low tide, and collected (1) cable-root tips, (2) pneumatophore tips, (3) feeding-root tips and (4) anchor-root tips. For each root type, we collected ten roots. The root samples were cut out along the axis of each root from the tip at 1 cm intervals. Histology The samples were fixed in FAA (70% ethanol, 10% formalin, 5% acetic acid, 90 : 5 : 5). The air in the tissue was evacuated using an oil rotary vacuum pump. The samples were dehydrated in an ethanol series and embedded in Paraplast Plus (Oxford Labs, USA) in 59°C. Sections were cut, 10–12 mm thick, by a rotary microtome (HM 350 Microm, Heidelberg Germany), stained in safranin/fast green (Johansen 1940; O’Brian and McCully 1981; Sanderson 1994), and permanently mounted using Bioleit. The observation was done using a light microscope (B ¥ 50, Olympus, Japan). Microscopic images were taken by microscopy camera (Olympus PM-C35, Japan) and recorded on Fuji Film Neopan F ISO 32/16° for black and white prints. For scanning electron microscopy, the tissue was dehydrated in graded ethanol/t-butyl alcohol and freeze-dried at -10°C (HITACHI ES-2030 Freeze Dryer). The dried samples were glued to the specimen stubs coated with conductive carbon tape. The samples were coated with platinumpalladium in a vacuum evaporator (HITACHI E-1030 Ion Sputter), and viewed and photographed using a scanning electron microscope (HITACHI S-4100). A maceration study was also carried out for sclereid observation. The samples were trimmed into slivers thinner than a toothpick and then kept in a mixture (1 : 1) of glacial
acetic acid and 6% hydrogen peroxide at 60°C for 36 h. After this treatment, the macerated materials were washed in distilled water and stained in safranin O. Macerated sclereids were mounted for observations. Porosity measurements Digital images of root cross sections were first taken by a digital microscopy camera (Fujix digital camera HC-300, Japan) and saved as image files using a software package of Fujix Photograb-300. The saved image files were then analyzed with Scion Image 1.63 software (Scion Corporation, Frederick, MD) to measure the percentage of root area composed of aerenchyma. Digital images of root cross sections (Fig. 1A) were adjusted to maximize contrast by converting the image to black and white only (Fig. 1B). To determine total cross-sectional area, aerenchyma spaces were filled, resulting in a solid, black silhouette (Fig. 1C), and the number of pixels was quantified. Aerenchyma area was determined by returning to the original image (Fig. 1B), then inverting it to form a negative image (Fig. 1D). Pixels composed of lacunae were quantified. The root porosity was determined according to the method of Armstrong (1979), Maricle and Lee (2002), and Visser and Bögemann (2003) using the equation: root porosity (%) = 100 ¥ (area of air spaces/total cross-sectional area) Root sections were taken from 1–100 mm from the root tip at 2-mm intervals from 0–10 mm and 10-mm intervals from 10–100 mm. Ten roots were sectioned for each root type, then measured and averaged. Root porosity results at each position relative to the apex were analyzed using one-way analysis of variance (ANOVA; Minitab version 13; a = 0.05).
Results Development and structure of the aerenchyma In anchor roots, tissues close to the root apex (100–300 mm) lacked intercellular spaces, and cortical cells filled up the area between the endodermis and the epidermis in each root type (Fig. 2A). All the cells in the cortex appeared round in cross section without intercellular spaces. In longitudinal view, cortical cells were tightly packed and appeared in files parallel to the root axis starting 100– 300 mm behind the apex (Fig. 3A). Surrounding the cortex there were generally three layers of small and rectangular cells that represent a multilayered epidermis (Fig. 2D). Inside the epidermal layers there were several layers of cortical cells (outer cortex) which were slightly larger than the epidermal cells and compactly packed side by side with radially elongated shapes (Fig. 2D). Inside the outer cortex, larger polygonal cells of the inner cortex filled the cross section (Fig. 2D). A distinct endodermis marked the inner border of the cortex (Fig. 2A, B). All cells of the root were arranged in longitudinal files near the root apices (Fig. 3A).
467 Fig. 1A–D. Representative images used in digital quantification of root porosity. A Grayscale digital image of feeding roots cross section. B Same image as A, converted to black and white. C Total root cross-sectional area. D Aerenchyma spaces. Total aerenchyma area is calculated by dividing the number of pixels in D by the number of pixels in C. Adopted from Maricle and Lee (2002). Bar = 300 mm
The aerenchyma formation occured in the inner cortex and started to develop at 3 mm behind the root apex. Cells were slightly separated (schizogenously) from the neighboring cells in some areas of the inner cortex (Fig. 2B). The intercellular spaces became larger as the distance from the root apex increased. Cortical cells in cross sections were nearly round near the root apex and then differentiated into two different shapes: rounded cells and armed cells with three to four protruding arms. These cells together created intercellular spaces (Fig. 2C, E). In longitudinal view, intercellular spaces appeared between longitudinal files of the cortical cells (Fig. 3B). The number of files between the endodermis and the outer cortex did not change during the root development (Table 1). Lysigenous cell dissolution was not observed in any cortical tissues of any roots. As the distance to the apex increased to 3–5 mm, the cortical cells appeared to be separated and produced schizogenous intercellular spaces (Fig. 3B). At 4 cm distant, intercellular spaces were well developed, forming long tubes running parallel to the root axis (Fig. 3C, D). At its maturity, the aerenchyma was round or radially elongated, elliptical or polygonal in cross section, 35–50 mm in diameter, and took the form of long tubes of indeterminate length in longitudinal section. The tubes had numerous small pores (about 7–10 mm in diameter) on the lateral wall, which is
formed by cortical cells between the neighboring aerenchyma tubes. The pores were schizogeneously formed by three or four cortical cells (Fig. 4A, B). The number of outer cortical cells surrounding the inner cortex did not increase during the root maturation (Table 1), and individual cells were tangentially enlarged and flattened (Fig. 2C, E). Root diameters in mature parts were about 1.8 times larger than those near the root apices. As a result of thickening growth, the primary epidermal layers had split and peeled away without secondary growth. The aerenchyma formation process observed in the other three root types was fundamentally the same as that of the anchor roots except for size variation. In feeding roots, cable roots and pneumatophores, the aerenchyma also formed by schizogeny. The aerenchyma was well-developed and was created by a spatially regulated distribution of different degrees of cell separation, expansion and division between cortical cells. The increase in root diameter from the root apices to the mature parts was about 1.8 times in feeding roots, 3.1 times in pneumatophores and 3.7 times in cable roots (Table 1). The average horizontal dimensions of the inner cortical cells increased 1.3–1.4 times in the vertical direction and 3.3–4.2 times in the horizontal direction (Table 2). Aerenchyma diameter in cross section was 35–40 mm in feeding
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Fig. 2. Cross sections of anchor roots of Sonneratia alba, obtained at 300 mm (A), 3 mm (B), 4 cm (C), 500 mm (D), and 8 cm (E), respectively, distant behind the root apex, showing development of aerenchyma gas spaces in cortex. A The gas spaces are not yet developed, cortical cells are relatively rounded. Bar = 100 mm. B Some cortical cells have separated and formed gas spaces. en Endodermis. Bar = 100 mm. C A well-developed aerenchyma (asterisk) is formed as
large lacunate cortex. There are two kind of cortical cells, rounded cells (rc) and arm cells (ac). Bar = 100 mm. D Multilayered epidermis (ep), outer cortex (oc) and inner cortex (ic) are visible. Bar = 50 mm. E Welldeveloped aerenchyma (asterisk) and the outer cortical layers that do not develop air spaces have replaced the epidermal layers for protection. Bar = 25 mm
roots, 80–100 mm in cable roots and 90–110 mm in pneumatophores. There were many sclereids developed in the aerenchyma of cable roots and pneumatophores (Fig. 4), while sclereids were not observed in anchor roots or feeding roots. Sclereids of cable roots and pneumatophores began to initiate in the inner cortex close to the root apex (3–5 mm from the root apex) and matured at 30–50 mm distant from the root apex. The sclereids were longitudinal with several arms that grew intrusively within the aerenchyma tube (Fig. 4A, B). The sclereid form was quite similar in cable roots and pneumatophores (Fig. 4C, D).
reached its maximum in feeding roots (39%) and anchor roots (41%), while gradually increasing further in cable roots to about 50% and in pneumatophores to about 60% at 10 cm from the root apex, although further increases may be expected in those roots.
Root porosity Root porosity in all root types rapidly increased between 0 and 10 mm from the root apex (Fig. 5). The porosity soon
Discussion Development and structure of the aerenchyma There was a marked change in the shape and size of cortical cells in all root types of Sonneratia alba during development. The distorted shapes of the inner cortical cells in root sections (transversal and longitudinal) with well-developed intercellular spaces clearly revealed that the intercellular spaces were created by the separation of cortical cells
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Fig. 3A–D. Longitudinal sections of anchor roots of Sonneratia alba, obtained at 100 mm (A), 3 mm (B), 4 cm (C), 8 cm (D), respectively, distant behind the root apex, showing development of aerenchyma gas spaces (asterisks) in cortex. A The gas space is not yet developed and cortical cells (co) are tightly packed. en Endodermis, ep epidermis, rc
root cap. B Some cortical cells are separated and form gas spaces. C Gas spaces are elongated parallel to the root axis, and cortical cells become enlarged. D Well-developed aerenchyma is formed as a wide and long lacunae. Bar = 50 mm
Table 1. Root diameter and cortical cell numbers at difference distances from the root tip in four root types of Sonneratia alba Distance from tip in different root types (mm) Feeding roots 2 6 10 20 Anchor roots 2 6 10 20 Pneumatophores 2 6 10 20 Cable roots 2 6 10 20
Diameter (mm)
Cells in outer cortex (cross-sectional view) (n)
Radial files of cells in the inner cortex (longitudinal view) (n)
0.95 ± 0.02 1.25 ± 0.02 1.68 ± 0.03 1.72 ± 0.02
368 ± 8.57 366 ± 7.03 365 ± 8.24 370 ± 7.98
22 ± 6.01 17 ± 5.23 16 ± 3.63 14 ± 4.03
1.25 ± 0.02 1.50 ± 0.02 1.68 ± 0.01 2.25 ± 0.02
269 ± 4.71 270 ± 4.73 270 ± 3.91 280 ± 4.80
15 ± 2.54 15 ± 3.07 13 ± 1.89 13 ± 1.04
2.25 ± 0.02 3.50 ± 0.03 4.25 ± 0.03 6.88 ± 0.02
430 ± 12.26 428 ± 15.04 445 ± 10.98 451 ± 20.43
38 ± 7.44 37 ± 4.62 36 ± 5.41 36 ± 3.22
1.90 ± 0.02 2.60 ± 0.03 3.50 ± 0.03 6.95 ± 0.04
465 ± 11.43 468 ± 12.56 473 ± 10.11 520 ± 23.65
35 ± 4.21 32 ± 5.35 30 ± 4.76 30 ± 4.56
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Fig. 4. Longitudinal scanning electron micrographs (SEM) showing aerenchyma and sclereids in the inner cortex of pneumatophores (A) and cable roots (B). Sclereids of pneumatophores (C) and cable roots
(D). aer Aerenchymabar tube, co cortical cell, sc sclereid. Arrows indicate small pores of aerenchyma walls. Bars = 120 mm in A, 200 mm in B, 100 mm in C, 200 mm in D, respectively
Table 2. Size of cortical cells measured from longitudinal sections taken at 0–250 mm (no gas spaces present) and 2–4 cm (with well-developed gas spaces) behind the root tip Root types
Size of cortical cells (mm) 0–250 mm
Feeding roots Anchor roots Pneumatophores Cable roots Average
Size increase 2–4 cm
Horizontal
Vertical
Horizontal
Vertical
Horizontal
Vertical
13.1 ± 1.9 11.3 ± 1.6 16.7 ± 3.2 16.3 ± 2.9 14.3 ± 2.5
9.6 ± 0.9 9.2 ± 1.3 14.8 ± 2.7 13.4 ± 3.3 11.7 ± 2.7
16.7 ± 4.2 15.7 ± 3.9 24.2 ± 6.1 23.9 ± 5.7 20.1 ± 4.5
40.6 ± 10.4 38.1 ± 7.6 48.8 ± 6.8 48.3 ± 10.2 43.9 ± 5.4
1.3 1.4 1.4 1.4 1.4
4.2 4.1 3.3 3.6 3.8
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intercellular spaces were essentially tubular and nontortuous in character (Justin and Armstrong 1987; Jackson and Armstrong 1999). Conard (1905) long ago noted that in Nymphaea the expansion of the lateral cells caused an increase in the size of lacunae and of the root itself. The mature aerenchyma of Nymphaea contains wide lacunae interrupted by diaphragms with small intercellular spaces. Some of the diaphragms appear to be punctured by astrosclereids that would presumably aid longitudinal air flow. As shown in this paper, Sonneratia alba has long aerenchyma tubes without diaphragms. Therefore, sclereids do not serve this function (puncturing the diaphragms) in this species. Besides the absence of diaphragms, this species has numerous small pores on the lateral walls of aerenchyma tubes. The small pores will support the orthographical transport of oxygen against the root axis. We observed sclereids only in the thicker roots (cable roots and pneumatophores) in S. alba. The absence of sclereids in the narrower roots (anchor roots and feeding roots) may mean that the sclereids serve only as mechanical support in the thicker roots. Fig. 5. Root-porosity development in the four root types of Sonneratia alba. Diamonds feeding roots, squares anchor roots, crosses cable roots, triangles pneumatophores. Data points are averages ± 1SD of 10 roots for each given length from the root apex, n = 10
(schizogenous origin). Close to the root apices where there were no intercellular spaces, cortical cells appeared rounded in cross section and were generally arranged in longitudinal files with intimate contact between adjacent files. Intercellular spaces developed because cortical cells became wide in the radial dimension and long longitudinally to the root axis. As the number of longitudinal files of cortical cells did not increase (Table 1), the increase in root diameter with distance from the root apices was mainly caused by cell expansion and the formation of intercellular spaces. Aerenchyma formation only occured in the inner cortex. The outer cortical layers that did not develop intercellular spaces replaced the epidermal layers for protection, and only resembled the exodermis of monocotyledon roots. There were three to four outer layers (Fig. 2D, E) which were darkly stained, presumably a deposition of suberin or lignin. These layers may play a role in preventing or reducing the outward radial diffusion of oxygen (Smirnoff and Crawford 1983; Justin and Armstrong 1987) and may also be the necessary structural framework for aerenchyma formation in mangrove plants. The aerenchyma type found in the present study is of the same general type in Rumex species (dicotyledonous wetland plant) and has been termed “honeycomb” by Justin and Armstrong (1987) and Laan et al. (1989). Honeycomb aerenchyma has been classified as schizogenous by Justin and Armstrong (1987) and Laan et al. (1989), but it is also clear that this type of aerenchyma arises from “differential expansion” (Seago et al. 2000). In longitudinal sections, cortical cells were usually elongated in the plane of the root axis and joined together forming longitudinal files. Consequently, the longitudinal
Root porosity as link to aerenchyma formation Root porosity in all root types of Sonneratia alba showed that these organs contain high percentages of gas spaces (39–60%). This condition was also found in many emergent wetland plant species: Nardus stricta (41.6%), Eriophorum angustifolium (50.6%) (Smirnoff and Crawford 1983); Carex nigra (31.6%), C. otrubae (36.7%), Juncus effesus (36.1%), J. inflexus (53%) (Justin and Armstrong 1987); and Halophila ovalis (37%) (Connel et al. 1999). Other mangrove plants with data taken from seedlings also showed various degrees of root porosity: Avicennia marina (45.7%), Rhizophora stylosa (27.9%), Bruguiera gymnorrhiza (30%), Aegiceras corniculatum (27.4%), Hisbiscus tiliaceus (14.8%), and Excoecaria agallocha (17.8%) (Youssef and Saenger 1996). High porosity is characteristic of plants adapted to growth in anaerobic sediments or flooded conditions, as it enhances the internal movements of gases (Sifton 1945; Armstrong 1979; Justin and Armstrong 1987). The high porosities in S. alba would facilitate the movement of oxygen from the aerial to the underground part of the roots. The porosity is higher in the pneumatophores (60.7%) and cable roots (50.1%) than in anchor roots (41.1%) and feeding roots (38.9%). Oxygen is taken in by pneumatophores at their lenticels which are aerial above the ground. The oxygen is supplied to feeding roots through the pneumatophores and to anchor roots through the pneumatophores and cable roots. The feeding and anchor roots are situated at the end of the oxygen pathway. Therefore, the lower porosity in these two root types may be adequate for oxygen requirements. High porosity in wetland plants is attained at various distances behind the root apex. S. alba attained high porosity within 80–100 mm of the root apex (38–60%). Other wetland plants with schizogenous aerenchyma, such as Rumex palustris, attain high porosity within 5–10 mm (40–
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45%), Carex acuta within 70–80 mm (40–45%) (Laan et al. 1989; Visser et al. 2000a), and Spartina alterniflora and S. anglica within 80–100 mm (25–35%) (Maricle and Lee 2002). The strategy of aerenchyma development in response to anaerobic conditions may involve a tradeoff between maintaining physiological function and reducing tissue respiration. While the aerenchyma system can provide benefits to the plant in terms of facilitating oxygen transport and increasing metabolic efficiency, the formation of aerenchyma also presents certain costs. Loss of cortex tissue can impede other root functions such as water and mineral uptake and transport (Moog 1998). Nonetheless, the aerenchyma in Sonneratia alba develops well and maximally in all root types. The present study revealed that this plant has developed the structural adaptation in its roots as an adaptation to its anaerobic habitat. Acknowledgements We thank Prof. Tokushiro Takaso, Research Institute for Humanity and Nature, Kyoto, and the staff of Iriomote Station, Tropical Biosphere Research Center, University of Ryukyus, for their great support in our field research; Dr. Qiang Sun for helpful comments and criticism on the manuscript. We also thank Kazutaka Kobayashi, Takahisa Tanaka, Youichi Hasegawa, Masanori Seki, and Hiroaki Terasawa for their field-sampling assistance.
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