AOBPreview originally published online on October 6, 2007
Annals of Botany 2007 100(7):1431-1439; doi:10.1093/aob/mcm239
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Cortical Aerenchyma Formation in Hypocotyl and Adventitious Roots of Luffa cylindrica Subjected to Soil Flooding
1 National Institute of Crop Science, 2-1-18 Kannondai, Tsukuba, Ibaraki, 305-8518, Japan
2 Biotron Institute, Kyushu University, 6-10-1 Hakozaki, Fukuoka, 812-8581, Japan
3 Department of Plant Resources, Faculty of Agriculture, Kyushu University, 111 Harumachi, Kasuya, Fukuoka, 811-2307, Japan
* For correspondence. E-mail shimamu{at}affrc.go.jp
Received: 4 June 2007 Returned for revision: 10 July 2007 Accepted: 2 August 2007 Published electronically: 6 October 2007
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Background and Aims: Aerenchyma formation is thought to be one of the important morphological adaptations to hypoxic stress. Although sponge gourd is an annual vegetable upland crop, in response to flooding the hypocotyl and newly formed adventitious roots create aerenchyma that is neither schizogenous nor lysigenous, but is produced by radial elongation of cortical cells. The aim of this study is to characterize the morphological changes in flooded tissues and the pattern of cortical aerenchyma formation, and to analyse the relative amount of aerenchyma formed.
Methods: Plants were harvested at 16 d after the flooding treatment was initiated. The root system was observed, and sections of fresh materials (hypocotyl, tap root and adventitious root) were viewed with a light or fluorescence microscope. Distributions of porosity along adventitious roots were estimated by a pycnometer method.
Key Results: Under flooded conditions, a considerable part of the root system consisted of new adventitious roots which soon emerged and grew quickly over the soil surface. The outer cortical cells of these roots and those of the hypocotyl elongated radially and contributed to the development of large intercellular spaces. The elongated cortical cells of adventitious roots were clearly T-shaped, and occurred regularly in mesh-like lacunate structures. In these positions, slits were formed in the epidermis. In the roots, the enlargement of the gas space system began close to the apex in the cortical cell layers immediately beneath the epidermis. The porosity along these roots was 11–45 %. In non-flooded plants, adventitious roots were not formed and no aerenchyma developed in the hypocotyl or tap root.
Conclusions: Sponge gourd aerenchyma is produced by the unique radial elongation of cells that make the expansigeny. These morphological changes seem to enhance flooding tolerance by promoting tissue gas exchange, and sponge gourd might thereby adapt to flooding stress.
Key words: Aerenchyma, Luffa cylindrica, primary cortex, flooding, oxygen, adventitious root, hypocotyl, porosity
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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When soil is flooded, the rhizosphere quickly reaches oxygen shortage conditions because of oxygen consumption during the early stages of flooding, not only by plant roots but also by soil micro-organisms. Although this environment is generally disadvantageous to plant growth, hygrophytes and some mesophytes can adapt to these conditions. In these plants, aerenchyma (tissue with much enlarged gas space) develops in the petioles, stems and roots, and enhances transport of atmospheric and photosynthetic oxygen to flooded tissues, thereby preventing serious damage to root organs (Armstrong, 1979; Dacey, 1980; Drew et al., 1985; Drew, 1997). On the other hand, many mesophytes have little ability to develop aerenchyma so, if the soil becomes flooded, their roots may become oxygen starved and damaged (Smirnoff and Crawford, 1983; Justin and Armstrong, 1987; Laan et al., 1989). Therefore, aerenchyma formation is thought to be one of the important morphological adaptations to hypoxic stress.
Two main types of cortical aerenchyma in stems and roots can be distinguished by their process of formation: lysigenous and schizogenous aerenchyma (Jackson and Armstrong, 1999; Evans, 2003; Visser and Voesenek, 2004; Seago et al., 2005). The former is created through cell disintegration (death) in the primary cortex of adventitious roots, as in rice (Justin and Armstrong, 1991), maize (Drew et al., 1979, 1981) and wheat (Huang et al., 1997), whereas the latter is formed by the separation of cells from each other, often accompanied by cell divisions and normal expansion as in Rumex species (Laan et al., 1989; Jackson and Armstrong, 1999; Colmer et al., 2004). The anatomical and morphological formation of both types has been reported in detail. In particular, much research has been done on the regulation of lysigenous aerenchyma formation using the roots of maize (Drew, 1997; Gunawardena et al., 2001) and rice (Kawai et al., 1998). However, another type of cortical aerenchyma was described in roots of Jussiaea (now Ludwigia) species by Martins (1866) and Schenck (1889) >100 years ago. Some Ludwigia species have pneumatophores (respiratory roots) that grow vertically upward and emerge above the water surface as in mangrove plants (Hartsema, 1927; Sculthorpe, 1967). The intercellular gas spaces are produced by radial elongation of living, thin-walled primary cortical cells. These aerenchymatous tissues are composed of a regular meshwork of rectangular spaces, and are produced in concentric layers in transverse sections of the roots (Martins, 1866; Schenck, 1889; Ellmore, 1981). The elongated cells appear T-shaped in longitudinal sections (Haberlandt, 1914). Although the variation is different from that of Ludwigia, recently intercellular gas spaces have been shown to be produced by primary cortical cell elongation in adventitious roots of the wetland plant Pontederia cordata (Seago et al., 2000) and is termed ‘expansigenous aerenchyma’ by Seago et al. (2005).
Sponge gourd (Luffa cylindrica, Cucurbitaceae) is an annual vegetable upland crop that originates in India and southern Asia, and is distributed mainly in tropical to warm-temperate areas. Compared with bitter melon (Momordica charantia), this species is flood tolerant, but its morphological changes in response to flooding stress have not been examined (Liao and Lin, 1996). In Taiwan, yield of bitter melon is increased by grafting with Luffa spp., which allows bitter melon to survive in flooded soils (Palada and Chang, 2003). In sponge gourd, it was found that the primary cortical tissues of newly formed adventitious roots under flooding created an aerenchyma that was neither schizogenous nor lysigenous, but took the form of elongated cortical aerenchyma. This aerenchyma is composed of cells that appear T-shaped in longitudinal sections. According to Jost (1887), intercellular gas spaces are created by T-shaped cells in roots of Luffa amara (now L. acutangulus).
T-shaped cells that are secondary tissues derived from a phellogen are also observed in flooded stems of Ludwigia (Schenck, 1889, see the English text in Arber, 1920), and the lacunate tissues seem to be similar to elongated primary cortical aerenchyma. However, the origin of the lacunate tissues in the stem of Ludwigia is strikingly different from that of aerenchyma observed in sponge gourd. Recently, morphological observations of T-shaped cells derived from a phellogen were reported in the root and stem of Decodon species (Little and Stockey, 2003, 2006) and Lythrum salicaria (Stevens et al., 1997), but there was no detailed observation of T-shaped cells derived from primary cortical cells. Ellmore (1981) described elongated cortical aerenchyma in mature pneumatophores of Ludwigia, but did not report how lacunae were created at an early stage; therefore, an investigation has been carried out to determine the developmental processes of this type of aerenchyma. In addition, it was found that such tissues were composed of radially elongated primary cortical cells in flooded hypocotyl of sponge gourd, but not of T-shaped cells. Here, the morphological changes in flooded tissues and the pattern of cortical aerenchyma formation are described for sponge gourd, and the relative amount of aerenchyma is analysed.
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MATERIALS AND METHODS |
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Plant material and growth conditions
Seeds of Luffa cylindrica Roem. (long fruit type) were germinated in the dark (25 °C) on filter paper soaked with deionized water for a few days. The germinated seeds were sown in low-humic andosols without chemical fertilizer in plastic pots of 11 cm diameter x 14 cm height (one seed per pot), and were covered by 2 cm of soil. The plants were grown in a growth cabinet under artificial light (25 °C, 14 h light/10 h dark, 590 µmol m–2 s–1). Sixteen days after sowing, some pots were placed inside 4 L tanks (one pot per tank) and the plants were grown under continuously flooded conditions, with the water level maintained 1–2 cm above the soil surface. The remaining plants were used as non-flooded controls. Thirty-two days after sowing the plants were harvested for anatomical observation and measurement of root porosity.
Sampling and cortical tissue observations
After washing off the soil, the root systems of flooded and non-flooded plants were compared. Stem (hypocotyl, 5–10 mm above the soil surface), tap root (50 mm below the base) and adventitious root (80 mm behind the root tip in flooded plants only, because there was no adventitious root in the non-flooded plants) were sampled. Transverse or longitudinal sections (100–400 µm in thickness) of fresh materials were cut on a plant microtome (MTH-1, Nippon Medical & Chemical Instruments Co. Ltd, Osaka, Japan) or a cryostat (CM1100, Leica Microsystems, Wetzlar, Germany), and then were stained with 0·05% toluidine blue O (w/v) or aceto-carmine. The sections were viewed with a light microscope (Eclipse 80i, Nikon Co. Ltd, Tokyo, Japan). For checking suberization of aerenchymatous cell walls, some sections of adventitious roots were stained for 1 h with 0·1% berberine hemisulfate (w/v) and subsequently for 30 min with 0·5% aniline blue (w/v), and finally for several minutes with 0·1% FeCl3 (w/v) in 50% glycerine (v/v) at room temperature (Brundrett et al., 1988). The sections were viewed with a fluorescence microscope (Axioskop2 plus, Zeiss, Oberkochen, Germany) using an ultraviolet filter set (excitation filter BP 365, dichroic mirror FT 395, barrier filter LP 397, Zeiss, Oberkochen, Germany).
Observation of surfaces of flooded hypocotyl and adventitious root
The surfaces of flooded hypocotyl and adventitious root were stained with 0·05% toluidine blue O and observed with a stereoscopic microscope (MZ16, Leica Microsystems, Wetzlar, Germany).
Pattern of cortical aerenchyma formation in adventitious root
Adventitious roots (>100 mm in length) were sampled in flooded plants. Transverse or longitudinal sections from the root tip to the base were cut on the plant microtome and observed under a light microscope (see above).
Measurement of adventitious root porosity
Distributions of porosity along adventitious roots (>100 mm in length) were estimated by a pycnometer method modified from Jensen et al. (1969). This method quantifies porosity as the percentage of root volume occupied by gas. Internal gas within the tissues was removed by evacuation under low pressure in deionized water instead of grinding the plant material to degas it in liquid N2 (Sojka, 1988; Bacanamwo and Purcell, 1999; Fan et al., 2003). The porosity of the root tissue was calculated as follows:
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Adventitious roots were divided into three parts (0–30, 30–60 and 60–90 mm behind the root tip). Three roots were used per replicate.
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RESULTS |
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Root system changes under flooded conditions
Under non-flooded conditions, the root system consisted of a tap root and lateral roots, and no adventitious roots appeared from the hypocotyl (Fig. 1A). In contrast, the adventitious roots of the flooded plants quickly and vigorously emerged over the soil surface at 4 d after initiation of flooding (Fig. 1B). At 16 d after flooding, thick white adventitious roots were formed as floating roots (Fig. 1C). A considerable part of the root system consisted of new adventitious roots that developed from the base of the hypocotyl, although the death of the tap root and lateral roots was not observed (Fig. 1D).
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Morphological changes of flooded tissues in transverse sections
In non-flooded plants, morphological changes such as aerenchyma formation were not observed in the hypocotyl or tap root: their cortical cells were tightly packed (Fig. 2A, B). Under flooding, the cortical cells of the hypocotyl and adventitious root elongated radially in transverse sections, and they extended and somewhat enlarged the intercellular gas spaces, although the inner cortical cell packing formation remained intact and hence there was no aerenchyma (Fig. 2C, E). Adventitious root had numerous and large air spaces as compared with the hypocotyl. Even under flooded conditions, aerenchyma did not form in the cortex of the tap root: cells remained closely packed (Fig. 2D). Nuclei were observed in elongated cortical cells (Fig. 2F).
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Slits in the surfaces of flooded hypocotyl and adventitious root
The formation of wide slits was observed on submerged parts of the hypocotyl (Figs 2C and 3A). The slits were also formed in the adventitious root surface (Fig. 2E). Although the slits were not observed in the surface of young root tissue near the tip (Fig. 3B), a number of narrow slits were found at a slightly more advanced stage (Fig. 3C) than shown in Fig. 3B, and the slits seen in the mature adventitious root were visible externally (Fig. 3D).
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Non-suberization of aerenchymatous cell walls
The elongated aerenchymatous cell walls of flooded adventitious roots, stained by a berberine–aniline blue procedure (Fig. 4A), did not show blue-white to blue fluorescence of suberin with fluorescence microscopy at 365 nm excitation (Fig. 4B), which indicated that the walls did not suberize.
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Elongated cortical cells in longitudinal sections
Elongated cortical cells had obvious different shapes in hypocotyl and adventitious roots under flooded conditions. Many cells simply and radially elongated outward in the hypocotyl (Fig. 5A). In adventitious roots, the elongated cortical cells were clearly T-shaped, and occurred regularly in mesh-like lacunate structures (Fig. 5B, C).
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Pattern of cortical aerenchyma formation in adventitious roots
No aerenchyma was created in transverse section near the adventitious root tip (Fig. 6A), and cortical cells appeared elongated along the root axis in longitudinal section (Fig. 6D). After elongation in the longitudinal direction, the first intercellular gas spaces were produced by radial elongation of cortical cells near the epidermis at 40 mm from the root tip (Fig. 6B), to form the branches observed at mid-cell body in longitudinal section (Fig. 6E). However, some cortical cells bordering the epidermis did not elongate. When the cortical cells began to elongate, the epidermal cells did not divide or expand, so that slits were formed in the surface of adventitious roots (Fig. 6B). The development of gas spaces was increased along the entire length of the adventitious roots, with some cortical cell layers elongated and numerous gas spaces formed at 60 mm from the tip (Fig. 6C, F).
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Porosity of adventitious roots of plants grown under flooded conditions
Only adventitious roots that grew under flooded conditions were examined because adventitious roots did not arise from the stem bases of non-flooded plants. The porosity of the adventitious root segments 0–30 mm behind the tip was only 11% (Fig. 7). In the segments 30–60 mm from the tip, however, the porosity rapidly increased to 34%, reaching 45% in segments 60–90 mm from the tip (Fig. 7).
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DISCUSSION |
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In various herbaceous dicots and woody species, swelling and formation of hypertrophic lenticels in the submerged portions of the stems have been reported (Kawase, 1974; Wample and Reid, 1979; Kozlowski, 1997; Núñez-Elisea et al., 1999). These morphological changes seem to enhance flooding tolerance by promoting tissue gas exchange. Lenticels are the first entry points for transporting oxygen to hypoxic roots, and the oxygen is then available to support root elongation and functioning. Experimental blocking or disruption of hypertrophic lenticels at the bases of L. salicaria (Stevens et al., 2002), soybean (Shimamura et al., 2002, 2003), Salix viminalis (Jackson and Attwood, 1996) and some woody plants (Armstrong, 1968) has been shown to inhibit oxygen transport to the roots and plant growth. Therefore, formation of hypertrophic lenticels enables these plants to survive under flooded conditions.
The present experiments show that flooded sponge gourd plants may have similar adaptations to promote oxygen transport. After flooding, slits were actively formed on the base of the hypocotyl by elongation of cortical cells (Figs 2 and 3). The slits are not lenticels as they are not derived from secondary tissue, but, like hypertrophic lenticels, they probably also serve as entry points for atmospheric oxygen. In addition, some adventitious roots floated on the surface of the water (Fig. 1), and slits were widely formed on the portions of the root that had formed aerenchyma (Figs 2, 3 and 6), so the oxygen may directly penetrate into the aerenchyma of roots. Floating adventitious roots with aerenchyma have also been observed in flooding-tolerant Sesbania aculeata (Scott and Wager, 1888). If the slits of the hypocotyl are submerged by the water surface rising, floating adventitious roots may have a very important role in the entrance of atmospheric oxygen. Sponge gourd seems to have several entry points of oxygen and can adapt to flooding stress. The detailed process of the epidermal slits in the hypocotyl and adventitious root was not investigated in this study. It is not known whether epidermal cell walls become loose and the cells separate naturally before cortical cells start to elongate radially or whether the epidermis is torn by the radial elongation power of cortical cells, so further research is needed.
The pattern of aerenchyma formation observed in sponge gourd is very interesting. Cortical cells are usually elongated along the root axis, but radial elongation was observed in adventitious roots (Fig. 5B, C). Therefore, the cells were T-shaped in longitudinal sections (Figs 5B, C and 6E, F). In sponge gourd, the cortical cells near the epidermis began radial elongation under flooded conditions in adventitious roots and became aerenchymatous cells at an early stage (Fig. 6B, E), and then the cells (indicated by arrows in Fig. 6E) just bordering T-heads of aerenchymatous cells probably began to extend (Fig. 6F). Schenck (1889) also observed this pattern in adventitious roots of Ludwigia species. However, aerenchymatous cells were not T-shaped in the hypocotyl (Fig. 5A), and their structures resembled palisade tissues of leaves. In contrast to adventitious roots, longitudinal sections showed that the elongation of cortical cells probably did not occur along the stem axis. It is very interesting that cortical cells expand radially in both hypocotyl and adventitious root in transverse sections, and that they are shaped differently in tangential sections: T-shaped in the adventitious root and non-T-shaped in the hypocotyl. There are thus several shapes of elongated aerenchyma cells. From all the results, it is clear that cortical aerenchyma of sponge gourd greatly resembles expansigenous aerenchyma which was demonstrated by Seago et al. (2005). However, sponge gourd has the unique radial elongation of cells (Figs 5 and 6) that makes the expansigeny differ slightly from what was illustrated by Seago et al. (2005). Furthermore, the aerenchyma of sponge gourd does not structurally resemble lysigenous or schizogenous aerenchyma but rather secondary aerenchyma. Secondary aerenchyma is also lacunate tissue that is produced by the radial elongation of cells derived from a phellogen. The specialized T-shaped cells originated from primary cortical cells in the present study, but were formed from a phellogen in the flooded stem and root of Lythraceae (Stevens et al., 1997; Lempe et al., 2001; Little and Stockey, 2003, 2006) and Ludwigia plants (Schenck, 1889; Angeles, 1992). Although their origin is obviously different, both types of aerenchyma are composed of clear, soft and living cells with thin walls (Figs 2F and 4).
Much research has been focused on the regulation of lysigenous aerenchyma formation in the cortex. For example, aerenchyma formation in rice begins with the programmed cell death of the mid cortex (Kawai et al., 1998), and is induced by ethylene or by nutrient shortage in maize (Drew, 1997; Gunawardena et al., 2001; Fan et al., 2003). In contrast, the physiological process of elongated cortical aerenchyma formation is not known at all. Ellmore (1981) found that ethylene was not detected in gas taken from pneumatophores of Ludwigia peploides, so there are probably basic physiological differences between lysigenous aerenchyma and elongated cortical aerenchyma.
In general, new organs such as adventitious roots induced by flooding have aerenchymatous tissues, but mature organs appear to show a different response. The cortex most probably had completed differentiation in the segments of the hypocotyl (5–10 mm above the soil surface) and tap root (50 mm below the base) before the flooding treatment, but, after flooding, cortical cells could elongate radially in the hypocotyl, while they could not elongate in the tap root (Fig. 2). What determines the elongation or non-elongation of mature cortical cells is unknown, and further research is needed to elucidate the regulation of this aerenchyma formation.
In herbaceous dicot species, research on elongated cortical aerenchyma has been focused on the roots of Ludwigia species. The present study, however, revealed hypocotyl and adventitious roots with this character even in the upland plant sponge gourd. Although the formation of this type of aerenchyma is limited to a few species at present, several herbaceous dicot plants with the ability to form aerenchyma will probably be found in the future. Cucurbitaceae include very important vegetable crops (cucumber, melon, pumpkin, etc.) that are not tolerant to flooding. The cucumber has no ability to form aerenchyma in roots under hypoxia, and its root porosity is <8% (Van Noordwijik and Brouwer, 1993) as compared with 11–45% in sponge gourd (Fig. 7). Oxygen transport via aerenchyma is demonstrated by using an 18O2 tracer (Dacey and Klug, 1982) or an oxygen microelectrode (Armstrong et al., 2000) in some wetland plants, and these methods will be very useful in confirming the role of aerenchyma of sponge gourd in future studies. If elongated cortical aerenchyma in sponge gourd is useful for flooding tolerance, this character may become an important genetic resource in Cucurbitaceae vegetable crops.
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