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. 2006 Mar;97(3):469–474. doi: 10.1093/aob/mcj054

Parenchyma–Chlorenchyma Water Movement during Drought for the Hemiepiphytic Cactus Hylocereus undatus

PARK S NOBEL 1,*
PMCID: PMC2803650  PMID: 16390846

Abstract

• Background and Aims Hylocereus undatus, a hemiepiphytic cactus cultivated in 20 countries for its fruit, has fleshy stems whose water storage is crucial for surviving drought. Inter-tissue water transfer during drought was therefore analysed based on cell volumes and water potential components.

• Methods In addition to determining cell dimensions, osmotic pressures and water potentials, a novel but simple procedure leading to an external water potential of zero was devised by which cells in thin sections were perfused with distilled water. The resulting volume changes indicated that the parenchyma–chlorenchyma water movement was related to more flexible cell walls in the water-storage parenchyma with its lower internal turgor pressure (P) than in the chlorenchyma.

• Key Results Under wet conditions, P was 0·45 MPa in the chlorenchyma but only 0·10 MPa in the water-storage parenchyma. During 6 weeks of drought, the stems lost one-third of their water content, becoming flaccid. About 95 % of the water lost came from cells in the water-storage parenchyma, which decreased by 44 % in length and volume, whereas cells in the adjacent chlorenchyma decreased by only 6 %; the osmotic pressure concomitantly increased by only 10 % in the chlorenchyma but by 75 % in the water-storage parenchyma.

• Conclusions The concentrating effect that occurred as cellular volume decreased indicated no change in cellular solute amounts during 6 weeks of drought. The ability to shift water from the parenchyma to the chlorenchyma allowed the latter tissue to maintain a positive net CO2 uptake rate during such a drought.

Keywords: Cell dimensions, cell wall, chlorenchyma, CO2 uptake, drought, hydrostatic pressure, Hylocereus undatus, osmotic pressure, parenchyma, water potential, water relations

INTRODUCTION

Inter-tissue water movement can be especially apparent during drought for shoots of desert succulents that have distinct tissues for water storage and for photosynthesis (Nobel, 1988; Gibson, 1996; Smith et al., 1997). For the columnar cactus Carnegiea gigantea and the barrel cactus Ferocactus acanthodes, water loss during drought is much greater from the water-storage parenchyma than from the chlorenchyma due to a decrease in solutes in cells of the water-storage tissue (Barcikowski and Nobel, 1984). Water is also preferentially lost from the water-storage parenchyma instead of the chlorenchyma during drought for the leaf succulent Peperomia magnolieafolia (Schmidt and Kaiser, 1987), the platyopuntia Opuntia ficus-indica (Goldstein et al., 1991a), the epiphyte Tillandsia ionantha (Nowak and Martin, 1997), and 30 other epiphytes (Martin et al., 2004). For such Crassulacean acid metabolism (CAM) plants under wet conditions, internal movement of water between the chlorenchyma and the parenchyma also occurs during 24-hour periods as the osmotic pressure in the chlorenchyma oscillates due to CO2 fixation into organic acids at night and the reformation of polymers during the daytime (Smith et al., 1987; Schulte et al., 1989; Goldstein et al., 1991b; Tissue et al., 1991). Even for C3 and C4 plants without prominent water storage tissue, inter-tissue water transfer is affected by osmotic and hydrostatic pressures as well as by cell wall elasticity (e.g. Zimmermann and Steudle, 1978; Hsiao and Xu, 2000).

Hylocereus undatus, the species considered in the present study, is cultivated in 20 countries for its fruit and is also used as an ornamental (Mizrahi and Nerd, 1999; Nobel and De la Barrera, 2004). It is a slender hemiepiphytic cactus native to dry tropical forests from Mexico to northern South America (Ortíz, 1999; Nobel and De la Barrera, 2004) and exhibits CAM, with stomatal opening predominantly at night (Ortíz et al., 1996; Raveh et al., 1998), leading to daily oscillations in stem thickness (Graham and Nobel, 2005). Its sequential stem segments can develop adventitious roots, so each rooted stem segment can act as an individual unit for water uptake. Water was withheld for up to 6 weeks, a relatively long drought but one that H. undatus can experience in its native habitats (Benzing, 1990; Sanford et al., 1994; Lüttge, 1997). The predicted inter-tissue water movement from the water-storage parenchyma to the adjacent chlorenchyma during drought has not previously been analyzed for cacti or other succulents in terms of components of the water potential together with cellular volume changes. Perfusion of excised sections of H. undatus with distilled water to expose cells of the chlorenchyma and the water-storage parenchyma to a known water potential and waiting for cellular volume changes to cease, a novel but easily executed procedure, revealed much about the hydrostatic and osmotic pressures underlying inter-tissue water transfer of this cactus during drought.

MATERIALS AND METHODS

Plant material

Plants of Hylocereus undatus (Haworth) Britton & Rose (Cactaceae) were grown in 15-cm-diameter pots that were filled to a depth of 12 cm with loamy sand from the north-western Sonoran Desert (Nobel, 1976); the soil had been sieved to remove stones and gravel particles greater than 3 mm in diameter. The plants were maintained with 50 % shading (close to optimal for net CO2 uptake by this species; Raveh et al., 1995) in a temperature-controlled glasshouse with average day/night air temperatures of 32/23 °C (maximum/minimum daily air temperatures of 35/18°C), which are close to optimal for net CO2 uptake by H. undatus (Nobel and De la Barrera, 2002a). The mean relative humidity ranged from 45 % during the daytime to 65 % at night, similar to values in its native habitats (Benzing, 1990; Castillo Martínez et al., 1996).

To provide wet conditions, the plants (one per pot) were watered weekly with 600 mL of 0·05-strength Hoagland solution no. 2 supplemented with micronutrients (Hoagland and Arnon, 1950; Epstein and Bloom, 2005). The soil water potential (ψsoil) in the centre of the root zone (6 cm below the soil surface) was determined with PCT-55 soil thermocouple psychrometers whose output was monitored with an HR-33T dew-point microvoltmeter (Wescor, Logan, USA). ψsoil was −0·24 ± 0·04 MPa (n = 5 plants) at 2 d after watering, −0·34 ± 0·05 MPa at 4 d, and −0·69 ± 0·07 MPa at 7 d after watering (just before routine rewatering), the latter being similar to the stem water potential of H. undatus under wet conditions (Nobel and De la Barrera, 2002b). Drought was induced by ceasing the watering.

To investigate cellular properties of H. undatus related to inter-tissue water movement without complications due to inter-segment water transfer (Nerd and Neumann, 2004), stem segments with no new branches developing on them were used. At the time of the measurements, the segments, which had been planted vertically, averaged 26 cm in length above ground (about 11 cm was below ground), were about 16 months old, and had three ribs averaging 20 mm in depth.

Cell dimensions

Pieces of the ribs 15 mm deep by 15 mm along the stem axis were cut from near mid-stem with a single-edged razor blade and then weighed; to standardize any effects of daily variations in CAM and hence in cell size (Smith et al., 1987), pieces were excised between 1300 and 1500 h. After the stem thickness at 10 mm from the rib crest was determined with calipers, free-hand sections (300–400 µm thick) at that location were made and examined without mounting medium at 100× with a BH-2 phase-contrast microscope (Olympus, Lake Success, USA) using an ocular micrometer to determine lengths of intact cells perpendicular to the stem surface. For each plant, 12 chlorenchyma cells and 12–14 adjacent water-storage parenchyma cells were measured in each of two sections at various times up to 6 weeks after watering. Maximum cell diameters were also determined under wet conditions and after 6 weeks without watering. Nearly all of the water-storage parenchyma cells contained chloroplasts, but their frequency was less than 10 % of that for the chlorenchyma cells.

After applying distilled water to cut sections to create an external water potential of zero, the sections were prepared and microscopically examined as described above. Lengths of approximately ten chlorenchyma cells and ten water-storage parenchyma cells were measured in each section within 150 s. The sections were then perfused with distilled water and surface-blotted with absorbent tissue, a step requiring about 30 s that was repeated five times on each section, after which cellular lengths were again measured from the same region as examined previously (often measuring the same cells). This procedure of perfusing and examining (requiring 5 min total) was repeated six times. Lengths of the chlorenchyma and the water-storage parenchyma cells were then routinely determined for plants under wet conditions (2–4 days after watering) and after perfusion of the thin sections with distilled water for 30 min.

Water relations, net CO2 uptake

To measure the tissue water potential (ψ), paradermal slices of the chlorenchyma (about 1 mm thick × 5 mm wide × 10 mm along the stem axis) or water-storage parenchyma (same slice size) were obtained from the excised stem pieces using a double-edged razor blade. After surface-blotting lightly to remove sap from the cut cells and mucilage, two slices were cut in half lengthwise, placed in the stainless-steel chambers of an SC10C TruPsi thermocouple psychrometer (Decagon Devices, Pullman, USA), and equilibrated for 3–4 h before measuring ψ. To measure the average cellular osmotic pressure (Π), two such slices of chlorenchyma or water-storage parenchyma were squeezed between plastic plates using a vice; the osmolality of the expressed cell sap (collected with a micropipette and immediately placed on an absorbent paper disk 6 mm in diameter) was determined with a Wescor 5500 vapour pressure osmometer and converted to Π at 20 °C using the Van't Hoff relation (Nobel, 2005).

The rate of net CO2 uptake per unit stem area was measured in the glasshouse from 0000 to 0200 h, a time of day when such rates are generally maximal for H. undatus (Nobel and De la Barrera, 2002b), using a LI-6200 portable photosynthesis system (LI-COR, Lincoln, USA). The gas-exchange cuvette was fitted to the flat side of a rib using a rectangular acrylic extension with an opening that was 10 mm wide by 30 mm along the stem axis. The sides of the extension were covered with a foam-rubber gasket to form an airtight seal with a rib's surface near mid-stem.

Data are presented as means ± s.e. (n = number of plants). Statistical significance was tested using Student's t-test.

RESULTS

Stem and cell dimensions

Stem thickness at 10 mm from the rib crest (essentially the middle of a rib) steadily decreased as drought progressed (Fig. 1A). Compared with the first 7 d after watering when the stem thickness averaged 7·76 ± 0·19 mm (n = 18 plants), the decrease was 18 % (P < 0·05) at 28 d without watering and 26 % at 42 d (P < 0·01). Visual observation indicated that the shrinkage was greater for the water-storage parenchyma (which averaged nearly 6 mm in thickness under wet conditions) than for the adjacent chlorenchyma (which totalled about 2 mm for both sides of a rib), a matter that reflected changes in individual cell dimensions (Fig. 1B).

Fig. 1.

Fig. 1.

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(A) Thickness at mid-rib and (B) lengths of chlorenchyma and water-storage parenchyma cells for planted stems of Hylocereus undatus at various times after watering or following rewetting. The time of rewetting is indicated by arrows; dotted lines indicate the time course for parameters after rewetting. Data are means ± s.e. (n = 6 plants).

In particular, the stem sections generally had six layers of chlorenchyma cells on each side of a rib. The length of these cells averaged 161 ± 1 µm (430 cells from n = 18 plants) during the first 7 d after watering, decreasing slightly but significantly at 35 d (P < 0·05) without watering and decreasing overall by 6 % at 42 d (P < 0·01; Fig. 1B). The water-storage parenchyma cells had more rapid and greater changes in length; these cells averaged 209 ± 2 µm (470 cells from n = 18 plants) in length during the first 7 d after watering, became shorter at 14 d (P < 0·01) after watering, and decreased overall by 44 % at 42 d after watering (P < 0·001; Fig. 1B).

Intercellular air spaces, which occupied only about 4 % of the rib volume under wet conditions, became progressively more prominent during drought, especially in the water-storage parenchyma. No significant changes (P > 0·05) in stem length (n = 8 plants) or in maximum diameter of chlorenchyma cells and water-storage parenchyma cells (12 cells from each of n = 8 plants) were noted during the 6 weeks without watering. In particular, maximum cell diameter was 87 ± 1 µm under wet conditions and 85 ± 2 µm after 6 weeks without watering for the chlorenchyma cells and 147 ± 2 µm and 143 ± 2 µm, respectively, for the water-storage parenchyma cells. The excised stem pieces (15 mm wide × 15 mm along stem axis) weighed 1·39 ± 0·03 g (n = 8 plants) under wet conditions and 0·96 ± 0·02 g after 6 weeks without watering (P < 0·001), when the stems were quite flexible, suggesting loss of cellular turgor pressure.

The responses of stem thickness and cell length to rewetting were more rapid than were the changes during drought (Fig. 1). In particular, 7 d after rewetting plants that had not been watered for 35 d, the stem thickness at mid-rib, the chlorenchyma cell length and the length of water-storage parenchyma cells were indistinguishable from values under wet conditions. The half-time for the increases in length of the water-storage parenchyma cells, which had the greatest percentage changes of the three quantities measured, was about 4 d (Fig. 1).

Perfusion with distilled water

The length of both chlorenchyma and water-storage parenchyma cells increased when the stem sections were perfused with distilled water (Fig. 2). In a representative case, the length became maximal at about 20 min for the chlorenchyma cells and 25 min for the water-storage parenchyma cells. The overall cellular increase was then 9 % for the chlorenchyma (P < 0·01) and 24 % for the water-storage parenchyma (P < 0·001; Fig. 2).

Fig. 2.

Fig. 2.

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Representative responses to perfusion with distilled water for the lengths of chlorenchyma and water-storage parenchyma cells in thin sections of excised stem pieces of H. undatus under wet conditions. Data are means ± s.e. (n = 6 sections from one plant).

For six plants (Table 1), the increase in cell length during 30 min of perfusion with distilled water was 16 µm (P < 0·001) for chlorenchyma cells and 50 µm (P < 0·001) for water-storage parenchyma cells. The percentage increase in length averaged 10 % for the chlorenchyma cells and 24 % for the water-storage parenchyma cells (P < 0·001; Table 1).

Table 1.

Length of chlorenchyma and water-storage parenchyma cells of Hylocereus undatus under wet conditions and after exposure of thin sections of excised stem pieces to distilled water

Cell length
Chlorenchyma
 Water-storage parenchyma
Initial (µm) Final (µm) Change (%) Initial (µm) Final (µm) Change (%)
162 ± 1 178 ± 2 9·8 ± 0·3 212 ± 2 262 ± 1 23·6 ± 0·7
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‘Initial’ refers to plants 2–3 d after watering; ‘Final’ refers to the same plants after six perfusion steps with distilled water requiring a total of 30 min.

Data are means ± s.e. (n = 6 plants).

Water potential, osmotic pressure, net CO2 uptake

The water potential (ψ) of the chlorenchyma was indistinguishable from that of the water storage parenchyma under both wet conditions (mean ψ = −0·58 MPa) and dry conditions due to about 6 weeks without watering (mean ψ = −1·15 MPa; Table 2). Under wet conditions, the osmotic pressure (Π) was 0·37 MPa higher for cells in the chlorenchyma than for cells in the water-storage parenchyma (P < 0·001), Π of the chlorenchyma was 0·45 MPa higher than was –ψ (P < 0·001), and Π of the water-storage parenchyma was 0·10 MPa higher than was –ψ (P < 0·05; Table 2). Under dry conditions, Π was indistinguishable between the chlorenchyma and the water-storage parenchyma and also was indistinguishable from –ψ (Table 2).

Table 2.

Water potentials and osmotic pressures for cells in the chlorenchyma and the water-storage parenchyma of stems of H. undatus under wet and dry conditions

Quantity Wet
 Dry
Chlorenchyma Water-storage parenchyma Chlorenchyma Water-storage parenchyma
ψ (MPa) –0·59 ± 0·02 –0·57 ± 0·03 –1·15 ± 0·04 –1·15 ± 0·04
Π (MPa) 1·04 ± 0·03 0·67 ± 0·02 1·14 ± 0·03 1·17 ± 0·03
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‘Wet’ refers to 2–4 d after watering; ‘Dry’ refers to 41–45 d after watering.

Data are means ± s.e. (n = 6 plants).

The maximal rates of net CO2 uptake, determined from 0000 to 0200 h, occurred for stems under wet conditions, 6·22 ± 0·20 µmol m−2 s−1 (n = 8 plants). When water was withheld, these rates decreased (P < 0·001). In particular, the rates were 2·53 ± 0·31 µmol m−2 s−1 at 2 weeks after watering, 1·05 ± 0·20 µmol m−2 s−1 at 4 weeks after watering, and 0·37 ± 0·12 µmol m−2 s−1 at 6 weeks after watering (n = 4 plants).

DISCUSSION

Because neither stem length nor maximum cellular diameter (dimensions parallel to the stem surface) of Hylocereus undatus changed significantly during drought, accompanying changes in cell length perpendicular to the stem surface mainly reflected changes in cell volume. Based on the decreases in length of chlorenchyma cells (6 %) and water-storage parenchyma cells (44 %) and their amounts at mid-stem, 95 % of the water lost during 6 weeks of drought came from the water-storage parenchyma. Again based on cellular dimensions, an overall decrease in stem thickness of 32 % was predicted; the discrepancy of 6 % between the measured (26 %) and the predicted changes in stem thickness was due at least partly to the observed enlargement of the intercellular air spaces during drought. The loss in weight of stem pieces (15 × 15 mm) during 6 weeks after watering was 31 %, consistent with an increase in intercellular air spaces, as the percentage loss was similar to the predicted decrease in stem thickness based on cell length.

The decreases in stem thickness and cell length during 35 d without watering was fully reversed 7 d after rewetting. The five-fold more rapid rehydration than dehydration for stems of H. undatus apparently reflected a greater root water uptake ability than was necessary to support transpiration under wet conditions. Similarly, the leaf succulent Agave deserti has a substantial redundancy with respect to daily water uptake requirements under wet conditions, although the entire root system is required for rapid recovery upon rewetting (Graham and Nobel, 1999). Rapid recharge of shoot water reserves has also been observed for other CAM plants (Reuss and Eller, 1985; North and Nobel, 1994) and is advantageous for epiphytic and hemiepiphytic species growing in limited soil volumes that have only transient periods of water availability (Benzing, 1990; Lüttge, 1997; Martin et al., 2004).

Because the water potential (ψ) and the osmotic pressure (Π) were measured for H. undatus under wet and dry conditions, the turgor pressure (P) can be calculated under both conditions (ψ = P − Π, or P = ψ + Π; Nobel, 2005). A few days after watering, cellular P was −0·59 + 1·04, or 0·45 MPa, in the chlorenchyma but only −0·57 + 0·67, or 0·10 MPa, in the water-storage parenchyma. The lower P in the latter cells suggests that they have less rigid (thinner) cell walls, allowing for the observed major changes in their cell volume during drought. In this regard, the volumetric elastic modulus (ɛ; Nobel, 2005) is three-fold larger for cells in the chlorenchyma than for cells in the water-storage parenchyma of the CAM plants Kalanchoe daigremontiana (Steudle et al., 1980) and O. ficus-indica (Goldstein et al., 1991a, b). After 6 weeks without watering, no detectable turgor pressure existed in the chlorenchyma or the water storage parenchyma, as ψ was then indistinguishable from –Π, consistent with the flaccid nature of the stems at that time.

The decrease in cell length and hence in cell volume during drought concentrated the solutes in the cells. For instance, after 6 weeks without watering, the volume of the chlorenchyma cells decreased by 6 % and their osmotic pressure increased by 10 % (versus a predicted increase of 7 % based on an inverse relationship between cell volume and Π; Nobel, 2005). For the larger changes in the water-storage parenchyma, the cellular volume decreased by 44 % during 6 weeks without watering and Π increased by 75 % (versus a predicted increase of 78 %). Thus, an inverse relationship existed between cell volume and osmotic pressure, suggesting that little change occurred in the absolute amount of solutes per cell in the chlorenchyma and the water-storage parenchyma of H. undatus during this 6-week period after watering. This agrees with results for Opuntia basilaris (Barcikowski and Nobel, 1984) but contrasts with results for other cacti, where longer droughts of 4–18 months are accompanied by a decrease in the amount of solutes per cell in the water-storage parenchyma for Carnegiea gigantea, Ferocactus acanthodes (Barcikowski and Nobel, 1984) and Opuntia ficus-indica (Goldstein et al., 1991a). For H. undatus, whose roots exist in a very limited soil volume under natural conditions, substantial osmotic adjustments may not occur during the rapid drying of the soil.

As the stems of H. undatus began to lose water during drought, the ostensibly more rigid cell walls of the chlorenchyma cells apparently caused a greater decrease in P than for cells in the water-storage parenchyma. The accompanying major decrease in the water potential in the chlorenchyma cells of H. undatus caused water to enter from the water-storage parenchyma (whose P decreased only slightly but whose Π increased substantially as cellular water was lost). This extended the period when the chlorenchyma could be metabolically active, both for net CO2 uptake and for the internal recycling of endogenously produced CO2 (CAM ‘idling’; Ting, 1985).

Perfusing tissue slices of H. undatus from plants under wet conditions (ψstem = −0·58 MPa) with distilled water and waiting until cellular volumes had ceased changing (within 30 min), a simple technique that apparently has not been previously described for such studies of plant water relations, presumably led to external and internal water potentials close to zero. Considering the 10 % increase in length and ostensibly in volume for the chlorenchyma cells, their internal osmotic pressure would decrease from 1·04 to 0·94 MPa, assuming no leakage of solutes. Because ψ was assumed to be zero after perfusion of the tissue sections with distilled water, P then equalled Π and so was 0·94 MPa for the chlorenchyma cells, which represents an increase of 0·94 − 0·45 or 0·49 MPa over the value for chlorenchyma cells from plants under wet conditions. For the water-storage parenchyma and again assuming no loss of solutes, the 24 % increase in cell length upon perfusion with distilled water reduced Π from 0·67 to 0·51 MPa, so P was then 0·51 MPa, which was an increase of 0·41 MPa over the value for cells from plants under wet conditions. The similar increase in P in the chlorenchyma cells (0·49 MPa) and the water-storage parenchyma cells (0·41 MPa) was accompanied by a 2·4-fold greater increase in length and hence in water uptake by the water-storage parenchyma cells. Conversely, more water would be released from the water-storage parenchyma to the chlorenchyma as ψ decreased during drought.

In conclusion, cells in the water-storage parenchyma of H. undatus evidently had a lower ɛ for their cell walls, so a greater loss of water for a given decrease in P would occur compared with the chlorenchyma cells. Cells of the water-storage parenchyma contained fewer chloroplasts and presumably had thinner cell walls, so not only would they be metabolically cheaper for H. undatus to produce than were chlorenchyma cells, but also they would be better suited to withstand large decreases in water content during drought. Therefore, this hemiepiphytic cactus could utilize nearly one-third of the water in its stem during 6 weeks of drying with little change in the volume of the chlorenchyma cells, which are maintained with a positive turgor pressure throughout the entire period. The maximal rate of net CO2 uptake, which was 6·2 µmol m−2 s−1 under wet conditions, decreased by 59 % at 2 weeks after watering, similar to a drop of 62 % for H. undatus in a slightly more rapidly draining sandy soil (Nobel and De la Barrera, 2002b, 2004). Although the maximal rate of net CO2 uptake decreased by 94 % during the 6-week drought, the parenchyma–chlorenchyma water movement for H. undatus extended the period for at least some positive net CO2 uptake and for internal recycling of CO2 produced by respiration.

Acknowledgments

I thank Kevin Coniff for the plant material, Adrienne Hou for plant maintenance, and Drs Erick De la Barrera, Eric A. Graham and Gretchen B. North for useful discussions. Financial support was provided by the UCLA–Ben Gurion University Program of Cooperation through the generous gift of Sol Leshin and by Research Grant No. IS-3282-01R from BARD, the United States–Israel Binational Agricultural Research and Development Fund.

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