Water Uptake and Structural Plasticity Along Roots of a Desert Succulent During Prolonged Drought
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Plant, Cell and Environment (1998) 21, 705–713 ORIGINAL ARTICLE OA 220 EN Water uptake and structural plasticity along roots of a desert succulent during prolonged drought G. B. NORTH1 & P. S. NOBEL2 1Department of Biology, Occidental College, Los Angeles, CA 90041, USA, and 2Department of Biology, University of California, Los Angeles, CA 90095–1606, USA ABSTRACT drought (Szarek et al. 1973; Nobel 1988; Ehleringer et al. 1991). Such a recovery of shoot function depends on Desert succulents resume substantial water uptake within renewed water uptake by the roots. In this regard, the roots 1–2 d of the cessation of drought, but the changes in root of long-lived species in generally unproductive habitats, structure and hydraulic conductivity underlying such such as desert succulents, tend to exhibit plasticity, which recovery are largely unknown. In the monocotyledonous helps maximize the uptake of intermittently available leaf succulent Agave deserti Engelm. substantial root mor- resources such as water (Grime 1994). Such plasticity can tality occurred only for lateral roots near the soil surface; be structural, for example the proliferation of lateral roots in nearly all main roots were alive at 180 d of drought. New response to a pulse of water (Fitter 1994; Dubrovsky, North main roots were initiated and grew up to 320 mm at soil & Nobel 1997), or physiological, for example an increase in water potentials lower than – 5·0 MPa, utilizing water the rate of water or nutrient uptake by existing roots from the shoot. The hydraulic conductivity of distal root (Jackson, Manwaring & Caldwell 1990). regions decreased 62% by 45 d of drought and 70% there- Agave deserti, a perennial monocotyledonous succulent after. After 7 d of rewetting, root hydraulic conductivity native to the Mojave and Sonoran deserts, can endure a was restored following 45 d of drought but not after 90 and year without rainfall (Nobel 1976). The hydraulic conduc- 180 d. The production of new lateral roots and the tivity of its root system can decrease by a factor of 105 renewed apical elongation of main roots occurred 7–11 d during a 6-month drought (Schulte & Nobel 1989), after rewetting following 180 d of drought. Hydraulic con- because of decreases in the hydraulic conductivity of indi- ductivity was higher in the distal region than at midroot vidual roots, in the conductivity of gaps that occur between and often increased again near the root base, where many roots and soil, and especially in the conductivity of the soil endodermal cells lacked suberin lamellae. Suberization itself (Nobel & Cui 1992). In addition, decreases in water and xylem maturation were influenced by the availability uptake can result from the death and abscission of lateral of moisture, suggesting that developmental plasticity along roots (Huang & Nobel 1992). Yet A. deserti resumes stom- a root allows A. deserti to capitalize on intermittent or atal opening within 12 h of watering after a drought of heterogeneous supplies of water. 5 months in the field (Nobel 1976), and its succulent leaves recover nearly 30% of their predrought thickness in 24 h Key-words: Agave deserti; endodermis; hydraulic conductiv- (Schulte & Nobel 1989). The structural and physiological ity; root development; xylem. characteristics of the root system that permit such shoot recovery were investigated for A. deserti during an INTRODUCTION imposed drought of 6 months. The primary goal was to assess the loss of root function during prolonged drought A trade-off can exist between the ability of a root system to and to determine whether new root growth was essential tolerate drought and its ability to respond quickly to brief or for renewed water uptake when the soil was rewetted. Root intermittent rainfall. Certain root properties associated with response to drought and rewetting have been examined for drought endurance, such as heavily suberized endodermal A. deserti in the laboratory and the field, but these studies and exodermal layers or periderm (Stasovski & Peterson were based on shorter and more sudden drying regimens 1993; North & Nobel 1995) and the abscission of fine (e.g. Nobel & Sanderson 1984) in which root systems had lateral roots (Huang & Nobel 1992), decrease water uptake not undergone long-term structural changes. by a root system. Yet desert succulents, several of which Three hypotheses guided the investigation. One, the rel- can endure 2–3 years without rainfall (Szarek, Johnson & atively long-lived main roots (arising from the stem base) Ting 1973; Nobel 1988), can resume stomatal opening and of A. deserti can survive a drought of 6 months, aided by carbon fixation within 1–2 days after the cessation of the import of water from the succulent shoot but at the cost of greatly reduced root hydraulic conductivity. Two, the Correspondence: Park S. Nobel. Fax: 310 825 9433; e-mail: psno- roots exhibit plasticity in both structure and hydraulic con- [email protected] ductivity; specifically, the distal region (including the root © 1998 Blackwell Science Ltd 705 706 G. B. North and P. S. Nobel tip) is less highly suberized and lignified than the proximal Tissues external to the stele were removed from a 10 mm region and consequently has higher conductivity. And length of the proximal end of a root segment, and the three, substantial new root growth after rewetting is exposed stele was inserted into a 10 mm section of Tygon required to restore the hydraulic conductivity of the root tubing attached to a glass capillary (internal diameter system to its predrought level. With regard to all three 0·8 mm) that was half-filled with water. A silicone and hypotheses, the possible water-uptake redundancy in the brass compression fitting (Lopez & Nobel 1991) was root system of A. deserti must be considered, as the water tightened around the tubing to prevent leaks from around needed for shoot recovery may be supplied by relatively the stele. To provide a waterproof seal, dental impression few roots or by root regions with sufficiently high material (polysiloxane) and two coats of acrylic copoly- hydraulic conductivity. mer (Nobel, Schulte & North 1990) were applied at the junction between the tubing and the stele as well as at the distal cut end of midroot and basal segments before MATERIALS AND METHODS immersion of the segment in distilled water. Water flow Plant material through the root was induced by applying a negative pres- sure of 20–50 kPa to the open end of the capillary. Thirty plants of Agave deserti Engelm. (Agavaceae), Pressure was regulated with a needle valve and monitored collected from Agave Hill at the University of California with a PS309 digital manometer (Validyne, Northridge, ° ′ 3 –1 Philip L. Boyd Deep Canyon Research Center (33 38 N, CA, USA). When the volumetric flow rate (QV, m s ) 116°24′ W, 820 m) 8 km south of Palm Desert, California, became constant at a given pressure (P, MPa), usually –1 –1 were grown in field soil in a glasshouse at the University of within 10 min, LP (m s MPa ) was determined as fol- California, Los Angeles. Plants received a mean total daily lows (Nobel et al. 1990): –2 –1 photosynthetic photon flux of 38 mol m d (80% of ∆ ∆ ambient solar radiation), with daily maximum/minimum LP =( QV/ P)(1/A) (1) air temperatures of ≈ 28 °C/16 °C. Soil water potential where A (m2) is the root surface area, calculated from root Ψ ( soil), as determined gravimetrically using a moisture- length and radius. Crystal violet dye was added at a con- release curve for the field soil (Young & Nobel 1986), was centration of 50 mg kg–1 to the immersion solution so that maintained above – 0·3 MPa by watering twice weekly leaks could be detected; if the dye appeared in the capil- with 0·1-strength Hoagland’s solution. Plants were lary, the measurement was disregarded. Axial conduc- 0·20–0·32 m tall with 8–14 unfolded leaves and 20–35 tance measured on 20 mm segments open to solution at main roots arising from nodes at the base of the stem just the distal end was always much greater than LP for intact below the leaf bases. or sealed segments, suggesting that the stele was not To distinguish between existing roots and new root crimped by the compression fitting, consistent with growth, 1 month before experiments entire root systems microscopic inspection. were immersed for 10 min in an aqueous solution of neutral To measure axial (xylem) conductance, the waterproof red dye (3-amino-7-dimethylamino-2-methylphenazine end-seals were removed with a razor blade from midroot hydrochloride, 500 g m–3; Schumacher et al. 1983) to stain segments and distal root segments were trimmed by 10 mm the existing roots. Plants were then placed in 0·50 m long × at the tip end to expose cut xylem vessels to the immersion 0·35 m wide × 0·15 m deep containers of soil from Agave solution. The cut end of the segment (about 1 mm) was Hill and watered twice weekly for 30 d before water was immersed in 100 mol m–3 potassium chloride to reduce withheld. Fifteen days after cessation of watering, to blockage (Sperry 1986). QV was measured as for LP and reduce temperature gradients the containers were insulated was used to calculate the root axial conductance per unit 4 –1 –1 on all sides with sheets of Styrofoam 20 mm thick and the pressure gradient (Kh, m s MPa ): soil was covered with Styrofoam pellets to a depth of ∆ 20 mm; the plants received no further water for up to 180 d. Kh = QV/( P /l) (2) Ψ At 45 d of drying, soil differed according to soil depth where the pressure drop ∆P was applied along the length l because of condensation on the sides and the bottom of the (m) of the root segment (Gibson, Calkin & Nobel 1984).