Morphological and physiological
characteristics of tomato roots associated
with potassium-acquisition efficiency
Jianjun Chen
*,1, Warren H. Gabelman
Department of Horticulture, University of Wisconsin, 1575 Linden Drive, Madison, WI 53706, USA
Accepted 17 May 1999
Abstract
Acquisition of potassium (K) by roots plays the most important role in K efficiency of plants. However, limited information is available on morphological and physiological characteristics of roots in response to low-K stress. In this report, two tomato strains representing two distinct phenotypes of K-acquisition efficiency were studied using a sand±zeolite culture system. One was apparently morphological, manifested by rapidly proliferating root length and concomitantly greater root absorbing surface areas to capture K. The other was physiological, demonstrated by high net K-influx coupled with low pH around root surfaces. The high K-influx, in association with high root cation-exchange capacity for K, brought about significant amounts of K accumulation in apoplast and on root surfaces, and K depletion in a zone between 1 and 3 mm from root surfaces. The accumulated K, in turn, could serve as a K pool favorable to K uptake. Results from this study indicate that soil K deficiency has been a selective force that leads plants to evolve characteristics for the efficiency of K-acquisition.#2000 Elsevier Science B.V. All rights reserved.
Keywords: K-acquisition; Nutrient ef®ciency; Root length; Sand±zeolite medium; Tomato
* Corresponding author. Tel.: +1-407-884-2034; fax: +1-352-392-9359.
E-mail address;[email protected] (J. Chen).
1
Present address: Department of Environmental Horticulture and Central Florida Research and Education Center, University of Florida, 2807 Binion Road, Apopka, FL 32703, USA.
1. Introduction
Potassium is the only univalent cation among plant essential elements. Its uptake is highly selective and transport is extremely mobile; its functions are mainly in pH stabilization, osmoregulation, enzyme activation and membrane transport processes (Bhandal and Malik, 1988; Marschner, 1995). Numerous experiments have been conducted on K uptake kinetics (Epstein, 1972; Glass, 1983; Kochian and Lucas, 1988; Nissen, 1989) using various solution culture techniques. In contrast, limited information is available on K-acquisition, i.e. K acquired from soils to root surfaces and transported into the cytoplasm (Nye and Tinker, 1977; Clarkson, 1985; Jungk, 1996).
In soils, K exists in soluble, exchangeable, difficult exchangeable and mineral forms (Barber, 1995). Transformation from one form to another is a dynamic process (Spark, 1987). Soluble K provides an immediate source for root absorption (Barber, 1995). Although K is the fourth most abundant mineral element in the lithosphere (Schroeder, 1978), K concentration in soil solution is low ranging from 0.1 to 1.0 mM (Adams, 1971). Roots absorb K, however, in a large amount, often between 1.0% and 5.0% of plant dry weight (Tisdale et al., 1993). As a result, diffusion is a dominant mechanism that governs the movement of K from soils to root surfaces (Barber, 1962). Nye (1977) studied the rate of K movement in soils and the amount of K absorbed by plants, and concluded that the rate-limiting step in the plant absorption of K lies in the movement of K through soils rather than in plants.
A systematic investigation of K-acquisition was initiated in our program using tomato (Lycopersicon esculentumMill.) as a model system. Tomato absorbs K in amounts larger than any of the other nutrients (Carpena et al., 1989; Mills and Jones, 1996; Chen and Gabelman, 1999) and K deficiency has been a major problem in commercial tomato productions (Picha and Hall, 1981; Hartz et al., 1999). First a sand±zeolite culture system was developed (Chen and Gabelman, 1990). This system can simulate K-diffusion characteristics of soil, maintain K concentrations at desired levels during the course of plant growth, and allow easy recovery of intact root systems. Using this culture system we evaluated 100 tomato strains for their responses to both low (0.25 mM) and adequate (1.0 mM) K supply, and isolated 22 efficient, 18 slowly growing, and 49 inefficient strains from the 100. Among the efficient strains, two distinct characteristics associated with K-acquisition efficiency were identified (Chen and Gabelman, 1995). One was root length proliferation and the other was a high net K-influx.
when used for screening, selecting and breeding tomato cultivars for K-acquisition efficiency.
2. Materials and methods
2.1. Culture system
A sand±zeolite culture medium (Chen and Gabelman, 1990) was used throughout this investigation. Zeolite IE-96 (Union Carbide, New York) was first saturated with K in order to remove sodium (Na) from zeolite cages and then the K was desorbed by calcium (Ca) and magnesium (Mg) until desired K concentration ratios, i.e. K/(CaMg)1/2, were reached, where Ca and Mg
concentrations were 1.75 and 0.5 mM, respectively, and K concentrations varied according to experimental needs (Chen and Gabelman, 1990). Coarse sand at particle sizes from 0.45 to 0.55 mm (Unimim, Portage, WI) was washed in distilled water until no residual K and Na were detectable and dried at 1008C. The sand was then mixed with the treated zeolite (a sand : zeolite ratio by weight 75 : 1). The sand±zeolite mixture was contained in plastic pots 15 cm high and 20 cm diameter for the top and 15 cm for the bottom. Four holes in the bottom of each pot facilitated drainage.
2.2. Plant materials and plant growth conditions
Four tomato strains, 483 and 576 representing efficient, and 320 and 525 representing inefficient in K-acquisition (Chen and Gabelman, 1995), were studied. A brief summary for the strains is presented in Table 1. Seeds were germinated in K- and Na-free sand medium, and seedlings were watered with a
Table 1
Description of selected two efficient (E) and two inefficient (I) tomato strains grown in the sand± zeolite medium with K concentration at 0.25 mM for 21 daysa
Accession
320 (I) 19.35 1.62 32.32 1.16
525 (I) 19.38 1.54 32.76 1.14
483 (E) 20.12 3.45 58.56 1.99
576 (E) 45.29 1.49 56.72 2.02
L: plant root length 21 days after transplanting; IN: net K-influx; TK: total K content (root and shoot); TDW: total dry weight (root and shoot).
aFor details see Chen and Gabelman (1995). b
culture solution devoid of K and Na. The composition of the culture solution was 1.75 mM Ca(NO3)2, 0.5 mM MgSO4, 0.25 mM NH4H2PO4, 20mM FeSO4, 12.5mM H3BO3, 2.5mM MnSO4, 1.0mM ZnSO4, 0.25mM CuSO4 and 0.0075mM (NH4)Mo7O24. Free-acid EDTA (H4-EDTA) was used to complex the iron in solution. The seedlings were transplanted singly into the sand±zeolite medium 14 days after seeds were sown. Plants were grown in a growth room under light intensities 150±200mmol mÿ2sÿ1at the top of the plant canopy with 16 h light cycle. Temperatures ranged from 348C to 368C during the light period and from 258C to 278C during the dark period. Plants were watered daily with 50±100 ml of the culture solution per pot during the first week of growth, and 150±200 ml daily thereafter. K, Na, Ca, and Mg concentrations as well as pH of the medium were monitored weekly by extracting solutions from randomly selected pots using a method described by Coltman et al. (1982).
Plants were harvested usually three weeks after transplanting by excising shoots at sand level and roots were carefully recovered by inverting the pots in water, washing the roots free from sand and zeolite and rinsing in distilled water three times. The roots and shoots were dried at 808C for 48 h and dry weights determined. Total K and Na concentrations (root and shoot) were analyzed using a Varian atomic absorption spectrophotometer model Spectra AA-22 (Mulgrave, Victoria, Australia).
2.3. Root morphology
The four tomato strains were grown in the sand±zeolite medium with a K concentration of 0.25 mM. The experiment was a randomized complete block design with five replications. Three weeks after transplanting, plants were harvested, and roots were recovered. The following morphological parameters of roots were measured according to the methods used by Chen and Barber (1990) and Rengel and Robinson (1990):
1. Root length (L) at harvest was measured by the modified line intersect method described by Tennant (1975). Root lengths of seedlings at time of transplanting were measured directly and ranged from 20 to 28 cm.
2. Rate of root growth (k) was assumed as exponential and calculated by an equationk(lnL)/t, whereL (cm) was root length at timet(s) of harvest.
3. Average root radius (r0) was determined by a formula r0(Fw/L)1/2, assuming a root specific gravity of 1.0 and a uniform cylindrical root, where
Fw was root fresh weight (g) at time of harvest.
4. Average half distance (r1) between root axes was calculated byr1(1/Lv)1/2, whereLvis the root length density (cm/cm3soil) based on regular distribution. 5. Root surface area (RSA) without considering root hairs was determined by the
2.4. Net K-influx
A series of sand±zeolite media with K concentrations of 0.1, 0.2, 0.3, 0.4, and 0.5 mM were prepared respectively. Seeds of the four tomato strains were germinated in these sand±zeolite media under a randomized complete block design with 12 replications. Seven days after seed germination, seedlings were thinned to one per pot. Care was taken to retain only uniform seedlings. Plants from six of the 12 replicates were harvested 14 days after seedling emergence and the remaining harvested another seven days later. Root fresh weights and root lengths were measured. Plant shoot and root materials were dried, total dry weight and total K content determined. Average net K-influx per unit of root length (IN) was calculated based on the equation: IN(N2ÿN1) ln(L2/L1)/ (t2ÿt1)(L2ÿL1), given by Brewster and Tinker (1972) and Williams (1948), where N2ÿN1was the amount of K (pmol) taken up by plant roots during the time period of t2ÿt1 (s), L2and L1 was the root length (cm) at the time of the second harvest (t2) and the first harvest (t1).
2.5. Rhizosphere pH and ionic gradients
The four tomato strains were transplanted into the sand±zeolite medium with a K concentration of 0.25 mM. The experiment was a randomized complete block design with six replications. The pH and ionic gradients in bulk, rhizosphere, and rhizoplane soils were measured 21 days after transplanting by obtaining soils from the rhizosphere and the rhizoplane using the method described by Riley and Barber (1971) and Ohno (1989). Briefly, (1) bulk soils were obtained directly by collecting soils not penetrated by roots; (2) rhizosphere soils were those loosely associated with roots, approximately 1±3 mm from root surfaces, and obtained by gently shaking the roots; (3) rhizoplane soils were those remaining in the rhizocylinder after rhizosphere soils were removed, which were about 1 mm in thickness, and collected by allowing the soils to air dry for about 30 min and then shaking. All three sources of soils were air-dried for 24 h and sieved through a 1.0 mm screen. The pH was measured, using a 1 : 2, soil : water ratio, after 30 min equilibrium (McLean, 1982). Water extractable and NH4OAc exchange-able K, Na, Ca, and Mg from each soil source were determined (Thomas, 1982). This experiment was repeated once.
2.6. Root cation-exchange capacity
measured according to the method described by Mengel and Steffens (1985). Briefly, 2 g of fresh root material from each replication were placed in columns, and four aliquots of 100 ml 10 mM BaCl2 were passed over the roots at a flow velocity of 1 ml/min. K, Na, Ca and Mg concentrations in the elute were determined. The exchange capacity was computed based on the equivalent of each replaced cation species per gram of root fresh weight, and total cation-exchange capacity was the sum of all replaced cation species. This experiment was repeated once.
3. Results
3.1. Morphological features associated with K-acquisition
The four tomato strains had similar average root radii when grown in the sand± zeolite medium with 0.25 mM K, but varied in other morphological features (Table 2). The predictive root growth rate of strain 576 was significantly greater than the others, so that this strain had the greatest root length, the shortest half distance between root axes (i.e., average half distance from one root axis to next) and the largest root surface areas. Strains 320, 483 and 525 had slower root growth rates; thus, root lengths and root surface areas were significantly less, and average half distances between root axes were significantly greater than strain 576.
3.2. Net K-influx
The average net K-influx of strains 320, 525, and 576 was quite similar during the third week after seedling emergence, while the influx of strain 483 was
Table 2
Root morphology parameters of two efficient (E) and two inefficient (I) tomato strains grown in the sand±zeolite medium with K concentration at 0.25 mM for 21 daysa
Strain r0 k
(sÿ1106)
L r1 Root surface
area (cm2)
320 (I) 0.22ab 2.68b 18.19b 0.45a 269.59b
525 (I) 0.22a 2.66b 19.14b 0.46a 262.11b
483 (E) 0.22a 2.65b 19.90b 0.45a 267.28b
576 (E) 0.22a 2.88a 45.39a 0.30b 652.21a
r0: average root radius (mm);k: rate of exponential root growth (values shown are multiplied by
106);
L: plant root length at harvest (m plantÿ1);
r1: average half distance between root axes (cm). a
Means of five replications.
significantly higher than that of the others (Fig. 1). This difference was illustrated by the fact that strain 483 was able to approach its maximum net K-influx level at low-K concentrations and reached the saturated state at a K concentration of 0.4 mM. Strain 576 demonstrated a similar pattern as strain 483, but its maximum K-influx level was significantly lower than that of 483, which was possibly due to its large root system. Strains 320 and 525, on the other hand, were unable to reach their maximum influx level at a K concentration of 0.5 mM.
3.3. Rhizosphere pH gradient
The average pH value in the extracted solutions derived from the sand±zeolite medium was 6.5 at the beginning of transplanting, and increased to 7.5 by harvest. The pH in bulk soils differed significantly from rhizosphere and rhizoplane soils (Fig. 2). Additionally, comparing pH values among strains at the three zones indicated that pH in bulk soils was similar for all strains, but varied in rhizosphere and rhizoplane soils. Strains 483 and 576 had lower pH in rhizosphere soils than 320 and 520; only strain 483 had a significantly lower pH in rhizoplane soils than the others.
3.4. Rhizosphere ionic gradient
The distribution patterns of both water extractable and NH4OAc exchangeable K
accumulation of K
around the root surface, with a depletion occurring between 1 and 3 mm away from root surfaces (Fig. 3(a) and (b)). Ca2
and Mg2 were only accumulated around root surfaces (data not shown), indicating that mass flow was the mechanism controlling their movement to root surfaces. Although K
in the bulk soil was similar among strains, significant differences were found in rhizosphere and rhizoplane soils. Both water extractable and NH4OAc exchangeable K
were significantly lower for strains 483 and 576 than for strains 320 and 525 in the rhizosphere zone. Strain 483, however, showed the highest K in the rhizoplane soils.
3.5. Root cation-exchange capacity
Concentrations of K, Ca, and Mg in the sand±zeolite medium were quite stable during the course of plant growth (i.e. K at concentration of 0.25, Ca at 1.75 and Mg at 0.5 mM), but cation-exchange capacities of roots for these ions varied (Table 3). Quantity of exchangeable cations per gram of root fresh weight was in the order of K
> Mg2> Ca2> Na
regardless of strains and total root cation-exchange capacity of the four strains was 483 > 576 > 525320. Roots of strain
483 contained significantly more K , Na
, and Mg2than the others, and hence possessed the highest root cation-exchange capacity.
4. Discussion
The rate of nutrient acquisition depends on both nutrient supply to root surfaces and active absorption by the root. Nutrient supply to the root surfaces relies on (1) the nutrient concentration in soil solution, (2) the soil buffer capacity for the nutrient and (3) the rate of the nutrient movement to root surfaces by diffusion or by mass flow. Since K buffering power and K concentration in the solution were effectively controlled in the sand±zeolite medium, phenotypic variations among tomato strains should reflect the difference of strains either in their ability to manipulate the rate of K movement to root surfaces by diffusion or in root absorption capacity for K or both.
Fig. 3. H2O extractable (a) and NH4OAc exchangeable (b) K
4.1. Efficiency in root length proliferation
Different methods are available for the estimation of root parameters and each has its merits (Bohm, 1979; Caldwell and Virginia, 1989; Harris and Campbell, 1989; Box, 1996). Based on the method used in this study, we found contrasting morphological differences associated with K-acquisition efficiency among tomato strains. The rapid rate of root growth by strain 576 resulted in a large surface area and a shorter half distance between root axes (Table 2). Since strain 576 had a similar net K-influx rate as strains 320 and 525, the high K content in 576 may be the result of extensive exploration, by its large root system, of the soil and concomitantly effective K capture because of its increased surface area absorption.
Silberbush and Barber (1983) conducted a sensitivity analysis with a mathematical model and found that K uptake was most sensitive to the root parameters k (rate of root growth) and r0 (root radius) in soybean plants under circumstances of diffusion limited K. Steffens (1986) compared K-acquisition by grass and legume plants and concluded that root length and root surface were substantially important factors for soil K-acquisition. Our results confirmed the importance of root growth rate, root length and root surface areas in K-acquisition efficiency.
4.2. Efficiency in K absorption capacity
Strain 483 exhibited similar root morphological features as strains 320 and 525, but acquired two times more K than the latter two. The high K content in strain 483 resulted from the higher K-influx when grown at low-K stress (Fig. 1). In addition, this high absorption capacity was coupled with a low pH in the Table 3
Exchangeable K
, Na
, Ca2
and Mg2
in fresh roots of two efficient (E) and two inefficient (I) tomato strains grown in the sand±zeolite medium with K concentration at 0.25 mM 21 for daysa
Strain Root exchangeable cations (meq gÿ1
)b
320 (I) 12.60bd 3.83bc 8.38b 10.49c 35.30c
525 (I) 13.02b 3.41c 9.35a 10.42c 36.20c
483 (E) 14.00a 5.81a 8.70b 13.72a 42.22a
576 (E) 13.00b 4.08b 9.72a 12.11b 38.91b
aMean of six replications. b
Micro-equivalent per gram of root fresh weight.
cTotal root cation-exchange capacity (meq gÿ1fresh weight). d
rhizosphere and more K accumulation on root surfaces and root apoplast (Figs. 2 and 3). The pH gradients in the soil±root interfaces appeared to support the indirect coupling hypothesis of K uptake (Kochian and Lucas, 1988), i.e. an electrical coupling between H
-efflux and K
-influx (Fig. 2). We concluded that the mechanism for strain 483 in acquisition of K was due to a high absorption capacity. The results of K accumulation around root surfaces and the high root cation-exchange capacity for K were unexpected although similar results were repeatedly obtained. Our explanation is that the unstirred boundary layer of root surfaces (Dalton, 1984; Nye and Tinker, 1977), the mucilaginous layer of epidermal cells (Oades, 1978) and the porosity and cation-exchange capacity of the cell wall (Clarkson, 1988) as well as root hairs may be implicated in this K accumulation (Tan and Nopamornbodi, 1981; Xu and Liu, 1983). Nevertheless, using the sand±zeolite system, we were able to identify intraspecific differences of tomato in acquisition of K and study morphological and physiological characteristics of roots in manipulating K bioavailability.
Adaptive responses for plants to acquire low mobile nutrients, such as phosphorus and iron, have been well documented (Gerloff and Gabelman, 1983; Marschner and Romheld, 1996; Schachtman et al., 1998). Results from this study along with the others (Steffens, 1986; Jungk and Claassen, 1989) indicate that plants also evolve mechanisms in facilitating K-acquisition when grown under low-K stress. Among the 22 efficient strains identified previously from the 100 (Chen and Gabelman, 1995), we found that 18 strains had a high K-influx rate but only four strains were in the category of root length proliferation. Although we did not determine the role of root hairs in K-acquisition efficiency, it appears that root K absorption capacity and root length proliferation are dominant mechanisms in facilitating K-acquisition efficiency in tomato.
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