Transport in Plants vol. 2. part 1. pp 372-393 (1976)
9. Genotypic Variation in Transport
A. Läuchli

1 Introduction

Ecologists have recognized for a long time that nature has confronted them with a great number of natural examples where plants are adapted to different nutrient regimes. For instance, mangroves growing in sea water can be contrasted with trees on the non-saline land next to them. The question arises as to why mangroves grow in sea water, and why do they not live further inland in the community of the less salt-tolerant tree species? A second example is given by the strikingly different floras on calcareous and acid soils, respectively. Why are there species which thrive on soils rich in lime and high in pH, whereas others occur only on acid soils low in Ca2+ and pH? Thirdly, serpentine soils bear a sparse yet characteristic flora. These soils are high in Mg2+ and certain heavy metals but contain little Ca2+. Why, on the one hand, is there such a characteristic serpentine flora, and why, on the other hand, are most species not able to exist on serpentine soils? Many more such examples could be added. All of them have in common that their existence follows from variation in the genotype of plants and from adaptation during the course of evolution.

The subject of adaptation of plants to different nutrient regimes will be dealt with in 9.2. It will be emphasized here that adaptation to nutritional factors may be correlated with genotypic variation in ion transport processes. From this circumstantial correlation the idea is developed that membrane transport per se is genetically controlled. Genetic control of transport in plants will be discussed in 9.3.

2. Ecotypes—Their Adaptation to Nutritional Factors

Species may have phenotypic plasticity in order to adjust their metabolic processes to take maximum advantage of changes in the environment. The existence of such systems is known for morphological and also for some physiological characters. However, the latitude of phenotypic responses to changes in the environment is limited within a genotype (BRADSHAW, 1965). What this simply means in terms of nutritional adaptation of roots is that particular roots do not cope with all mineral substrates. Edaphic factors have, however, given rise to adaptation to the mineral habitats of the earth. Such adaptation has become evident on two levels. Differences in nutritional adaptation are well-known among species and may be also recognized among families. This type of adaptation led KINZEL (1969) to develop the concept of the comparative physiology of mineral metabolism. It is beyond the scope of this chapter to present an extensive survey of the comparative physiology on the species, genus and family levels, though a brief introduction will be presented as this is deemed necessary for the understanding of the other type of adaptation, i.e. genotypic adaptation to nutritional factors. This second type is a consequence of evolutionary processes leading to ranges of genotypes known as ecological races or ecotypes. For a recent introduction to nutritional adaptation the reader is referred to EPSTEIN (1972).

Possibilities for a comparative physiology of mineral metabolism as suggested by KINZEL (1969) are given with respect to three nutritional factors, i.e. Ca2+ heavy metals, and salt.

2.1 Calcium

It is well known that plants common on calcareous soils (calcicole plants) show high contents of soluble Ca2+ and malate while those confined to acid, low-calcium soils (calcifuge plants) contain little soluble Ca2+ because of the presence of oxalate precipitating Ca2+ as oxalate salt (KINZEL, 1963). One way of distinction is by comparing the ratios of the soluble fractions of K+/Ca2+ in the plants. Using such an approach, all examined species of the Crassulaceae showed molar K+/Ca2+ ratios below I and belong to the calcicole plants, but many species of Caryophyllaceae and Labiatae had K+/Ca2+ ratios up to 100 and are considered to be calcifuge (KINZEL, 1969). That the extreme differences in K+/Ca2+ ratios between calcicole and calcifuge species are under genetic control is indicated by the following example. Anthyllis vulneraria, a calcicole species which is also able to grow on acid soil, was collected from a calcareous and an acid soil and the K+/Ca2+ ratio in the plant determined. Plants from both sites contained more soluble Ca2+ than K+ emphasizing the inherent calcicole character (HORAK and KINZEL, 1971).

CLARKSON (1965) presented evidence that calcicole species may be discernible from calcifuge species through differences in mechanisms of Ca2+ uptake. Agrostis setacea, common on acid soil, appeared to possess an uptake system with a high affinity for Ca2+ approaching its maximal rate at 0.25mM Ca2+ The calcicole species Agrostis stolonifera, however, accumulated progressively more Ca2+ in the shoots with increasing Ca2+ concentration in the medium. Since uptake by whole plants was measured, transpiration-dependent Ca2+ uptake may have been important in CLARKSON'S experiments. (Uptake of Ca2+ by roots is discussed in 3.3.5.) In a comparative study involving Vicia faba (calcicole) and Lupinus luteus (calcifuge), SALSAC (1973) found that a much greater fraction of Ca2+ was exchangeable in the root of the calcicole than in that of the calcifuge species.

ATPases associated with membranes appear to be involved in ion transport (Part A, Chap. 10). In KYLIN'S laboratory it has been shown that the activity of membrane-associated ATPases from roots of wheat, which has a high demand for Ca2+, was stimulated more by Ca2+ than by Mg2+. On the other hand, ATPase activity from roots of oat having a high need for Mg2+ was stimulated more by Mg2+ than by Ca2+, (KYLIN and KÄHR, 1973; KÄHR and KYLIN, 1974). Important physiological characteristics of membranes (i.e. mechanism of Ca2+ uptake, ATPases) may thus be fundamentally different in calcicole and calcifuge species, enabling the respective plants to be fit for their natural substrate. Species may differ too in their selectivity to Ca2+ and Mg2+ taken up to the shoot by largely transpiration-dependent processes. Transport to the shoot may be 10 or more times greater than uptake or accumulation in the roots (3.3.5.1; see also LEGGETT and GILBERT, 1969).

Genotypic adaptation to Ca2+ was found in TrifoIium repens. Populations from acid and calcareous soils differed in Ca2+ contents of the shoot (SNAYDON and BRADSHAW, 1969). The differences were suggested to be largely due to variations in selective Ca2+ uptake.

2.2 Heavy Metals

Certain plants are able to grow and develop on habitats contaminated with toxic levels of heavy metals. The subject of heavy metal tolerance in plants has been reviewed thoroughly by ANTONOVICS et al. (1971). Survival of heavy metal tolerant plants is not due to metal exclusion from the plant (e.g. LANGE and ZIEGLER, 1963; TURNER, 1969; SEVERNE and BROOKS, 1972; JAFFRÉ and SCHMID, 1974). Rather, heavy metal tolerant plants may be capable of synthesizing chelating compounds which form non-toxic complexes with the heavy metals (JOWETT, 1958). An extreme case is represented by certain encrusting lichens which are able to colonize the bare rock on slags contaminated with mining debris. Heavy metal tolerance in these lichens may be due, in part, to a predominant deposition of insoluble metal compounds on the surface of a lichen (NOESKE et al., 1970). The specialized habitat of a metal-contaminated area has proved extremely valuable to studies on the evolution of ecotypes.

Genotypic adaptation to high levels of heavy metals (e.g. Zn, Cu, Ni, Pb) mainly studied by BRADSHAW and his group (cf. ANTONOVICS et al., 1971), does not seem to be correlated with variations in rates of uptake for heavy metals. In populations of Agrostis tenuis differing in tolerance to Zn, the subcellular distribution of bound Zn in roots varied with the degree of Zn tolerance (MATHYS, 1973). With increasing Zn2+ concentration in the medium, the percentage fraction of Zn bound to the cell walls increased in the roots of the tolerant population but decreased in those of the sensitive ones. The reverse was evident for Zn bound to a cytoplasmic fraction. Nonetheless, the study by MATHYS (1973) does not allow us to assume a clear relation between Zn tolerance and the mechanism of Zn2+ uptake. The nature of tolerance to heavy metals is probably a matter of degree; there is not an all-or-nothing effect as demonstrated for root growth of Cu tolerant and non-tolerant populations of Agrostis tenuis (Fig. 9.1). Tolerance to Cu in these populations is inherited in a dominant rather than a recessive manner (Fig. 9.1). From a genetic point of view, particularly important is the finding by GREGORY and BRADSHAW (1965) that the tolerance of plants to a given heavy metal is metal-specific. Recent evidence suggests that selection for tolerance can occur easily. WU and BRADSHAW (1972) found populations of Agrostis stolonifera near a Cu-refining industry in England, which obviously developed from plants that were tolerant to aerial copper pollution and had formed by mutation or segregation. This demonstrates evolution related to aerial pollution. Of particular interest is that this evolution must be of very recent origin and may still be in the process of occurring.