Plant and Soil 72, 261-273 (1983). 9 1983 Martinus Nijhoff/Dr W. Junk Publishers, The Hague. Printed in the Netherlands.

PN 22

Genotypic differences in the mineral metabolism of plants adapted to extreme habitats M. POPP Institut fiir Pflanzenphysiologie der Universitiit Wien, Althanstrasse 14, Postfach 285, A-1091 Wien, Osterreich

Key words Calcicole Calcifuge Calciphob Calcioltrophic Halophytes accumulation Salt exclusion Serpentine plants

Metallophytes Salt

Summary Halophytes, metallophytes, serpentine plants, calcicoles, and calcifuges are adapted to soil conditions which are deleterious for other plants. Some mechanisms responsible for these adaptations are described. The respective changes in the genome for these alterations of the mineral metabolism are probably not too far-reaching, because already intraspecific differentiation may lead to resistant ecotypes. On the other hand it seems likely that some families or species are favoured in occupying extreme soil types in consequence of their basic physiological features (i.e. Chenopodiaceae, Poaceae in saline habitats, Brassicaceae, Caryophyllaceae on heavy metal soils),

Introduction Extreme habitats will be confined in this paper to those environments which are special in their mineral composition and therefore only inhabitated by particularly adapted plants: halophytes, metallophytes, serpentine plants, calcicoles, and calcifuges. Emphasis will be put not only on intraspecific variations, which enable certain ecotypes of a species to cope with harsh edaphic conditions, but also on physiological features of broader taxonomic units (i.e. genus, family), which favour their adaptation to extreme soil types. For the entirety of the physiological characteristics common to the members of a taxonomic unit, Kinze129, Albert and Kinzel 2 proposed the term "physiotype". Concerning mineral metabolism physiotypical characteristics such as the dominant cation, K +/Na § or K § §2 ratios, overall low ion uptake, preference for NO3- or NH4 + are of some consequence for our understanding of how certain plants can survive under soil conditions which are deleterious for others. To prevent any misunderstanding it should be pointed out here that the terms "tolerance" or "tolerant" will be not used according to Levitt's definition in stress physiology37, but synonymous with "resistance" or "resistant", which do not indicate the mechanisms responsible for the adaptive effect. 261

262

POPP

Halophytes Two ways in which halophytes cope with the high salt content of their habitats are shown in Fig. 1. 'Salt accumulators' such as Salicornia rubra (Chenopodiaceae) are resistant to high salt concentrations in their shoots. 'Salt excluders' such as Puccinellia airoides (Poaceae), which may grow beside Salieornia rubra, are able to keep the salt content of their shoots rather low. Both mechanisms demand considerable specialisation in ion uptake and transport. In contrast to halophilic bacteria, in which the whole metabolic machinery is adapted to high salinity levels (el ref. 34) a number of enzymes from halophytes have been shown to be as salt-sensitive as those from nonhalophytes 1,15,t6,22,54. Even when the kinetic properties of some enzymes of halophytes are positively influenced by high NaC1 concentrations in the growth medium 45, it was assumed that approximately two thirds of the salt accumulated in these plants is sequestered within the vacuole 17,~8.Evidence for the validity of this assumption has now been obtained 7a5,55 and we may ask how can such concentration differences be achieved and maintained? In accumulator types this question concerns mainly the K § Na + distribution between cytoplasm and vacuole in the shoots and translocation processes between roots and shoots, while within

1000 other onions

so,. ~E

"0

CI

~- 500 E D 0-

Pucc inelli a airoides

S a l ic o r n i a rubra

Fig. 1. Ion content (equiv. m - 3 plant water) of two halophytcs, Puccinellia airoides (Poaceae) and Salicornia rubra (Chenopodiaceae), growing side by side at the Great Salt Lake (USA) (Albert, R. unpublished results).

GENOTYPIC DIFFERENCES IN PLANTS OF EXTREME HABITATS

263

excluder types the ion uptake mechanisms in roots compared to those of nonhalophytes have to be altered, as well as the ion movement from the roots to the shoots. Such alterations were first shown for leaf slices of the mangrove Avicennia marina by Rains and Epstein 48, who observed that K + uptake in the high concentration range was not decreased in the presence of concentrations of Na +, which would have an inhibitory effect on K + uptake in nonhalophytes (of ref.9). Similar observations were reported by Jefferies27 for K + uptake into roots of Triglochin maritima. In a solution containing 10 equiv, m -3 K + (high concentration range) 10 equiv, m 3 Na + had a slighly enhancing effect on K § uptake compared to the control at zero Na + . Furthermore Jefferies27 detected a positive influence of Na + on K + uptake even in the low concentration range. Roots of Suaeda maritima did not show such marked differences in their K + uptake properties Ye017), but a special feature of this and other salt accumulating halophytes seems to be a preferential transport o f N a + to the shoots. As pointed out by Osmond et al. 44 it is difficult to decide to what extent symplastic and apoplastic transport contribute to the high Na + concentrations in the shoots. In any case effective compartmentation of Na + between cytoplasm and vacuole requires unusual properties, especially of the tonoplast membranes. Investigations of strains of sugar beet 33 and Plantago species 1~, differing in their salt tolerance, as well as Halocnemum strobilaceum 42indicated marked changes in the (Na + + K +) ATPase activities in relation to the varying salt sensitivity of the organisms. And even the lipid composition of the membranes themselves seemed to be of importance for adaptation to salinity 11,32,33. Although there are many factors involved in adjustment of plants to saline habitats, the respective changes for this purpose in the genome are probably not too far-reaching, because intraspecific differentiation can lead to salt tolerant ecotypes. Interestingly these ecotypes are mainly species belonging to the Poaceae or Juncaceae, families in which the halophytes are, with few exceptions, salt excluders characterized by K +/Na § ratios greater than unity with low CIand SO4 -2 uptake 4,2~. The adaptive significance of salt exclusion from the shoots becomes evident from experiments with Agrostis stolonifera, Festuca rubra 24,51 and Juncus buffonius 5~, where the salt tolerant ecotypes always contained less salt in their shoots than the non tolerant ones. Evidence for ecotypical differentiation in salt accumulator types is scarce. Fig. 2 shows the wide range of possible salt accumulation in the chenopod Salicornia utahensis in habitats of different salinity. Even under non saline conditions chenopods usually show a preponderance for Na § and are characterized by a high anion content due to high CI- uptake and storage of free oxalate. It remains to be determined whether or not the great variation in salt content seen in Fig. 2, and observed in other cases 44 is due to a wide physiological amplitude of one genotype or is provoked by intraspecific differentiation. If the latter is the case this would mean that in contrast to the ecological races of the Poaceae and

264

POPP

Salicornia utahensis 1500o

c-

:::::~

~-I000

::::"

ID

M~

other ufliu.~

K

S04

Na

Cl

g soo

Fig. 2. Ion content (equiv. m-3 plant water) of the halophyte Salicronia utahensis (Chenopodiaceae) from severalhabitats throughout USA differingin soilsalinity(Albert, R. unpublishedresults).

Juncaceae mentioned above, the more salt tolerant ecotypes of the Chenopodiaceae are the better salt accumulators. Salt glands are of course another special feature in the mineral metabolism of halophytes and should be mentioned in the context of this brief review. They are not necessarily restricted to salt excluders, but seem to function also in maintaining the appropriate salt concentration in salt accumulators like many Atriplex species 44. There is great variety in the structure and physiological properties throughout the halophytes (cf ref.38). For example in some C1appears to be the actively transported ion while in others it is Na +.

Metallophytes Cu, Zn, Mn, Mo, and possibly Ni are necessary micronutrients for all plants, but when they occur in high concentrations such as in ore deposits or mining wastes, these and other heavy metals without known physiological function such as Cd, Pb, Cr become deleterious for most plants. Heavy metal tolerant plants are not adapted to all heavy metals, but only to those which occur in their natural habitats. For instance a plant from a Cu-rich soil is only Cu- and not Ni-, Zn-, or Mn-tolerant (e.g. different ecological races of Agrostis tenuis) 23. From these and other observations it was assumed that for each heavy metal there exists a particular detoxifying mechanism in the resistant plants. The shoots of heavy metal-tolerant plants may behave as accumulators or as excluders as was seen in halophytes. Exclusion may be achieved by reduced absorption by the roots and/or by lower translocation from the roots to the shoots 6. In any case the basic mechanisms are not well understood. For Mn it is

GENOTYPIC DIFFERENCES IN PLANTS OF EXTREME HABITATS

265

proposed that excluders are able to oxidise the available divalent form to the unavailable tetravalent ion ~9. Zn and Ni are found in high amounts bound to the cell walls (cf. ref]4) and for different ecotypes of Silene cucubalus Ernst 13observed a positive correlation between cation exchange capacity of the roots and the uptake of Zn and Cu. Translocation to the shoots may be decreased either by reaction of heavy metals with phosphate to form sparingly soluble salts ~2or by increasing the Ca § support 53. These two possibilities are not special features of heavy metal tolerant plants, but are generally of some consequence for the distribution of heavy metals between roots and shoots. Again, as in the halophytes, even those metallophytes which accumulate heavy metals mainly in their shoots, possess no heavy metal resistant enzymes4~ Possible mechanisms of preventing the damaging effects of heavy metals on

Poaceae

A

i

Cyperaceae

I

Liliaceae Cicbori~c~ae i

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t

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Brassicaceae Caryophyllaceae Fagaceae

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Ranunculaceae

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!

!

200

400

600

800

(783~ + 271) -

p~

Mn

Fig. 3A The means __+95~ confidence limits of Mn content (ppm dry substance) of different plant families collected from various habitats throughout Austria 43.

266

POPP

metabolism are i) complex formation and chelation with different organic compounds, ii) storage in the vacuole and iii) retention by the cell walls. Organic compounds involved in detoxification are mainly organic acids (oxalate, malate, citrate), amino acids or mustard oil glucosides. Presumably members of the Caryophyllaceae, for which free oxalate content is typical, and members of the Brassicaceae, which are specialised in mustard oil glucoside production, may therefore be favoured in heavy metal habitats. In case of Zn and Ni the complexing mechanisms are highly effective, so that tolerant plants have a higher demand for these elements to reach optimal growth (i.e. to get the necessary amount of the micronutrient in an available form) than their sensitive counterparts. There exists no special preference of certain plant families for particular heavy metals as was shown in an extensive study by Mutsch 43on a great variety of plant species in many different habitats throughout Austria. Only in the case of

I

Poaceae

B

Cyperaceae I

Liliaceae

#

Cichoriaceae

#

Asteraceae Lamiaceae

|

Plantaginaceae

j

Scrophulariaceae

. _ ~ i ~ b ( 1 5 , 8 #

~ 3,2)

Apiaceae

I

Fabaceae Crassulaceae

$

Rosaceae

t

Ericaceae Brassicaceae

#

Caryophyllaceae I

~

!

Fagaceae Ranunculaceae Pinaceae

I

5

!

10

I

15

p~

F i g . 3 B . The means ___9 5 % confidence limits of Cu content (ppm dry substance) of different plant families collected from various habitats throughout Austria43.

GENOTYPIC DIFFERENCES IN PLANTS OF EXTREME HABITATS

267

Ericaceae (Fig. 3A) was there a trend for Mn accumulation. It should be pointed out that while these plants occur only in Mn-rich locations such as bogs some members such as Vaccinium uliginosum do not accumulate Mn beyond the range found in " n o r m a l " plants. Somewhat higher than normal levels of Mn are also found in members of Fagaceae and Pinaceae, but in this case accumulation might be a consequence of their tree-like structure. With respect to Cu content (Fig. 3B) the Boraginaceae are slightly higher than all the other families but compared to Cu accumulators (see ref. 14) their Cu storage is relatively low and they cannot be regarded as especially Cu tolerant.

Serpentine plants A high Mg+2/Ca +2 ratio, a high Ni content and rather small amounts of macro-nutrients are three main features of serpentine soils 46. But there is a wide variation of these factors in serpentine habitats and Cr as well as Co may occur in relatively high concentrations (cf. ref.31). "Serpentine" plants therefore have not only to face heavy metal toxicity, but have also to cope with an extreme nutritional situation. For instance, in normal plants increasing amounts of Mg +2 reduce the uptake of K + (Fig. 4, Helianthus annuus) and Ca +2. A serpentine tolerant plant Such as Helianthus bolanderi var. exilis seems adapted in so far as its K + uptake is not influenced by Mg +2 levels up to 1 M 9 m -3 (ref. 39and Fig. 4).

550

Hk

m..

+6 6 >- ~50 7

9 H b o l a n d e r t vat exihs

o

"~"

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9 H. a n n u u s

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II

0.01 Fig. 4.

,%

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03

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!

1 2 Mg*2Mm -3nutrient solution

K + content (pmol 9 g - ] dry matter) of the serpentine-tolerant Helianthus bolanderi var.

exilis and the non-tolerant Helianthus annuus grown with various Mg +2concentrations (logarithmic scale) in the nutrient solution (from Kinzel and Weber31 after data from Madhok and Walker39).

268

POPP

This plant is also able to reduce Mg +2 accumulation in the shoots and this is of some consequence, because high levels of Mg +2 exhibit a negative effect on processes in the cytoplasm 31. However, reduced Mg +2 storage in the shoots accompanied by a higher demand for Mg § to obtain optimal growth is not necessarily a common feature of all serpentine plants. As shown in Table 1 different species growing on the same serpentine soil vary widely in their K +, Ca § and Mg +2 content (heavy metals seem to be of minor importance in this habitat) and reflect their physiotypical characteristics. In Festuca cinerea (Poaceae) even on a serpentine soil K + is the dominant cation while in Sedum album (a member of the calciotrophic family of the Crassulaceae 28) accumulates Ca § 2 although soil content of this cation is very low. Because of their free oxalate content members of the Caryophyllaceae such as Cerastium arvense might detoxify excess levels of Mg as the sparingly soluble oxalate salt 31. In contrast to heavy metal tolerant plants for which Antonovics 5 reported that ecological races occur in 30 different species very little is known about serpentine tolerant and non-tolerant ecotypes. Kruckeberg 47reported such ecotypes of Gilia capitata and Achillea borealis, but the physiological consequences of the intraspecific differentiation were not revealed.

Caicicoles and ealeifuges An obvious difference between calcareous and silicate soils is of course their Ca content. But other soil factors such as HCO3- concentration, free A1 ion content, Fe-availability, and pH also vary and are of considerably consequence for plant growth. As pointed out by KinzeP ~ for some plants it would be more correct to

Table 1. K +, Na +, Ca + 2, M g + 2 in #mol 9 g - l dry matter, the molar K +/Ca + 2 ratio, and content of heavy metals in p p m dry matter from the shoots of plants from a serpentine soil (Gurhofgraben, Austria). Data for cations are from Horak 26, data for heavy metals are from Mutsch 43

K+/ Plant species

Ca + 2 N a + K + Ca + 2 M g + 2 F e

Cerastium arvense 307.0 4.3 Euphoriba cyparissias 6.3 1.7 Thtaspi montanum 9.1 3.1 Biscutella laevigata 4.1 4.4 Sedum album 0.5 5.6 Potentilla arenaria 47.7 1.5 Genistapilosa 2.8 1.7 Dorycniumpentaphyllum agg. 6.0 2.4 Festucacinerea 20.9 1.8

799

2.6 325

276

44

344

453

Mn ZnCu

Mo Co

226 283 74 4.9 0.04 2.10

Ni

Cr

9.4 0.94

60

35 41 5.3 0.05 2.37 33.9 0.21

50

404

506 124

775

108

29 25 9.6 0.04 0.58 18.0 0.36

156 298 572 12

560 210

79

37 51 7.3 0.08 0.62 16.8 0.23

59

21

126

199

33

300

88

21 17 5.2 0.05 0.14 21.3 0.23

376

18

50

69

28 29 5.3 0.07 0.04 13.1 0.21

GENOTYPIC D I F F E R E N C E S IN PLANTS OF E X T R E M E HABITATS

o C

121

E ~ &O"

269

leaves/Ca

•i

,,,, l

I

I

I H

l

Ill

I

V

IV

Fig 5 A K + and Ca +2 content (equiv. m -3 plant water) of leaves of Kalanchoe daigremontiana grown in nutrient solutions with different K + / C a +2 ratios. 12.8/0.2; II 2.5/0.5; III 2.0/1.0; IV 1.5/1.5; V 0.5/2.5 K + / C a +2 equiv, m -3 nutrient solution. (R66ner, upublished results).

classify them as acidophilic or basiophilic, because their response to Ca +2 is not very pronounced. Plants may vary appreciably in their Ca +2 content and Iljin 28 distinguished between calciotrophs which are rich in soluble Ca +2, and calciphobes, the pressure sap of which contains almost no free Ca +2. These terms for the

I

~, 400'~ B roots E

t

"t --'~

>,,,

13

t

".K

I l I

g2oo-

_..-,----Ca !

!

I I!

!

!

Ill IV

!

V

Fig 5 B K + and Ca + 2 content (equiv. g - 1 dry matter) of roots of Kalanchoe daigremontiana grown in nutrient solutions with different K + / C a +2 ratios. K + / C a +2 ratios are given in 5A. (R6Bner, unpublished results).

270

POPP

physiological features concerning Ca content should not be confused with the specifications for the ecological distribution (calcicole, calcifuge). A calciotrophic plant need not necessarily be a calcicole and vice versa 3,28'3~ The low Ca +2 content found in physiology calciophobic plants like Chenopodiaceae, Caryophyllaceae, Polygonaceae and others depends on their storage of free oxalate. During extraction of the plant material oxalate from the vacuole mixes with Ca +2 from all other cell compartments and forms insoluble Ca-oxalate. Thus it is difficult to assess what the usual Ca +2 distribution in vivo is in these plants. For a calciotriophic plant such as Kalanchoe daigremontiana (Crassulaceae) R6Bner (in prep.) showed in a recent study that its preference for Ca +2 is restricted to the leaves, while the roots and the xylem sap contain more K § than Ca § even in nutrient solutions, where the K+/Ca +2 ratio is below unity (Fig. 5). From this and other experiments it seems likely that K. daigremontiana is not only a better Ca +2 accumulator, but also a better K + retranslocator than other plants. A similar situation was observed in the calciotrophic members of the Brassicaceae, where the K/Ca +2 ratio of the leaves was below unity while the stems was markedly above unity 49. As mentioned above these physiological features are not of very much consequence in determining the ecological distribution in relation to Ca § Possibly it is not the high absolute Ca § content of calcareous soils, but the very low K+/Ca +2 ratio, which is unfavourable for certain plants. Silicate soils are not higher in K +, but markedly lower in Ca +2 (ref. 2~ and the changed K§ § 2 ratio seems to be of importance. Snaydon and Bradshaw 52investigated ecotypes of Festuca ovina from habitats differing in their Ca +2 content. In the ecotype from the soil poor in Ca +2 K + uptake was reduced by amounts of Ca + 2 (100 ppm), which had no effect in plants from a Ca + 2 - rich habitat. Although the calcicole-calcifuge problem should be not reduced to the Ca+2-factor, it would lead too far to consider all the other soil conditions in the context of this paper (for further information see refs.3~176

Concluding remarks Since the review by Epstein and Jefferies ~~knowledge on genetic control of ion transport has increased significantly. While the varietal changes of ion uptake in cultivated plants are of practical interest, studies on edaphic ecotypes of wild plants are also helpful for our understanding of genotypic variation in ion transport 35. Furthermore investigations of wild plants from extreme habitats illustrate also the great variability of mineral metabolism in higher plants. It may be assumed that some families are favoured to live on harsh soil conditions (i.e. Chenopodiaceae, Poaceae in saline habitats, Brassicaceae, Caryophyllaceae on heavy metal soils) because o f their basic physiological constitution.

GENOTYPIC DIFFERENCES IN PLANTS OF EXTREME HABITATS Aeknowledgements

271

The author is thankful to Doz. R. Albert and Prof. H. Kinzel for fruitful

discussions. Special thanks are due to Dr. C. A. Atkins for reading the manuscript.

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Albert R and Kinzel H

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24

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25

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36 37 38 39 40

41

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GENOTYPIC DIFFERENCES IN PLANTS OF EXTREME HABITATS 42

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43

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44

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49

Rattenb6ck H 1978 Chemisch-physiologische Charakterisierung der Brassicaceae. Ein Beitrag zum Physiotypenkonzept. Phil. Diss. Universitiit Wien. 50 Rorison I H (ed) 1969 Ecological aspects of the mineral nutrition of plants. Blackwell Scientific Publications, Oxford, Edinburgh. 51 Rozema J 1978 On the ecology of some halophytes from a beach plain in the Netherlands. Ph. Th. Freie Universit~it, Amsterdam. 52 Snaydon R W and Bradshaw A D 1961 Differential response to calcium within the species Festuca ovma L. New Phytol. 60, 219-234. 53 Wainwright S J and Woolhouse H 1977 Some physiological aspects of copper and zinc tolerance in Agrostis tenuis Sibth: Cell elongation and membrane damage. J. Exp. Bot. 28, 1029 1036. 54 Weimberg R 1970 Enzyme levels in pea seedlings grown on highly saline media. Plant Physiol. 46, 466-470. 55 Yeo A R 1981 Salt tolerance in the halophyte Suaeda maritima L. Dum Intracellular compartmentation of irons. J. Exp. Bot. 32, 487497.