Chemical Composition of Australian Mangroves II. Low Molecular Weight Carbohydrates

Chemical Composition of Australian Mangroves II. Low Molecular' Weight Carbohydrates MARIANNE POPP

Institut flir Pflanzenphysiologie, Universitat Wien, Postfach 285, A-1091 Wien, Austria Received October 19, 1983 . Accepted November 18, 1983 Summary Low molecular weight carbohydrates (LMWC) occurring in both young and old leaves of 22 mangrove species from Northern Queensland (Australia) were identified using gas liquid and gas capillary chromatography. The cyclitol, pinitol, was the most prevalent compound in all members of the Rhizophoraceae and in the mangrove fern Acrostichum speciosum. In addition, Aegialitis annulata stored chiro-inositol. Another cyclitol, quebrachitol, occurred in Excoecaria agallocha. Mannitol, a polyol, was dominating in Aegiceras corniculatum, Lumnitzera littorea, Lumnitzera racemosa, Sonneratia alba and Scyphiphora hydrophylacea. The sugars sucrose, glucose, and fructose were not generally stored in high concentrations (except Xylocarpus granatum, 300 mol· m- 3 plant water). Those species which contained no cyclitols or mannitol were low in their LMWC content. LMWC concentrations were higher in young leaves than in old ones in nearly all species under investigation. Polyols and cyclitols may have taxonomically associated distributions and may playa role in osmotic adjustment.

Key words: Mangroves, chiro-inositol, mannitol, pinitol, quebrachitol. Introduction Low molecular weight carbohydrates playa paramount role in osmoregulation of several algae (Hellebust 1976; Kirst and Bisson 1979; Munns et al. 1983). They are also involved in turgor generation of those angiosperm halophytes which partially exclude Na+ and Cl- from their leaves (Albert and Popp 1978; Gorham et al. 1980, 1981). A function as a compatible solute is ascribed to sorbitol in the cases of several Plantago species (Ahmad et al. 1979; Gorham et al. 1981; Konigshofer 1981; Briens and Larher 1983). Pinitol is assumed to be a compatible solute in Honkenya peploides (Gorham et al. 1981) and is reported to occur in Spergularia media (Albert and Popp 1978; Gorham et aI. 1980). It was, therefore, important to include LMWC determinations in this study to gain information on their possible contribution to osmotic adjustment in mangrove leaves. Former studies include data on sucrose and reducing sugars (Walter and Steiner 1936), respectively reducing and total sugars (Karmarkar 1982), but no data on polyols and cyclitols are available.

Abbreviations: LMWC = low molecular weight carbohydrates; pw = plant water.

Z. Pjlanzenphysiol. Bd. 113. S. 411-421. 1984.

412

MARIANNE POPP

Materials and Methods Sites and collection procedures of mangrove leaves were the same as described by Popp 1984. In addition, fully developed leaves of some species related to mangroves were collected in the Botanic Garden in Canberra during summer. The LMWC fraction of the hot-water extracts (for preparation see Popp 1984) was obtained by removing the charged compounds with cation- and anion exchanger resins (Albert and Popp 1978). Qualitative and quantitative determinations of the single components were performed using two gas chromatographic methods (SE 30, Sweely et al. 1963; Dexsil300, Albert and Popp 1978). Since the hexitols: sorbitol, mannitol and dulcitol appeared at the same retention time in both of the above mentioned methods, samples containing high concentrations of hexitols were additionally analyzed on a capillary GC column (fused silica capillary column, 50 m long, OV 101, N 2-flow 1.5ml·min-l, split 1: 70). This method provided a satisfactory resolution between the three hexitols. The three compounds were not differentiated in samples with low hexitol content, but since the standard calibrations curves for the compounds were the same, errors were not introduced into the quantitative calculations.

Results The same species groupings as in part I (Popp 1984) have been retained here to facilitate consideration of possible relationships between mineral and LMWC metabolism. In addition, the bracketed numbers in the figure legends are the differences between the sums of CI-, Na+, K+, Mg2+ and Ca2 + for young and old leaves

sol-,

ESI

pinitol

~

0

mannito I

~

[]) sucrose

20

i

~

c:

§

~

chiro-inosiiol

a.

~

E 100

'0

E

young old

A.i.

A.a.

A.c.

A.m.

Fig. 1: LMWC concentrations in young and old leaves of salt-secreting mangrove species (mol· m -3 pw). The entire column height represents the sum of LMWC with the major compounds indicated by patterned areas. The bracketed numbers below represent the differences in the sum of ion concentrations between young and old leaves (mol· m- 3 pw). A.i. = Acanthus ilicifalius ( + 133.7); A.a. = Aegialitis annulata ( + 133.5); A.c. = Aegiceras cami· culatum (+84.9); A.m. = Avicennia marina (+505.1).

Z. Pjlanzenphysial. Ed. 113. S. 411-421. 1984.

Low molecular weight carbohydrates in mangrove leaves

Gi

200

young

413

~ pinitol

0; J ~

c

.!!

a.

':'

E 100

"0

E

R.I. B.e. B.g. C.t. R.B. Fig. 2: LMWC concentrations in young and old leaves of Rhizophoraceae (mol· m- 3 pw). For explanations see Fig. 1. B.e. = Bruguiera exaristata (+267.0); B.g. = Bruguiera gymnorhiza (+228.4); c.t. = Ceriops tagal ( + 232.7); R.a. = Rhizophora apiculata ( + 108.0); R.l. = Rhizophora lamarckii ( + 273.1).

also in mol· m- 3 plant water. (Ion concentrations m part I were expressed as equ· m- 3 pw and presented in another scale.) Fig. 1 (corresponding to Fig. 3, part I) shows the LMWC concentrations of salt-secreting species. The LMWC concentrations for the fifth salt-secretor, Avicennia eucalypti/olia, are not shown, but were rather the same as for A vicennia marina. These species are representative of most of LMWC storage features. Acanthus ilici/olius and the two A vicennia species had little LMWC storage and no marked concentrations of polyols and cyclitols. Aegiceras corniculatum was representative of the mannitolaccumulating species with a steep decline in mannitol content as leaf age increased (difference between young and old leaves: 111 mol· m- 3 pw). Aegialitis annulata was an unusual case of a species with not only one dominate compound, but also several LMWC occurring in appreciable amounts. Two cyclitols, pinitol and chiroinositol were stored in addition to sucrose in Aegialitis annulata. Pinitol was the most prevalent LMWC, 70 to 85 % in the members of Rhizophoraceae (Figs. 2 and 3 a; corresponding to the samples included in Figs. 4 and 5 in part I). The decrease of pinitol in the old leaves was associated with a concomitant decline in LMWC except in Bruguiera gymnorhiza where pinitol increased in old leaves. Pinitol concentrations in young leaves of three different Rhizophora stylosa trees had little intraspecific variation, whereas the older leaves differed markedly intraspecifically (Fig. 3 a). This was probably because older leaf samples were not so uniform in age and ion content as the younger ones. The decrease in pinitol as leaf age increased was most pronounced in the plant with the highest increase of Na+ Z. Pjlanzenphysiol. Ed. 113. S. 411-421. 1984.

414

MARIANNE POPP

300

Rhizophora sty/osa

~

;; ~

c.,

0.

7

E

~

pinitol

200

'0 E

100

young old

y. o·

y. o. small big hypocotyls

Fig. ~ a: LMW~ concentrations in youn~ and old leaves as well as in hypocotyls of viviparo~s seedhngs of Rhtzophora stylosa (mol· m - pw). The three sets of columns represent three dIfferent trees. For explanations see Fig. 1. Rhlzopho,.

.tylo ••

1000 ~

-:;; ~

C IV

0. 50 M

I

E

"e"

el

young

old

small big hypocolyls

Fig. 3 b: Ion concentrations in young and old leaves as well as hypocotrls of viviparous seedlings of Rhizophora stylosa (equ· m- pw). Fig. 3 b corresponds to the right hand set of columns in Fig. 3 a.

and CI- concentrations in old leaves (Fig. 3 b, Fig. 4 in part I). The influence of leafage on pinitol content was also seen in Ceriops tagal where pinitol concentration in the senescent leaves was only 30 % of that in the young leaves. Pinitol increased as hypocotyl ages increased in the viviparous seedlings of Rhizophora stylosa (Fig. 3 a) although the ion content varied little between the developmental stages (Fig. 3 b; Lotschert and Liemann 1967). Both Lumnitzera species as well as Sonneratia alba accumulated mannitol, again to a much higher extent in young than in old leaves (Fig.4, corresponding to Fig. 6, Z. Pjlanzenphysiol. Bd. 113. S. 411-421. 1984.

Low molecular weight carbohydrates in mangrove leaves

415

Table 1: Low molecular weight carbohydrates (LMWC) in mangrove leaves of different age (mol· m- 3 plant water). y = young,o = old, s = senescent; fru = fructose, glc = glucose, suc = sucrose, myo-i = myo-inositol, scy-i = scyllo-inositol, pin = pinitol; hex = hexitols (sorbitol + dulcitol + mannitol), in case of Sonneratia alba and Lumnitzera racemosa mannitol was proven to be the major hexitol. Species

Ceriops tagal

Leaf age

fru

y

10.0 0.2

8.8 1.9 2.0

22.2 21.5 13.0

5.3 4.6

2.3 1.7 0.9

25.4 7.0 3.1 7.2 6.1 + 35.1 11.3 81.2

21.7 9.1 3.7 7.1 6.2 7.5

5.8 10.1 1.7

199.7 79.1 19.5

1.7 Ll 0.3

4.4 5.9 3.9

lOLl 91.4 57.1

1.0 0.4 0.8

25.0 9.8 40.4

21.8 51.3 19.1

1.3 8.4

2.5 1.6 1.6

0

Sonneratia alba

y 0

Lumnitzera racemosa

y 0

Osbomea octodenta

y 0

glc

suc

hex

mYO-l

SCY-l

pm

I; LMWC

182.0 79.8 5Ll 1.8 0.4

230.6 105.1 71.6 256.1 106.8 28.3 120.8 110.0 69.3

0.6

3.5

0.9

5.5

88.5 75.3 157.1

- non detected. + detected, but in too low concentrations to be quantified.

D Ill!

Gi 10

200

mannitol fructose

~ glucose I[J] sucrose

~

.

;:

young

c-

old

<;>

E 100

.... .... .... ....

"0

E

.... .... .... ..... ,"

....

.... . ... .... .... ..... ...

.... .... L.I.

L.r.

s. a.

X. g.

~

X.m.

Fig. 4: LMWC concentrations in young and old leaves from Combretaceae, Sonneratiaceae and Meliaceae species (mol· m- 3 pw). For explanations see Fig. 1. L.l. = Lumnitzera littorea (-91.7); L.r. = Lumnitzera racemosa (+88.6); S.a. = Sonneratia alba (+486.6); X.g. = Xylocarpus granatum (-708.4); X.m. = Xylocarpus mekongensis.

part I), as was also the case in Aegiceras corniculatum (Fig. 1). Table 1 presents more details of age-induced changes in LMWC content. A ten-fold decrease in mannitol Z. Pjlanzenphysiol. Ed. 113. S. 411-421. 1984.

416

MARIANNE POPP

was observed between young and senescent leaves in Sonneratia alba while this poly01 was reduced to about 50 % in the senescent leaves of Lumnitzera racemosa. The two Xylocarpus species were different in LMWC accumulation, although they had similar ionic and free amino acid compositions (parts I and III). Xylocarpus granatum was the only species where high LMWC concentration was accomplished by glucose, fructose and sucrose storage without any marked contribution of polyols or cyclitols, although chiro- and myo-inositol were present (Table2). Table 2: Low molecular weight carbohydrates (LMWC, mol· m -3 plant water) in young leaves of mangrove species and in fully developed leaves of related species collected at the Botanic Garden in Canberra. fru = fructose, glc = glucose, suc = sucrose, tri = trisaccharide, myo-i = myo-inositol, scy-i = scyllo-inositol, chi-i = chiro-inositol, pin = pinitol, que = quebrechitol, hex = hexitols (sorbitol + dulcitol + mannitol), in case Scyphiphora hydrophylacea mannitol was proven to be the major hexitol. Species

Family

Osbomea actodenta Melaleuca /rypericifolia Excoecaria agallocha Micrantheum hexandrum Scyphiphora hydrophylacea Opercularia rolubilis Xylocarpus granatum Xylocarpus mekongensis Melia azedarach Heritiera littoralis

Myrtaceae

35.1 25.0

21.8

-

2.5

Myrtaceae Euphorbiaceae Euphorbiaceae

17.7 13.0 34.2 29.0 19.1 18.4

17.6 3.5 15.7 62.6 19.6 -

15.8 3.5 26.2

Commersonia fraseri

Rulingra pannosa Thomasia sp. Acrostichum speciosum Pteris tremula

Rubiaceae

fru

glc

6.8 91.3

suc

tri

hex

myo-i scy-i chi-i pin

5.4 31.6 233.5

11.8 25.3

-

3.2

Meliaceae Meliaceae Meliaceae

63.5 96.5 100.2 7.7 8.4 32.8 84.8 75.2 119.8 -

16.6 5.4 32.7

Sterculiaceae Sterculiaceae Sterculiaceae Sterculiaceae

25.9 21.9 23.8 43.4

Pteridaceae Pteridaceae

23.4 12.2 20.8 28.9

54.1 52.0 105.9 79.5

33.0 5.2 22.2 86.7 6.3 20.6 56.4 43.4

-

0.9 -

2.4

que

3.5 -

4.2

0.6 12.8 35.7 10.3

-

E 88.5

4.4 72.0 88.5 175.1 145.9

-

1.2

Rubiaceae

5.6

0.6

369.8 45.9 25.3 2.2

+ -

302.1 56.5 312.5

1.9 -

90.9 76.0 173.3 107.3

71.4 -

236.7 228.8

6.9 4.1

- non detected. + detected, but in too low concentrations to be quantified. Fig. 5 (corresponding to Fig. 7, part I) includes those species with ion ratios or concentrations different from all other groups_ Hibiscus tiliaceus and Heritiera littoralis, two species without marked accumulation of Na+ and Cl-, also had low LMWC concentrations, however in other respects they differed little from salt-secreting species such as Acanthus ilicifolius and Avicennia marina (Fig. 1). The large difference between LMWC concentrations of young and old Heritiera littoralis leaves originated in part from the marked changes in water content in this species (part I). However, the usual decrease of LMWC was also observed when expressed on dry matter basis (young leaves 87.9 J.'mol· g-I dry matter, old leaves 32.8 p.mol· g-I dry matter). An appreciable amount of glucose was found in Scyphiphora hydrophylacea as well as high concentrations of mannitol. Thus, in young leaves of Scyphiphora hydrophyZ. Pjlanzenphysiol. Bd. 113. S. 411-421. 1984.

Low molecular weight carbohydrates in mangrove leaves

417

370

D

~ quebrachitol

200 ~

OJ J

I!Il young

fructose

f;;] glucose

nIl

o

~

c

.!!!

sucrose mannitol

II.

7

E 100

old

"0

E

E.a.

i

0.0.

[Q S.h.

H.t.

~ H.I.

Fig. 5: LMWC concentrations in young and old leaves of mangroves from various families. For explanations see Fig. 1. E.a. = Excoecaria agallocha (+91.8); 0.0. = Osbomea octodenta (-185.6); S.h. = Scyphiphora bydrophylacea (+308.1); H.t. = Hibiscus tiliaceus (-140.0); H.I. = Heritiera littoralis (-394.2).

lacea, LMWC accounted for 370 mol· m -3 pw, the highest value observed in all species under investigation. Osbomea octodenta was another species with limited LMWC accumulation in both young and old leaves although this fraction increased exceptionally in senescent leaves (Tab. 1). Quantitative conversion of sucrose to glucose and fructose concentrations for old leaves provided only a partial explanation for the observed increase in the two hexoses in senescent leaves. Quebrachitol, another cyclitol derived from myo-inositol (Kindl et a1. 1966), was stored by Excoecaria agallocha. Quebrachitol did not reach such high concentrations as pinitol in the Rhizophoraceae and made up for a smaller fraction, circa 50 % of LMWC. Some non-mangrove species were included in this investigation to enable consideration of hexitol and cyclitol occurrences on a taxonomic basis. Since non-mangrove Rhizophoraceae were not available Acrostichum speciosum, a fern occurring in the mangrove formation, was included as an example of a pinitol-accumulator. Mangrove and non-mangrove species taxonomically grouped by families are compared in Table2. Total LMWC concentrations were generally similar in members of the same family except the two members of the Rubiaceae, Scyphiphora hydrophylacea and Opercularia volubilis. The difference in LMWC concentrations between these two species was due to high mannitol storage by the mangrove species, whereas Z. Pjlanzenphysiol. Ed. 113. S. 411-421. 1984.

418

MARIANNE POPP

mannitol was not detectable in the non-mangrove relative. Since leaf age seems to be a very influential factor in LMWC content, it is not valid to place too much importance in quantitative contrasts between mangrove and non-mangrove species. Qualitatively, the non-mangrove species usually lacked those cyclitols (except myoinositol) and hexitols which were typical of their mangrove counterparts. Discussion

Polyols and cyclitols occur widely in the plant kingdom and are not restricted to halophilous species (Anderson and Wolter 1966; Kindl and Hoffmann-Ostenhof 1966; Hegnauer 1966, 1973; Karrer 1958; Lewis and Smith 1967; Holligan and Drew 1971; Diamantoglou 1974; Konigshofer et al. 1979; Smith and Phillips 1982). However, occurrence may refer to only trace amounts which is quite different from the accumulation which occurs in mangroves. Nevertheless, high amounts of pinitol, 25 to 33 mg . g-I dry matter, have been demonstrated in non-halophytes such as clover and soybean. That is approximately half of the pinitol concentration found in young leaves of Rhizophoraceae species. Pinitol concentrations reported for the halophyte, Spergularia media, were much lower (about 32 mol· m- 3 pw in both investigations, Albert and Popp 1978; Gorham et al. 1980) than those in mangroves (Figs. 2,3 a). Quantitative data on other cyclitols are scarce except for myo-inositol which is assumed to be the precursor of other cyclitols (Kindl et al. 1966). Myo-inositol, having a key function in metabolism, was, therefore, present in all species investigated, but as in other halophytes, never stored to great extent (Albert and Popp 1978). Chiroinositol made up 3 to 7 % of dry matter in the seagrass Cymodocea nodosa (Drew 1978), while it contributed only 1.2 % to the dry matter of Aegialitis annulata. Quebrachitol is a known constituent of Euphorbiaceae (Hegnauer 1966) and also present in leaves and bark of several trees (Acer, Aesculus; Karrer 1958). Quebrachitol accounted for about 2 % of dry matter in Acer campestre leaves (Diamantoglou 1974), and 3.5 % of dry matter in Excoecaria agallocha of the Euphorbiaceae. Mannitol is the most widely distributed polyol in angiosperms (Lewis and Smith 1967). It was present in sievetube exudates of Oleaceae and Combretaceae (Zimmermann and Ziegler 1975) and in the leaves of Myoporaceae and Rubiaceae (Hegnauer 1973). In Gardenia sp. (Rubiaceae), mannitol was accumulated to similar high extent, 8 % of dry matter, as in the related mangrove species, Scyphiphora hydrophy· lacea (Lewis and Smith 1967). The occurrence of specific polyols and cyclitols seems to be associated with taxonomic groupings, although this did not apply to own comparisons between mangrove and non-mangrove species from the same families (Table 2). But, those compounds reported for the Combretaceae, Rubiaceae and Euphorbiaceae in the literature were also the major compounds of the LMWC fraction in their respective mangrove species. Z. Pjlanzenphysiol. Bd. 113. S. 411-421. 1984.

Low molecular weight carbohydrates in mangrove leaves

419

Since pinitol was observed in 6 species of the Rhizophoraceae, more investigations on Rhizophora, Bruguiera, Ceriops and Kandelia species are needed to ascertain if pinitol accumulation is a physiotypical characteristic of the whole family (Albert and Kinzel 1973; Kinzel 1982). Polyol and cyclitol functions are difficult to assess as long as nothing is known about their compartmentation. Since high concentrations were observed it does not seem likely that they were located solely in the cytoplasm. The situation may be similar to that of proline in Nicotiana rustica (Pahlich et al. 1983). In non-stressed plants, proline was distributed between the vacuole and the cytoplasm rather equally while in water-stressed plants the proline distribution ratio changes to 1: 3 between vacuole and cytoplasm. Compatible solutes are also assumed to increase with increasing salt load. The reverse was true for mannitol and cyclitols in most of the mangrove species in this study. Moreover, for Ceriops tagal, a clear correlation between an increase in sol- and a decrease in pinitol was shown (Popp et al., in press). The high concentrations of pinitol in the relatively salt-poor hypocotyls of Rhizophora stylosa (Fig. 3 a) and Ceriops tagal (Popp et al., in press) suggest also that this substance functions not only as cytoplasmic, but also as cellular osmoticum. High concentrations of pinitol have not been tested for their effect on enzymes, because pinitol is commercially not available. Sorbitol was recently demonstrated to protect enzymes against heat inactivation (Smirnoff and Stewart, in press). This observation also favours the view that polyols and cyclitols are of importance to both plant compartments, cytoplasm and vacuole. Mangroves stored LMWC more commonly and to a greater extent than herbaceous halophytes (Albert and Popp 1978; Gorham et al. 1980, 1981; Briens and Larher 1982). Those halophytes which adapt osmotically by accumulating LMWC, accumulate primarily sucrose, glucose and fructose. There was only one mangrove, Xylocarpus granatum, which derived its LMWC concentration by storing these three sugars; all other mangroves which exclusively accumulated sugars were comparatively low in total LMWC concentration. Polyol and cyclitol occurrence is rather limited in halophytes (see Introduction), but 8 of the 22 mangrove species investigated stored cyclitols and 5 stored mannitol. Since little is known about the break-down pathways of these compounds, it is not known if concentration differences between young and old leaves are due to metabolism or transport. Pinitol, for instance, was reported as an inert end product in clover and soybean (Smith and Philipps 1982), and mannitol was regarded as a respiration substrate in the Phaeophyceae Fucus serratus (Kremer 1975). Further research is needed to elucidate this aspect of osmotic adaptation in mangroves. Acknowledgements This study was supported by grants from the H. and E. Walter-Stiftung (West Germany, Schimper-Fellowship 1981) and by the Austrian Science Research Fund (project No. P4051). The author expresses her gratitude to Dir. Dr. J. Bunt, E. Bunt and Dr. B. Clough (AIMS,

Z. Pjlanzenphysiol. Bd. 113. S. 411-421. 1984.

420

MARIANNE POpp

Townsville) for their kind help and support during sample collection. Gifts of pinitol, quebrachitol and chiro-inositol from the Institute of Biochemistry, University of Vienna are gratefully acknowledged. Thanks are due to Doz. Dr. J. Jurenitsch for identification of the hexitols using capillary GC, to Mag. V. Langer for technical assistance and to Dr. E. Kandeler, I. Holzapfel and M. Hinterleitner for help in preparing the final version of the manuscript. The author is especially grateful to A. Dickie for comments on the manuscript.

References AHMAD, I., F. LARHER, and G. R. STEWART: Sorbitol, a compatible osmotic solute in Plantago maritima. New Phytol. 82, 671-678 (1979). ALBERT, R. and H. KINZEL: Unterscheidung von Physiotypen bei Halophyten des Neusiedlerseegebietes (Osterreich). Z. Pflanzenphysiol. 70, 138-157 (1973). ALBERT, R. und M. POPP: Zur Rolle der loslichen Kohlenhydrate in Halophyten des Neusiedlersee-Gebietes (Osterreich). Oecol. Plant 13, 27-42 (1978). ANDERSON, L. and K. E. WOLTER: Cyclitols in plants: biochemistry and physiology. Ann. Rev. Plant Physiol. 17,209-222 (1966). BRiENs, M. and F. LARHER: Osmoregulation in halophytic higher plants: a comparative study of soluble carbohydrates, polyols, betains and free proline. Plant, Cell and Environment 5, 287-292 (1982). - - Sorbitol accumulation in Plantaginaceae; further evidence for a function in stress tolerance. Z. Pflanzenphysiol. 110,447-458 (1983). DIAMANTOGLOU, S.: Dber das physiologische Verhalten von Cycliten in vegetativen Teilen hoherer Pflanzen. Biochem. Physiol. Pflanzen 166, 511-523 (1974). DREW, E. A.: Carbohydrate and inositol metabolism in the seagrass, Cymodocea nodosa. New Phytol. 81, 249-264 (1978). GORHAM, J., L. L. HUGHES, and R. G. WYN JONES: Chemical Composition of salt-marsh plants from Ynys-Mon (Anglesey) - the concept of physiotypes. Plant, Cell and Environment 3, 309-319 (1980). GORHAM, J., L. L. HUGHES, and R. G. WYN JONES: Low-molecular-weight carbohydrates in some salt-stressed plants. Physiol. Plant 53, 27-33 (1981). HEGNAUER, R.: Chemotaxonomie der Pflanzen. Vol. VI Rafflesiaceae - Zygophyllaceae. Birkhauser, Basel, Stuttgart, 1973. - Chemotaxonomie der Pflanzen. Vol. IV Daphniphyllaceae - Lythraceae. Birkhauser, Basel, Stuttgart, 1966. HELLEBUST, J. A.: Osmoregulation. Ann. Rev. Plant Physiol. 21, 485-505 (1976). HOLLIGAN, P. M. and E. A. DREW: Routine analysis by gas-liquid chromatography of soluble carbohydrates in extracts of plant tissues. II Quantitative analysis of standard carbohydrates and the separation and estimation of soluble sugars and polyols from a variety of plant tissues. New Phytol. 70, 271-297 (1971). KARMARKAR, S. M.: Senescence in mangroves. In: D. N. SEN, K. S. RAJPUROHIT (eds.) Contributions to the ecology of halophytes, Tasks for vegetation science 2. Dr. W. Junk Publishers, The Hague, Boston, London, p. 173-187, 1982. KARRER, W.: Konstitution und Vorkommen der organischen Pflanzenstoffe. Birkhauser, Basel, Stuttgart, 1958. KiNDL, H. und O. HOFFMANN-OSTENHOF: Cyclite: Biosynthese, Stoffwechsel und Vorkommen. In: L. ZECHMEISTER (ed.), Fortschritte der Chemie organischer Naturstoffe. Springer, Wien, New York, Vol. 24, p. 150-205, 1966. KiNDL, H., R. SCHOLDA, and O. HOFFMANN-OSTENHOF: The biosynthesis of cyclitols. Angew. Chern. internat. Edit. 5, 165-173 (1966).

Z. Pjlanzenphysiol. Bd. 113. S. 411-421. 1984.

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