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Adaptive responses of roots and root systems to seasonal changes
Environmental and Experimental Botany, Vol. 33, No. l, pp. 175-188, 1993 Printed in Great Britain.
0098 8472]93 $6.00 + 0.00 © 1993 Pergamon Press Ltd
A D A P T I V E R E S P O N S E S OF R O O T S A N D R O O T SYSTEMS TO SEASONAL C H A N G E S MEI LIU, RUI-JUN LI and MING-YUAN LIU Department of Biology, Harbin Normal University, Harbin 150080, People's Republic of China
(Received 3 March 1992; acceptedin revisedform 11 April 1992) LIu M., LI R.-J. and LIu M.-Y. Adaptive responses of roots and root systems to seasonal changes. ENVIRONMENTALAND EXPnRIMENTALBOTANY33, 175--188, 1993.--The developmental rhythm and morphology of some perennial herbs in Heilongjiang province, China, have been observed over several years. In the present paper, the development of root systems of mature plants of four species is reviewed. The seasonal growth cycle of root and root system throughout one year is differentiated into three types: (i) renewal type, including partial renewal (Panax ginseng) and total renewal (Fritillaria ussuriensis), (ii) continuous growth (Asarum heterotropoides), and (iii) an intermediate type (Adonis amurensis). The developmental rhythm of the root system of P. ginseng is co-ordinated with the modern local climate, whereas the developmental rhythms of the other three species are not. These observations indicate that the seasonal growth cycle of a root system can be either the result of an adaptive response of the species to the particular environment in which it grows, or it is the outcome of its past ecological and evolutionary history. Chinese medicinal compounds of economic importance (e.g. ginsenoside) are found in roots and also show seasonal fluctuations.
berized portion of root on raspberry plants under irrigated conditions and found a clear seasonal peak in length, with much of the root produced THE phenology of growth and development during 1 year either dying or becoming suberized reflects both the genetic control of the plant and during the same year. I n apple, the rate of root the characteristics of the environment. T h e thickening was found to be low in J u n e and most degree of root branching and other growth rapid from mid-July to mid-September,/11/ and characteristics m a y exhibit both inter- and intraATKINSON(4) suggested that there are varying rates specific differences in the same environment./2~/ ZOBnL/25/ suggested that approximately 30% of of new growth in fruit trees at different times in the year. T h e roots of pot-grown pine seedlings the plant genome is involved in root growth ceased growth in October when summer ends and development. However, environmental charand, although the plants were transferred to acters such as soil conditions and normal seasonal w a r m greenhouses, this d o r m a n c y lasted until changes can have direct effects on the growth and mid-April./16~ It seems that the d o r m a n c y of the development of roots and root systems. (9-H'~5'~9) There have been m a n y studies on the seasonal root is a response to the season and can be explained as an adaptive strategy. pattern of root growth in fruit tree species/~'18/ Reserves for the survival of plants during the and conifers, 03'16'17) but little is known of this pattern in herbaceous plants. ATmNSON/2/ described winter, and for the resumption of growth in the a seasonal change in the length of the white unsu- spring, are very important. Seasonal fluctuations 175 INTRODUCTION
M. LIU et al.
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of carbohydrates and nitrogenous components in the roots of herbaceous perennials in temperate climes are strongly associated with their overwintering strategy. Studies on these components in the roots of perennial weeds have tbund that carbohydrates comprise the bulk of the reserve material./5-8/Starch content and nitrogenous compounds underwent significant seasonal fluxes, with sugars reaching a minimum in late autumn and ti'ee amino acids and soluble proteins reaching a maximum. For roots of fruit trees, the pattern is less clear or absent, possibly due to the fact that in the winter soil temperatures are usually higher than air temperatures./21/ In this study, we have selected four herbaceous perennial species of economic importance for observation of the seasonal pattern of roots and root systems. We investigated their growth and development, structure and morphology and, in some cases, the content of important metabolic reserves. While root growth has received considerable attention in the past, a consideration of the complete developmental rhythm of root and root system is obviously appropriate.
MATERIALS AND M E T H O D S
Study sites The studies were conducted in the Harbin (45°45'N, 126°30'E) and Wuchang (44°29'N, 127°31'E) counties of Heilong~iang province in Northeast China. The climate in this area belongs to the continental monsoon type. The summer is short and rainy with high temperatures; winter is long, cold and snowy. Spring and autumn are transitional seasons, the temperature being higher in spring than in autumn, whereas rainfall is greater in autumn than in spring. The average temperature of the coldest months is - 19.4°C in Harbin and - 1 9 . 1 ° C in Wuchang; the respective average rainfalls are 533 and 625 ram.
were collected at different stages of development (Table 1). Asarum heterotropoides Fr. Schmidt (Aristolochiaceae) is a shade plant. Plant material of this and the two other species referred to below were collected from the Botanical Garden of Harbin Normal University where the soil type is a chernozem. Four plants were collected at each developmental stage (Table 1). Fritillaria ussuriensis Maxim. (Liliaceae) is an early spring plant of semi-mountainous terrain and is tolerant of a colder climate. Three to four mature plants were collected at different stages (Table 1). Adonis amurensis Regel et Radde (Ranunculaceae) is also an early spring plant, distributed naturally in the mountains. Four plants were collected at different stages (Table 1).
Observation of root systems Root material collected at different stages in the year was brought to the laboratory, washed, observed and photographed with a Zeiss stereomicroscope. Some roots were fixed in FAA for anatomy and histochemistry. The usual method of dehydration through an alcohol series and embedding in paraffin wax was employed. Serial transections and longitudinal sections were cut at 6-8/tin thickness and stained with hematoxylin, safranin and fast green. Observation and photographs were made with an Olympus BH2 photomicroscope.
Analysis of volatile oil About 50 g of fresh roots ofA. heterotropoides at the different developmental stages were collected. Volatile oil was extracted by steam distillation, washed in 1% Na2CO 3 solution and then in 1% N a O H solution. Total oil content was determined as ml/100 g FW. RESULTS
Plant materials Panax ginseng Mey. (Araliaceae)
(ginseng) grows naturally in mixed forests of coniferous and broad-leaf trees. The material used in this study was 2- to 6-year-old cultivated plants collected from a ginseng farm in Wuchang county. The soil type in this area is dark brown earth. Two plants
Panax ginseng The root system of ginseng is a tap root system. The main root of a 1-year-old ginseng plant develops from the radicle. Lateral root primordia arise from the pericycle. Adventitious roots, which have the same morphology and structure as lateral roots, develop from the rhizome of 2-
ROOT RESPONSES TO SEASONAL CHANGES
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Table 1. Timing of various stages of development throughout the year in four species of perennial herbs; the root systems were studied in the months shown
Species/Month m
Panax ginseng
Developmental stage Sprouting Expanded leaves Flowering Fruiting Post-fruiting Withered Underground growth Non-growing, over-wintering
Early May Late May Mid-June Late June early August Late September Mid-October * Mid -October
Asarum heterotropoides
~ April / May ) } July-August
Fritillaria ussuriensis
March April May June June
_
•
Adonis amurensis
Mid-February Mid-March Late April Early June
September-October July August September-October Late August * Late October November November
* This stage was absent. year-old plants. Lateral or adventitious roots can similarly give rise to additional branches later on. The development of mature plants during the period of a year can be divided into seven stages (Table 1). The development of absorbing roots, the growth pattern of resin ducts, and the presence of metabolic substances in the root system show seasonal changes throughout the year. Absorbing roots are developed from the winter root primordia (WRP). WRP often originate within lateral or adventitious roots near the base of withered, previously formed absorbing roots of the second or third order, i.e. in the angle between roots (Fig. 1, arrow B). A few WRP originate from the non-axillary parts of the adventitious root (Fig. 1, arrow C). W R P initiate late in the growing stage (green fruit stage in late June-early July), when the bases of the absorbing roots begin to wither (Fig. 1, arrow A). They then enlarge after the fruiting stage (late September), and become dormant when the nearby axes wither completely (mid-October). They resume growth to form new absorbing roots in the following spring (early May, mid-June) (Fig. 1, arrows D and E). When the bases of the absorbing roots begin to wither, the pericycle, phelloderm and cork cambium ceils become active in regions of the parent axis where the absorbing roots are connected (Fig. 2A). Periclinal and anticlinal divisions of
these cells form several layers (Fig. 2B) and the derivatives of further divisions constitute an incipient primordium (Fig. 2C and Fig. 1, arrow B). The base of the absorbing roots finally withers at this time (Fig. 1). The primordium then grows by a series of periclinal and anticlinal divisions (Fig. 2D) establishing the structure of the vascular cylinder, cortex and root cap-epidermis complex. The primordium is covered by a sheath composed of layers of cork cells that are continuous with that of the parent axis. Resin is present between the primordium and the cork sheath (Fig. 3A, arrow). As the above-ground part of the plant withers, the absorbing roots of the last order abscind either partly or completely. The primordium enlarges slightly and the cavity between the primordium and the cork sheath also enlarges. At this point, all primordia enter a dormant state and are termed 'winter root primordia' (WRP) (Fig. 3B). Following an over-wintering period, the W R P continue to develop and enlarge during springtime (Fig. 1, arrows D and E). The space between the primordium and cork sheath shrinks. The tip of the sheath thins and the resin decreases (Fig. 3C). The WRP then grow through the cork sheath, the root tips emerge (Fig. 3D), and vascular tissue of each W R P connects with that of the parent lateral or adventitious root. The root tips grow further and form new absorbing roots. These
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Late Juneearly July
Late Sept.
Mid.- Oct.
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Mid.- June
FIG. 1. Yearly rhythm of root system development of Panax ginseng.
absorbing roots branch and form new absorbing roots up to the second or third order. Resin ducts are distributed in roots of ginseng, and comprise primary and secondary resin ducts (Fig. 4A, arrows a and b, respectively). Primary resin ducts originate from the pericycle and are produced once during the life of the root. Secondary resin.ducts originate from the cambium and are produced in a ring within the secondary phloem opposite the secondary xylem (Fig. 4B, arrow c). The number of resin ducts is small initially but increases gradually during later growth. Seasonal changes of carbohydrate and ginsenoside in root systems of 5- and 6-year-old plants are similar/14/ (Fig. 5). The content of glucose in roots is higher throughout winter than in spring, whereas starch is lower. When plants are flowering (June), the glucose content of the root increases to a maximum and starch is minimal. From late June, glucose decreases rapidly and starch gradually accumulates (Fig. 5 B,C). This pattern coincides with the appearance of radial fissures, seen in transverse sections: fissures are largest when the glucose content is highest (Fig. 4C), but decrease and disappear when the glucose level is minimal in early September (Fig. 4D). During overwintering and development of winter buds, starch in the roots changes into soluble
carbohydrate. At the same time, some small new fissures appear. Seasonal fluctuations of ginsenoside (Fig. 5A), a secondary chemical substance, are less obvious than those of glucose and starch. The highest content coincides with that of glucose. Asarum heterotropoides
After the seed is shed, the roots germinate but the plumules do not emerge (Fig. 6A). These remain dominant throughout winter and emerge the following year. A 1-year-old plant with a primary root and lateral roots forming in a root system is shown in Fig. 6B. One to three adventitious roots develop from each node of the rhizome in 2-year-old plants (Fig. 6C). The number of adventitious roots increases with age (Fig. 6D). The primary root usually stops growing and withers after 3-5 years. Adventitious roots (one to three per node of rhizome) replace the tap root system and comprise a fibrous root system (Fig. 6E). The development of mature plants can be divided into five stages (Table 1) and the corresponding characteristics of the root system are as follows: the root system grows rapidly as new adventitious roots emerge from the rhizomes. Old adventitious roots produce new branches and the tips continue extending after the fruiting stage.
R.OOT R E S P O N S E S T O S E A S O N A L C H A N G E S
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FIG. 2. A D . Longitudinal sections of Panax ginseng showing the initiation and development of WRP. a . Pericycle, phelloderm and cork c a m b i u m cells divide in lateral or adventitious roots eommeting with the hases of ahsorbing roots that are beginning to wither. B. Perielinal divisions ti'om several layers of cells. T h e withered absorbing root is on the left. C. T h e dcri\'alives of earlier divisions constitute an incipient primordium. D. T h e main body of a primordium. Bars, 100/~m.
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FIG. 3. A D. Longitudinal sections of" ginseng roots showing the development of WRP. A. The structure of the vascular cylinder, cortex and rootcap epidermis complex is seen in the primordium. The outside of the primordium is covered by a cork sheath. There is resin between the primordium and cork sheath (arrow). B. The W R P enlarges and the space between primordiuin and cork sheath also enlarges. (I. The W R P enlarges further, the space between primordium and cork sheath becomes smaller. The top of the cork sheath thins and resin decreases. 1). The W R P grows through tile cork sheath and the root tip emcrges. Bars, 100 Iml.
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Fro. 4. Transverse sections of roots stained with safranin and fast green (A,B), PAS (C,D) or safranin (E-G). A. One-year-old ginseng root showing primary and secondary resin ducts (arrow labelled 'a' and 'b'). B. Three-year-old ginseng root showing the newly differentiated secondary resin ducts (arrow labelled 'c'). C. Ginseng root in spring showing fissures. D. Ginseng root in summer. The fissures have disappeared. E G. The structure of adventitious roots of (E) Asarum helerolropoide,~, (F) b)ilillaria ussuriensis, and ((;) Adoni,~ amurensi.~. Bars, 100 l~m.
ROOT RESPONSES TO SEASONAL CHANGES
heterotropoides increases from a minimum in early spring (April), to a peak 1 month later, at which time the plants are flowering. It then decreases rapidly and remains at a constant level from summer to winter (Fig. 7).
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In winter, the above-ground parts of the plant wither, but the root system grows slowly and winter buds enlarge. Growth of the root system accelerates in July of the following year. The colour of the root changes from white to yellow as the root ages. Roots of A. heterotropoides continue to grow for at least 10 years during which time they retain a mainly primary structure (i.e. without secondary tissues) (Fig. 4E). The content of volatile oil found in roots of A.
Fritillaria ussuriensis It takes 6 years from seed germination for plants ofFritillaria ussuriensis to mature. Seeds are shed in early August, germinate, and the radicle elongates and develops into the main root. The plumule emerges and forms a leaf during winter. The hypocotyl enlarges and forms the bulb. The fibrous root system comprises adventitious roots arising from the base of the bulb. The roots show a primary structure throughout their life (Fig. 4F). The development of a mature plant throughout a year can be divided into six stages (Fig. 8) (Table 1). Roots and buds begin to grow in March. Bulbils, 102 m m in diameter, develop from the edge of the scale leaves; roots elongate further when the leaves expand (April); roots arise from the bulbils at the same time. When flowering occurs (May), the root system grows slowly and the scale leaves become translucent and membranous. Bulbils fall and form new plantlets. A new bulb is formed in the basal plate. At this stage, the root system stops growing, the membranous scale leaves wither and the new bulb enlarges during the fruiting stage (June). In J u l y August, the root system withers, the old scale leaves are shed and the new bulb enlarges further and becomes dormant. However, in SeptemberOctober root primordia develop into a new fibrous root system, buds sprout and bulbils are differentiated on the edge of the scale leaves in the growing underground part. When the soil is frozen, plants are forced into winter dormancy (late October-early March). Adonis amurensis After seed germination and a year-long seedling stage, the radicle develops a tap root system, which includes main root and lateral roots. Adventitious roots are produced from nodes which bear sheath-like leaves on 2-year-old seedlings. These roots increase in the following year. The primary root, however, grows slowly, begins to wither and finally the tap root system changes
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FxG. 6. The external developmental morphology of the root system of Asarum heterotropoides.
into a fibrous root system. The vegetative growth stage ofA. amurensis lasts for at least 6 years. After entering the sexually reproductive phase, the development of the mature plant during the year can be divided into six stages (Fig. 9) (Table 1). Buds sprout in early spring (mid-February)
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FIO. 7. Seasonal pattern of volatile oil (ml per 100 g fresh weight) in roots in Asarum heterotropoides.
and flower (mid-March). The root system does not grow at this time and roots are yellow- or reddish-brown. W h e n the leaves have expanded, fruits are borne (late April) and new adventitious roots arise from the rhizome. These roots are white and unbranched. Branches are developed later and the new roots change gradually from white to light yellow or brown. The older roots can also branch or their tips renew growth. The new roots turn dark yellow-brown and stop growing in a withered and d o r m a n t state in summer (early June). The root system recommences growth during an underground growing stage in a u t u m n (late August) and is similar to that of the early growth stage; d o r m a n t buds enlarge. The root system finally stops increasing (November). The older roots change from dark yellow to red or black-brown while new roots show some slight growth. The roots which are white to light yellow-
ROOT RESPONSES TO SEASONAL CHANGES March
April
May
June, July and Aug.
Sept.
185 Oct.
Fro. 8. Yearly rhythm of root system development of a mature plant of Fritillaria
ussuriensis.
brown are closest to the shoot apex and were formed in the current year. Two-year-old roots are red-brown, and are located further back. Roots older than 3 years are black-brown, and are furthest from the shoot apex. The roots retain a primary structure throughout their life (Fig. 4G). Figure 10 indicates the level of cardiac glycoside in roots of different developmental stages. (23/ Cardiac glycoside decreases from a maximum in early spring to a minimum during late spring and early summer. When plants are in summer dormancy, glycoside increases gradually from the summer minimum and remains high during the autumn. DISCUSSION
The developmental characteristics of the root system in the four species included in the present
study include one of renewal, i.e. the growing points of the root systems of mature plants, with either a tap root or a fibrous root system, usually renew. Three different patterns of root system development were encountered within a year: (i) The renewal type. This includes the partial renewal and the total renewal type. In the partial renewal type, absorbing roots wither and abscind before the winter, and dormant (WRP) primordia are produced near the base of withered absorbing roots and develop into new absorbing roots in the following spring (e.g. Panax ginseng). In the total renewal type the whole root system withers and abscinds in a given season. A new root system is produced at a suitable time in the same year (e.g. Fritillaria ussuriensis). (ii) The continuous growth type. The growing points of the root system slow their elongation in winter, but continue in the following spring (e.g.
Asarum heterotropoides ).
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M. LIU et al. Mid.- Feb.
Mid.- March
Late April
Early Jane
Late August
November
÷ I~ New absorbent root
I | Root the some year
~ Withered root
II o,d root
| New
| Root Item
root
FIG. 9. Yearly rhythm of root system development of a mature plant of Adonis amurensis.
(iii) The intermediate type. A new set of roots is produced once; their growing points do not die but continue after the overwintering stage. However, some older absorbing roots do die, but there is also formation of new root primordia which develop into new absorbing roots, i.e. new roots do not turn-over, but the older roots do so (e.g. Adonis amurensis ). Our results indicate that, depending on the species, the growth and development of root systems of mature plants, especially the renewal behaviour of absorbing roots, have different
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FIG. 10. Seasonal pattern of cardiac glycoside (g per 100 g dry weight) in roots of, Adonis amurensis. After WANG et al. (23)
adaptive patterns to seasonal change. A possible explanation of the partial renewal of the root system in Panax ginseng lies in its adaptation to the rhythm of the modern local climate. Late in the growing season, many absorbing roots begin to wither, die and abscind. At this time, WRPs are covered with their cork sheath. They will develop as new absorbing roots in the next growing season. These developmental characteristics may be advantageous to the plants, enabling them to adapt to colder winters in temperate climes. A cyto-geographic analysis o f Panax showed that P. ginseng is a polyploid species which has developed in one group of the genus as an adaptation suitable to the harsh mountain climates in Northeast China during its northbound migration. I24) Another renewal type, total renewal, is not coordinated with the modern local climate. Fritillaria ussuriensis is an early spring plant. Its growing period lasts about 4 months (April to J u l y August). The roots wither and fall when the aboveground part withers upon bearing fruits (July-August), and the plants become dormant during the summer (this period is the growing season for other species). In autumn new adventitious roots are formed, and these roots comprise
ROOT RESPONSES TO SEASONAL CHANGES a new root system which survives the winter. In temperate regions the change between warmer summer and colder winter profoundly affects the developmental rhythm of many species. Clearly, this adaptation of the root system of FritiUaria ussuriensis to seasonal change may reflect the fact that this taxon was formed during the Ice Age and retains some characteristics for adaptation to a cold climate. In the studies of the Arctic tundra by SHAVER and BILLINGS,(20) roots of Eriophorum angustifolium are annual, and hence an entirely new root system is produced each year. This developmental pattern of the root system constitutes a particular evolutionary strategy in the Arctic environment, and differs from that adopted by F. ussuriensis, even though this plant is tolerant of cold habitats. The developmental characteristics of root systems of continuous growth and intermediate types are also not co-ordinated with the local climate. The continuous growth characteristic of Asarum heterotropoides may indicate that this species evolved in a zone where the seasons were undifferentiated, but the roots still show some features that are not adapted to the present-day climate. The intermediate type shown by Adonis amurensis has obviously adapted positively to the modern climate by showing two periods of dormancy during the year. Root systems of all plants may be divided simply into either a tap root system or a fibrous root system. It is noteworthy that there are several different groups of herbaceous perennials that can be classified in terms of the development of their underground part (especially the root system) during a year. This pattern of seasonal growth which a species exhibits is established as a result of adaptation to the particular environment in which it currently grows, or as an outcome of its past ecological and evolutionary history. The perennial plants of temperate climes mostly exhibit a seasonal pattern of growth and development. Because the aerial portions of herbaceous perennials do not survive the winter, their root systems undergo extensive physiological changes during the overwintering period and regrow in the spring. The seasonal fluctuations of carbohydrate and nitrogenous components in these roots are strongly associated with their overwintering strategy. (5 8) The increase in soluble
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carbohydrates of ginseng roots during the late autumn and early winter coincides with a decline in starch. Maintenance respiration during overwintering and rapid growth during early spring probably account for a significant proportion of the carbon lost from the storage carbohydrate. Many radicular fissures appear, and the level of ginsenoside increases in this period. KIM et al. ~21 found that two groups of biologically active dammarane-saponins showed a seasonal variation and they noticed higher levels in roots in summer. LI eta/. (14) also found that ginsenoside levels in roots were significantly higher in summer than in winter and that accumulation of ginsenoside was inversely related to the level of starch. However, seasonal patterns of cardiac glycoside in roots of Adonis amurensis are different from those of ginsenoside. The glycoside decreased in the spring and early summer, and increased from mid-summer to winter. The change of volatile oil in roots of Asarum heterotropoides was only associated with flowering and did not reflect any obviously seasonal pattern. Accumulation of secondary metabolic materials can be related with primary metabolism. It is also necessary to understand thoroughly the role played by these substances since they may also be adaptive responses of the root to seasonal change. Acknowledgement--We wish to thank Dr P. W. Barlow for his helpful comments. REFERENCES
1. ATKINSOND. (1972) Seasonal periodicity of blackcurrant root growth and the influence of simulated mechanical harvesting. J. Hortic. Sci. 47, 165-172. 2. ATKINSOND. (1973) Seasonal changes in the length of white unsuberized root on raspberry plants grown under irrigated conditions. J. Hortic. Sci. 48, 413M.19. 3. ATKINSOND. (1980) The growth and activity of fruit tree root systems under simulated orchard conditions. Pages 171-185 in D. E. SEN, ed. Environment and root behaviour. Geobios International, Jodhpur, India. 4. ATKINSOND. (1983) The growth, activity and distribution of the fruit tree root. Pages 23-35 in D. ATKINSON,K. K. S. BHAT, M. P. COUTTS, P. A. MASONand D. J. READ, eds Tree root systems and their mycorrhizas. Martinus Nijhoff, The Hague.
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15. MUROMTSEVI. A. (1984) Active parts of root system 5. CVR D. R. and BEWLEVJ. D. (1989) Carbon and of fruit plants. Amerind Publishing, New Delhi. nitrogen reserves of leafy spurge (Euphorbia esula) 16. ORLOV A. Y. (1980) Cyclic development of roots roots as related to overwintering strategy. Phyof conifers and their relation to environmental facsiologia Pl. 77, 67-72. 6. CYR D. R. and BEWLEY J. D. (1990) Annual tors. Pages 43-61 in D. E. SEN, ed. Environmental rhythmicity of nitrogen reserves in the roots of and root behaviour. Geobios International, Jodhpur, pernicious perennial weeds. British Society for Plant India. Growth Regulation, Monograph 21,353-368. 17. PERSSONH. A. (1983) The distribution and pro7. CYR D. R. and BEWLEYJ. D. (1990) Seasonal ductivity of fine roots in boreal forests. Pages 87variation in nitrogen storage reserves in the roots 101 in D. ATKINSON,K. K. S. BHAT, M. P. COUTTS, of leafy spurge (Euphorbia esula) and responses to P. A. MASONand D.J. READ,eds Tree root systems decapitation and defoliation. Physiologia Pl. 78, and their mycorrhizas. Martinus Nijhoff, The Hague. 361-366. 18. ROGERS W. S. and HEAD G. C. (1969) Factors 8. CYR D. R. and BEWLEYJ. D. (1990) Seasonal affecting the distribution and growth of roots of dynamics of carbohydrate and nitrogenous comperennial woody species. Pages 280-292 in W. J. ponents in the roots of perennial weeds. Pl. Cell WHITTINGTON,ed. Root growth. Butterworths, LonEnvir. 13, 359-365. don. 9. HEAD G. C. (1966) Estimating seasonal changes 19. RUSSELLR. S. (1977) Plant root systems: theirfunctions in the quantity of white unsuberized root on fruit and interaction with the soil. McGraw-Hill, London. trees. J. Hortic. Sci. 41, 197-206. 20. SHAVER G. R. and BILLINGSW. D. (1975) Root 10. HEAD G. C. (1967) Effects of seasonal changes in production and root turnover in a wet tundra ecoshoot growth on the amount of unsuberized root system, Barrow, Alaska. Ecology 56, 401 409. on apple and plum trees. J. Hortic. Sci. 42, 16921. TROMPJ. (1983) Nutrient reserves in roots of fruit 180. trees, in particular carbohydrates and nitrogen. I 1. HEADG. C. (1968) Seasonal changes in the diamPages 401-413 in D. ATKINSON,K. K. S. BHAT, eter of secondarily thickened roots of fruit trees in M. P. COUTTS,P. A. MASONand D.J. READ, eds relation to growth of other parts of the tree. J. Tree root systems and their mycorrhizas. Martinus Hortic. Sci. 43, 275-282. Nijhoff, The Hague. 12. RIM S. K., SAKAMOTOI., MORIMOTOK., SAKATA 22. TROUGHTONA. and WHITTINGTONW. J. (1969) M., YAMASAKIK. K. and TANAKA O. (1981) The significance of genetic variation in root Seasonal variation ofsaponins, sucrose and monosystems. Pages 296-313 in W.J. WHITTINGTON,ed. saccharides in cultivated ginseng roots. Pl. Med. Root growth. Butterworths, London. 42, 181 186. 13. LANGLOISC. G., GODBOUTL. and FORTINJ. A. 23. WANG D., Ltu M., Liu L., LI R. and Liu M. (1991) Dynamics of cardiac glycoside in roots of (1983) Seasonal variation of growth and develAdonis amurensis at different developmental stages. opment of the roots of five second-year conifer J. Chin. Med. Mater. 14, 7-8 (in Chinese). species in the nursery. Pages 35 62 in D. ATKINSON, 24. YANG D. (1981) The cyto-taxonomic studies on K. K. S. BHAT, M. P. COUTTS, P. A. MASONand some species of Panax L. Acta Phytotaxon. Sin. 19, D.J. READ, eds Tree root systems and their mycorrhizas. 298-303 (in Chinese with English summary). Martinus Nijhoff, The Hague. 14. LI S., CHUI S., Lo W., WANG Y. and WANG Z. 25. ZOBEL R. W. (1975) The genetics of root devel(1988) Studies on the dynamics of active comopment. Pages 261-275 in J. G. TORREY and D. ponents of roots in Panax ginseng. Ginseng Research T. CLARKSON, eds The development and function of 1, 42-48 (in Chinese). roots. Academic Press, London.
0098 8472]93 $6.00 + 0.00 © 1993 Pergamon Press Ltd
A D A P T I V E R E S P O N S E S OF R O O T S A N D R O O T SYSTEMS TO SEASONAL C H A N G E S MEI LIU, RUI-JUN LI and MING-YUAN LIU Department of Biology, Harbin Normal University, Harbin 150080, People's Republic of China
(Received 3 March 1992; acceptedin revisedform 11 April 1992) LIu M., LI R.-J. and LIu M.-Y. Adaptive responses of roots and root systems to seasonal changes. ENVIRONMENTALAND EXPnRIMENTALBOTANY33, 175--188, 1993.--The developmental rhythm and morphology of some perennial herbs in Heilongjiang province, China, have been observed over several years. In the present paper, the development of root systems of mature plants of four species is reviewed. The seasonal growth cycle of root and root system throughout one year is differentiated into three types: (i) renewal type, including partial renewal (Panax ginseng) and total renewal (Fritillaria ussuriensis), (ii) continuous growth (Asarum heterotropoides), and (iii) an intermediate type (Adonis amurensis). The developmental rhythm of the root system of P. ginseng is co-ordinated with the modern local climate, whereas the developmental rhythms of the other three species are not. These observations indicate that the seasonal growth cycle of a root system can be either the result of an adaptive response of the species to the particular environment in which it grows, or it is the outcome of its past ecological and evolutionary history. Chinese medicinal compounds of economic importance (e.g. ginsenoside) are found in roots and also show seasonal fluctuations.
berized portion of root on raspberry plants under irrigated conditions and found a clear seasonal peak in length, with much of the root produced THE phenology of growth and development during 1 year either dying or becoming suberized reflects both the genetic control of the plant and during the same year. I n apple, the rate of root the characteristics of the environment. T h e thickening was found to be low in J u n e and most degree of root branching and other growth rapid from mid-July to mid-September,/11/ and characteristics m a y exhibit both inter- and intraATKINSON(4) suggested that there are varying rates specific differences in the same environment./2~/ ZOBnL/25/ suggested that approximately 30% of of new growth in fruit trees at different times in the year. T h e roots of pot-grown pine seedlings the plant genome is involved in root growth ceased growth in October when summer ends and development. However, environmental charand, although the plants were transferred to acters such as soil conditions and normal seasonal w a r m greenhouses, this d o r m a n c y lasted until changes can have direct effects on the growth and mid-April./16~ It seems that the d o r m a n c y of the development of roots and root systems. (9-H'~5'~9) There have been m a n y studies on the seasonal root is a response to the season and can be explained as an adaptive strategy. pattern of root growth in fruit tree species/~'18/ Reserves for the survival of plants during the and conifers, 03'16'17) but little is known of this pattern in herbaceous plants. ATmNSON/2/ described winter, and for the resumption of growth in the a seasonal change in the length of the white unsu- spring, are very important. Seasonal fluctuations 175 INTRODUCTION
M. LIU et al.
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of carbohydrates and nitrogenous components in the roots of herbaceous perennials in temperate climes are strongly associated with their overwintering strategy. Studies on these components in the roots of perennial weeds have tbund that carbohydrates comprise the bulk of the reserve material./5-8/Starch content and nitrogenous compounds underwent significant seasonal fluxes, with sugars reaching a minimum in late autumn and ti'ee amino acids and soluble proteins reaching a maximum. For roots of fruit trees, the pattern is less clear or absent, possibly due to the fact that in the winter soil temperatures are usually higher than air temperatures./21/ In this study, we have selected four herbaceous perennial species of economic importance for observation of the seasonal pattern of roots and root systems. We investigated their growth and development, structure and morphology and, in some cases, the content of important metabolic reserves. While root growth has received considerable attention in the past, a consideration of the complete developmental rhythm of root and root system is obviously appropriate.
MATERIALS AND M E T H O D S
Study sites The studies were conducted in the Harbin (45°45'N, 126°30'E) and Wuchang (44°29'N, 127°31'E) counties of Heilong~iang province in Northeast China. The climate in this area belongs to the continental monsoon type. The summer is short and rainy with high temperatures; winter is long, cold and snowy. Spring and autumn are transitional seasons, the temperature being higher in spring than in autumn, whereas rainfall is greater in autumn than in spring. The average temperature of the coldest months is - 19.4°C in Harbin and - 1 9 . 1 ° C in Wuchang; the respective average rainfalls are 533 and 625 ram.
were collected at different stages of development (Table 1). Asarum heterotropoides Fr. Schmidt (Aristolochiaceae) is a shade plant. Plant material of this and the two other species referred to below were collected from the Botanical Garden of Harbin Normal University where the soil type is a chernozem. Four plants were collected at each developmental stage (Table 1). Fritillaria ussuriensis Maxim. (Liliaceae) is an early spring plant of semi-mountainous terrain and is tolerant of a colder climate. Three to four mature plants were collected at different stages (Table 1). Adonis amurensis Regel et Radde (Ranunculaceae) is also an early spring plant, distributed naturally in the mountains. Four plants were collected at different stages (Table 1).
Observation of root systems Root material collected at different stages in the year was brought to the laboratory, washed, observed and photographed with a Zeiss stereomicroscope. Some roots were fixed in FAA for anatomy and histochemistry. The usual method of dehydration through an alcohol series and embedding in paraffin wax was employed. Serial transections and longitudinal sections were cut at 6-8/tin thickness and stained with hematoxylin, safranin and fast green. Observation and photographs were made with an Olympus BH2 photomicroscope.
Analysis of volatile oil About 50 g of fresh roots ofA. heterotropoides at the different developmental stages were collected. Volatile oil was extracted by steam distillation, washed in 1% Na2CO 3 solution and then in 1% N a O H solution. Total oil content was determined as ml/100 g FW. RESULTS
Plant materials Panax ginseng Mey. (Araliaceae)
(ginseng) grows naturally in mixed forests of coniferous and broad-leaf trees. The material used in this study was 2- to 6-year-old cultivated plants collected from a ginseng farm in Wuchang county. The soil type in this area is dark brown earth. Two plants
Panax ginseng The root system of ginseng is a tap root system. The main root of a 1-year-old ginseng plant develops from the radicle. Lateral root primordia arise from the pericycle. Adventitious roots, which have the same morphology and structure as lateral roots, develop from the rhizome of 2-
ROOT RESPONSES TO SEASONAL CHANGES
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Table 1. Timing of various stages of development throughout the year in four species of perennial herbs; the root systems were studied in the months shown
Species/Month m
Panax ginseng
Developmental stage Sprouting Expanded leaves Flowering Fruiting Post-fruiting Withered Underground growth Non-growing, over-wintering
Early May Late May Mid-June Late June early August Late September Mid-October * Mid -October
Asarum heterotropoides
~ April / May ) } July-August
Fritillaria ussuriensis
March April May June June
_
•
Adonis amurensis
Mid-February Mid-March Late April Early June
September-October July August September-October Late August * Late October November November
* This stage was absent. year-old plants. Lateral or adventitious roots can similarly give rise to additional branches later on. The development of mature plants during the period of a year can be divided into seven stages (Table 1). The development of absorbing roots, the growth pattern of resin ducts, and the presence of metabolic substances in the root system show seasonal changes throughout the year. Absorbing roots are developed from the winter root primordia (WRP). WRP often originate within lateral or adventitious roots near the base of withered, previously formed absorbing roots of the second or third order, i.e. in the angle between roots (Fig. 1, arrow B). A few WRP originate from the non-axillary parts of the adventitious root (Fig. 1, arrow C). W R P initiate late in the growing stage (green fruit stage in late June-early July), when the bases of the absorbing roots begin to wither (Fig. 1, arrow A). They then enlarge after the fruiting stage (late September), and become dormant when the nearby axes wither completely (mid-October). They resume growth to form new absorbing roots in the following spring (early May, mid-June) (Fig. 1, arrows D and E). When the bases of the absorbing roots begin to wither, the pericycle, phelloderm and cork cambium ceils become active in regions of the parent axis where the absorbing roots are connected (Fig. 2A). Periclinal and anticlinal divisions of
these cells form several layers (Fig. 2B) and the derivatives of further divisions constitute an incipient primordium (Fig. 2C and Fig. 1, arrow B). The base of the absorbing roots finally withers at this time (Fig. 1). The primordium then grows by a series of periclinal and anticlinal divisions (Fig. 2D) establishing the structure of the vascular cylinder, cortex and root cap-epidermis complex. The primordium is covered by a sheath composed of layers of cork cells that are continuous with that of the parent axis. Resin is present between the primordium and the cork sheath (Fig. 3A, arrow). As the above-ground part of the plant withers, the absorbing roots of the last order abscind either partly or completely. The primordium enlarges slightly and the cavity between the primordium and the cork sheath also enlarges. At this point, all primordia enter a dormant state and are termed 'winter root primordia' (WRP) (Fig. 3B). Following an over-wintering period, the W R P continue to develop and enlarge during springtime (Fig. 1, arrows D and E). The space between the primordium and cork sheath shrinks. The tip of the sheath thins and the resin decreases (Fig. 3C). The WRP then grow through the cork sheath, the root tips emerge (Fig. 3D), and vascular tissue of each W R P connects with that of the parent lateral or adventitious root. The root tips grow further and form new absorbing roots. These
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~
Late Juneearly July
Late Sept.
Mid.- Oct.
Early May
Mid.- June
FIG. 1. Yearly rhythm of root system development of Panax ginseng.
absorbing roots branch and form new absorbing roots up to the second or third order. Resin ducts are distributed in roots of ginseng, and comprise primary and secondary resin ducts (Fig. 4A, arrows a and b, respectively). Primary resin ducts originate from the pericycle and are produced once during the life of the root. Secondary resin.ducts originate from the cambium and are produced in a ring within the secondary phloem opposite the secondary xylem (Fig. 4B, arrow c). The number of resin ducts is small initially but increases gradually during later growth. Seasonal changes of carbohydrate and ginsenoside in root systems of 5- and 6-year-old plants are similar/14/ (Fig. 5). The content of glucose in roots is higher throughout winter than in spring, whereas starch is lower. When plants are flowering (June), the glucose content of the root increases to a maximum and starch is minimal. From late June, glucose decreases rapidly and starch gradually accumulates (Fig. 5 B,C). This pattern coincides with the appearance of radial fissures, seen in transverse sections: fissures are largest when the glucose content is highest (Fig. 4C), but decrease and disappear when the glucose level is minimal in early September (Fig. 4D). During overwintering and development of winter buds, starch in the roots changes into soluble
carbohydrate. At the same time, some small new fissures appear. Seasonal fluctuations of ginsenoside (Fig. 5A), a secondary chemical substance, are less obvious than those of glucose and starch. The highest content coincides with that of glucose. Asarum heterotropoides
After the seed is shed, the roots germinate but the plumules do not emerge (Fig. 6A). These remain dominant throughout winter and emerge the following year. A 1-year-old plant with a primary root and lateral roots forming in a root system is shown in Fig. 6B. One to three adventitious roots develop from each node of the rhizome in 2-year-old plants (Fig. 6C). The number of adventitious roots increases with age (Fig. 6D). The primary root usually stops growing and withers after 3-5 years. Adventitious roots (one to three per node of rhizome) replace the tap root system and comprise a fibrous root system (Fig. 6E). The development of mature plants can be divided into five stages (Table 1) and the corresponding characteristics of the root system are as follows: the root system grows rapidly as new adventitious roots emerge from the rhizomes. Old adventitious roots produce new branches and the tips continue extending after the fruiting stage.
R.OOT R E S P O N S E S T O S E A S O N A L C H A N G E S
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D
FIG. 2. A D . Longitudinal sections of Panax ginseng showing the initiation and development of WRP. a . Pericycle, phelloderm and cork c a m b i u m cells divide in lateral or adventitious roots eommeting with the hases of ahsorbing roots that are beginning to wither. B. Perielinal divisions ti'om several layers of cells. T h e withered absorbing root is on the left. C. T h e dcri\'alives of earlier divisions constitute an incipient primordium. D. T h e main body of a primordium. Bars, 100/~m.
180
FIG. 3. A D. Longitudinal sections of" ginseng roots showing the development of WRP. A. The structure of the vascular cylinder, cortex and rootcap epidermis complex is seen in the primordium. The outside of the primordium is covered by a cork sheath. There is resin between the primordium and cork sheath (arrow). B. The W R P enlarges and the space between primordiuin and cork sheath also enlarges. (I. The W R P enlarges further, the space between primordium and cork sheath becomes smaller. The top of the cork sheath thins and resin decreases. 1). The W R P grows through tile cork sheath and the root tip emcrges. Bars, 100 Iml.
181
Fro. 4. Transverse sections of roots stained with safranin and fast green (A,B), PAS (C,D) or safranin (E-G). A. One-year-old ginseng root showing primary and secondary resin ducts (arrow labelled 'a' and 'b'). B. Three-year-old ginseng root showing the newly differentiated secondary resin ducts (arrow labelled 'c'). C. Ginseng root in spring showing fissures. D. Ginseng root in summer. The fissures have disappeared. E G. The structure of adventitious roots of (E) Asarum helerolropoide,~, (F) b)ilillaria ussuriensis, and ((;) Adoni,~ amurensi.~. Bars, 100 l~m.
ROOT RESPONSES TO SEASONAL CHANGES
heterotropoides increases from a minimum in early spring (April), to a peak 1 month later, at which time the plants are flowering. It then decreases rapidly and remains at a constant level from summer to winter (Fig. 7).
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In winter, the above-ground parts of the plant wither, but the root system grows slowly and winter buds enlarge. Growth of the root system accelerates in July of the following year. The colour of the root changes from white to yellow as the root ages. Roots of A. heterotropoides continue to grow for at least 10 years during which time they retain a mainly primary structure (i.e. without secondary tissues) (Fig. 4E). The content of volatile oil found in roots of A.
Fritillaria ussuriensis It takes 6 years from seed germination for plants ofFritillaria ussuriensis to mature. Seeds are shed in early August, germinate, and the radicle elongates and develops into the main root. The plumule emerges and forms a leaf during winter. The hypocotyl enlarges and forms the bulb. The fibrous root system comprises adventitious roots arising from the base of the bulb. The roots show a primary structure throughout their life (Fig. 4F). The development of a mature plant throughout a year can be divided into six stages (Fig. 8) (Table 1). Roots and buds begin to grow in March. Bulbils, 102 m m in diameter, develop from the edge of the scale leaves; roots elongate further when the leaves expand (April); roots arise from the bulbils at the same time. When flowering occurs (May), the root system grows slowly and the scale leaves become translucent and membranous. Bulbils fall and form new plantlets. A new bulb is formed in the basal plate. At this stage, the root system stops growing, the membranous scale leaves wither and the new bulb enlarges during the fruiting stage (June). In J u l y August, the root system withers, the old scale leaves are shed and the new bulb enlarges further and becomes dormant. However, in SeptemberOctober root primordia develop into a new fibrous root system, buds sprout and bulbils are differentiated on the edge of the scale leaves in the growing underground part. When the soil is frozen, plants are forced into winter dormancy (late October-early March). Adonis amurensis After seed germination and a year-long seedling stage, the radicle develops a tap root system, which includes main root and lateral roots. Adventitious roots are produced from nodes which bear sheath-like leaves on 2-year-old seedlings. These roots increase in the following year. The primary root, however, grows slowly, begins to wither and finally the tap root system changes
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FxG. 6. The external developmental morphology of the root system of Asarum heterotropoides.
into a fibrous root system. The vegetative growth stage ofA. amurensis lasts for at least 6 years. After entering the sexually reproductive phase, the development of the mature plant during the year can be divided into six stages (Fig. 9) (Table 1). Buds sprout in early spring (mid-February)
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and flower (mid-March). The root system does not grow at this time and roots are yellow- or reddish-brown. W h e n the leaves have expanded, fruits are borne (late April) and new adventitious roots arise from the rhizome. These roots are white and unbranched. Branches are developed later and the new roots change gradually from white to light yellow or brown. The older roots can also branch or their tips renew growth. The new roots turn dark yellow-brown and stop growing in a withered and d o r m a n t state in summer (early June). The root system recommences growth during an underground growing stage in a u t u m n (late August) and is similar to that of the early growth stage; d o r m a n t buds enlarge. The root system finally stops increasing (November). The older roots change from dark yellow to red or black-brown while new roots show some slight growth. The roots which are white to light yellow-
ROOT RESPONSES TO SEASONAL CHANGES March
April
May
June, July and Aug.
Sept.
185 Oct.
Fro. 8. Yearly rhythm of root system development of a mature plant of Fritillaria
ussuriensis.
brown are closest to the shoot apex and were formed in the current year. Two-year-old roots are red-brown, and are located further back. Roots older than 3 years are black-brown, and are furthest from the shoot apex. The roots retain a primary structure throughout their life (Fig. 4G). Figure 10 indicates the level of cardiac glycoside in roots of different developmental stages. (23/ Cardiac glycoside decreases from a maximum in early spring to a minimum during late spring and early summer. When plants are in summer dormancy, glycoside increases gradually from the summer minimum and remains high during the autumn. DISCUSSION
The developmental characteristics of the root system in the four species included in the present
study include one of renewal, i.e. the growing points of the root systems of mature plants, with either a tap root or a fibrous root system, usually renew. Three different patterns of root system development were encountered within a year: (i) The renewal type. This includes the partial renewal and the total renewal type. In the partial renewal type, absorbing roots wither and abscind before the winter, and dormant (WRP) primordia are produced near the base of withered absorbing roots and develop into new absorbing roots in the following spring (e.g. Panax ginseng). In the total renewal type the whole root system withers and abscinds in a given season. A new root system is produced at a suitable time in the same year (e.g. Fritillaria ussuriensis). (ii) The continuous growth type. The growing points of the root system slow their elongation in winter, but continue in the following spring (e.g.
Asarum heterotropoides ).
186
M. LIU et al. Mid.- Feb.
Mid.- March
Late April
Early Jane
Late August
November
÷ I~ New absorbent root
I | Root the some year
~ Withered root
II o,d root
| New
| Root Item
root
FIG. 9. Yearly rhythm of root system development of a mature plant of Adonis amurensis.
(iii) The intermediate type. A new set of roots is produced once; their growing points do not die but continue after the overwintering stage. However, some older absorbing roots do die, but there is also formation of new root primordia which develop into new absorbing roots, i.e. new roots do not turn-over, but the older roots do so (e.g. Adonis amurensis ). Our results indicate that, depending on the species, the growth and development of root systems of mature plants, especially the renewal behaviour of absorbing roots, have different
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adaptive patterns to seasonal change. A possible explanation of the partial renewal of the root system in Panax ginseng lies in its adaptation to the rhythm of the modern local climate. Late in the growing season, many absorbing roots begin to wither, die and abscind. At this time, WRPs are covered with their cork sheath. They will develop as new absorbing roots in the next growing season. These developmental characteristics may be advantageous to the plants, enabling them to adapt to colder winters in temperate climes. A cyto-geographic analysis o f Panax showed that P. ginseng is a polyploid species which has developed in one group of the genus as an adaptation suitable to the harsh mountain climates in Northeast China during its northbound migration. I24) Another renewal type, total renewal, is not coordinated with the modern local climate. Fritillaria ussuriensis is an early spring plant. Its growing period lasts about 4 months (April to J u l y August). The roots wither and fall when the aboveground part withers upon bearing fruits (July-August), and the plants become dormant during the summer (this period is the growing season for other species). In autumn new adventitious roots are formed, and these roots comprise
ROOT RESPONSES TO SEASONAL CHANGES a new root system which survives the winter. In temperate regions the change between warmer summer and colder winter profoundly affects the developmental rhythm of many species. Clearly, this adaptation of the root system of FritiUaria ussuriensis to seasonal change may reflect the fact that this taxon was formed during the Ice Age and retains some characteristics for adaptation to a cold climate. In the studies of the Arctic tundra by SHAVER and BILLINGS,(20) roots of Eriophorum angustifolium are annual, and hence an entirely new root system is produced each year. This developmental pattern of the root system constitutes a particular evolutionary strategy in the Arctic environment, and differs from that adopted by F. ussuriensis, even though this plant is tolerant of cold habitats. The developmental characteristics of root systems of continuous growth and intermediate types are also not co-ordinated with the local climate. The continuous growth characteristic of Asarum heterotropoides may indicate that this species evolved in a zone where the seasons were undifferentiated, but the roots still show some features that are not adapted to the present-day climate. The intermediate type shown by Adonis amurensis has obviously adapted positively to the modern climate by showing two periods of dormancy during the year. Root systems of all plants may be divided simply into either a tap root system or a fibrous root system. It is noteworthy that there are several different groups of herbaceous perennials that can be classified in terms of the development of their underground part (especially the root system) during a year. This pattern of seasonal growth which a species exhibits is established as a result of adaptation to the particular environment in which it currently grows, or as an outcome of its past ecological and evolutionary history. The perennial plants of temperate climes mostly exhibit a seasonal pattern of growth and development. Because the aerial portions of herbaceous perennials do not survive the winter, their root systems undergo extensive physiological changes during the overwintering period and regrow in the spring. The seasonal fluctuations of carbohydrate and nitrogenous components in these roots are strongly associated with their overwintering strategy. (5 8) The increase in soluble
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carbohydrates of ginseng roots during the late autumn and early winter coincides with a decline in starch. Maintenance respiration during overwintering and rapid growth during early spring probably account for a significant proportion of the carbon lost from the storage carbohydrate. Many radicular fissures appear, and the level of ginsenoside increases in this period. KIM et al. ~21 found that two groups of biologically active dammarane-saponins showed a seasonal variation and they noticed higher levels in roots in summer. LI eta/. (14) also found that ginsenoside levels in roots were significantly higher in summer than in winter and that accumulation of ginsenoside was inversely related to the level of starch. However, seasonal patterns of cardiac glycoside in roots of Adonis amurensis are different from those of ginsenoside. The glycoside decreased in the spring and early summer, and increased from mid-summer to winter. The change of volatile oil in roots of Asarum heterotropoides was only associated with flowering and did not reflect any obviously seasonal pattern. Accumulation of secondary metabolic materials can be related with primary metabolism. It is also necessary to understand thoroughly the role played by these substances since they may also be adaptive responses of the root to seasonal change. Acknowledgement--We wish to thank Dr P. W. Barlow for his helpful comments. REFERENCES
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