tree physiol 1995 yamamoto 713 9

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Summary Two-year-oldFraxinus mandshuricaRupr. var.

japonicaMaxim. seedlings were flooded to 8 cm above soil

level for 70 days. The flooding treatment altered the growth,

morphology, stem anatomy and ethylene production of theseedlings. Although flooding did not affect height growth, it

stimulated diametergrowth of the submerged stems by increas-

ing both the number and size of wood fibers produced; how-

ever, the thickness of the cell walls of the wood fibers was

reduced by flooding. In response to the flooding treatment, the

seedlings formed abundant hyperhydric tissues, originating

from the vicinity of lenticels on the surface of the flooded

stems, andadventitiousroots, which grewthroughthehyperhy-

dric tissues. Aerenchyma tissues were observed in the bark of

the adventitiousroots. The flooding treatment didnot affect dry

weight increment of leaves and stems, but it reduced the total

dry weight increment of the root system even though it pro-

moted adventitious root formation. Flooding also enhancedethylene production in the submerged portions of stems. The

potential roles of flood-induced ethylene in cambial growth

andadventitious rootformation inflooded plants arediscussed.

Keywords: adventitious roots, cambial growth, diameter

growth, dry weight increment, ethylene, height growth.

Introduction

Morphological and physiological responses of woody plants to

flooding vary (Kozlowski 1984, Kozlowski et al. 1991). In

general, angiosperms are more flood tolerant than gymno-

sperms (Kozlowski 1984). In various woody angiosperms,both hypertrophic stem growth and adventitious root forma-

tion occur in submerged portions of stems and may contribute

to flood tolerance (Kozlowski 1984, Hook 1984, Kozlowski et

al. 1991). However, hypertrophic stem growth is not always

correlated with xylem increment. Furthermore, there is little

evidence of increased cambial activity or accelerated wood

production in hypertrophied stems of flooded woody plants.

For example, short-term flooding increased stem diameter of

several coniferous seedlings largely because of an increase in

bark thickness rather than an increase in wood production

(Kozlowski et al. 1991).

Both hypertrophic stem growth and adventitious root forma-

tion have been attributed to the regulatory effects of endo-

genous hormones. Flooding stimulates ethylene production in

both herbaceous and woody plants (Kawase 1972, Tang andKozlowski 1982b, Reid and Bradford 1984, Jackson and Drew

1984, Jackson 1985, Yamamoto and Kozlowski 1987a, 1987b,

1987c, 1987d, 1987f, Yamamotoet al. 1987). Moreover, ethyl-

ene has been implicated in regulating both cambial growth

(Yamamoto and Kozlowski 1987e, 1987f, Savidge 1988) and

adventitious root formation (Riov and Yang 1989, Bollmark

and Eliasson 1990, Liu et al. 1990).

To obtain more detailed information about the relationship

between ethylene production and the morphological and ana-

tomical responses of flooded woody plants, we studied the

effects of flooding of soil on growth, morphology, stem anat-

omy and ethylene production ofFraxinus mandshuricaRupr.

var.japonicaMaxim. seedlings. A primary objective was to

assess the regulatory roles of ethylene in cambial growth and

adventitious root formation in submerged portions of stems.

We chose to studyF. mandshurica, which is native to swamp

areas along rivers in Hokkaido, Japan, because this species is

tolerant of flooding and grows vigorously even in poorly

aerated soils (Terazawa et al. 1989).

Materials and methods

Treatments

Fraxinus mandshuricaseedlings were grown in the nursery of

the Hokkaido Forest Research Institute. Seventeen-month-oldseedlings were lifted from the nursery in October 1990 and

transported to Tottori University, and each seedling was

planted in a 1/1 (v/v) mix of sand and bark compost in a 19.5

14.5 cm plastic pot. On July 2, 1991, 108 seedlings were

selected foruniformity of sizeand development.Average seed-

ling height and stem diameter at 3 cm above ground level were

29.9 5.4 cm and 8.3 2.0 mm, respectively. At the beginning

of the experiment, 12 untreated seedling were harvested. Six

of the seedlings were separated into leaves, stems and roots,

and their dry weights were determined separately after drying

at 80 C for 48 h. The other six seedlings were used for

Physiological, morphological and anatomical responses ofFraxinus

mandshurica seedlings to flooding

FUKUJU YAMAMOTO,1

TSUTOMU SAKATA1

and KAZUHIKO TERAZAWA2

1Department of Forestry Science, Faculty of Agriculture, Tottori University, Koyama, Tottori 680, Japan

2Hokkaido Forestry Research Institute, Higashiyama, Koshunai, Bibai, Hokkaido 079-01, Japan

Received March 17, 1994

Tree Physiology15, 713719

1995 Heron PublishingVictoria, Canada


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ethylene analysis as described below. The remaining 96 seed-

lings were divided into two groups: 48 untreated control

plants, and 48 flooded plants. The 70-day flooding treatment

was initiated on July 2 by raising the water level in the plastic

pots to 8 cm above the soil level. Tap water was periodically

added to keep the water level 8 cm above the soil level, but

the water was not changed. The untreated control plants were

watered daily with tap water. Changes in heights and stem

diameters of six control and six flooded seedlings were deter-

mined at Days 7, 14, 21, 28, 42, 56 and 70. Stem diameters

were measured with a microcaliper at the water level of the

flooded seedlings and at comparable stem heights on the con-

trol seedlings. To identify the amount of xylem produced

before the flooding treatment, pin-markings were made on the

same portions of stems used for diameter measurements ac-

cording to the method of Wolter (1968). At the end of the

experiment, the seedlings were harvested, separated into

leaves, stems and roots, and their dryweights determined after

drying at 80 C for 48 h.

Ethylene determination

Six control and six flooded seedlings were harvested on Days

0.5, 1, 3, 7, 14, 28, 42 and 70 for determination of the amount

of ethylene released from the stems. Ethylene release was

determined in a 1-cm stem segment taken at water level from

each flooded seedling. Stem segments were also taken from

comparable stem heights on control plants.

Ethylene was determined by a modification of the method

of Tang and Kozlowski (1982a). Each stem segment was

placed in a 10-ml vial, sealed with an isoprene rubber stopper,

and incubated in a water bath at 30 C for 5 h. Aliquots (1 ml)

of head space gas were taken and analyzed for ethylene with aHitachi 263-50 gas chromatograph equipped with a flame

ionization detector and a spiral glass column (0.35 200 cm)

packed with 60/80 mesh activated aluminum. Column, injector

and detector temperatures were 70, 80 and 100 C, respec-

tively; the carrier gas was N2, and the flow rate was 15 ml

min1. Amounts of ethylene released were determined from

standard curves obtained from known concentrations of ethyl-

enenitrogen mixtures (4.97, 24.8 and 49.7 ppm) obtained

from Seitetsu-kagaku Co. Ltd. (Tokyo, Japan). The amount of

ethylene released by stem segments (nmol gDW1) was calcu-

lated as described by Yamamoto et al. (1987).

Histological observations and measurements

Each stem sample was fixed in FAA solution (formalde-

hyde/aceticacid/ethanol/water, 5/5/60/30,v/v) for 24 h, rinsed

in water, dehydrated in ethanol, and sealed in a paraffin block.

Samples were sectioned transversely at 15 m through the

pin-marks described earlier on a sliding microtome, stained

with safranin-fast green solution, and mounted in Diatex. For

eachsection, thexylem increment and thenumber of libriform

wood fibers formed after flooding, bark thickness, and radial

diameter and cell wall thickness of the newly formed wood

fibers were studied by light microscopy.

Results

Growth and stem anatomy

TheF. mandshuricaseedlings had already formed dormant

buds before flooding was initiated, therefore, neither the con-

trol nor the flooded seedlings exhibited height growth during

the 70-day flooding treatment. However, flooding greatlystimulated diameter growth of the submerged portions of

stems(Figures 1 and 2). Increases in stem diameter at the water

level were evident after 7 days of flooding. After 70 days, the

cumulative diameter increment of the flooded seedlings was

approximately four times that of the control seedlings. The

increase in stem diameter resulted largely from both in-

creased number and size of xylem cells consisting mainly of

libriform wood fibers (Tables 1 and2, Figure 3). In the flooded

seedlings, the newly formed xylem was more than twice as

thick at the water level and more than three times as thick 3 cm

below the water level than that at comparable heights in control

seedlings. The number of wood fibers in the flooded seedlings

was more than twice that in control seedlings. The wood fibers

in the floodedseedlings were greatlyenlargedin both radial and

tangential directions; however, the thickness of the walls of the

wood fibers was reduced by flooding, with the reduction

2 YAMAMOTO, SAKATA AND TERAZAWA

Figure 1. Fraxinus mandshuricaseedling flooded for70 days showing

hypertrophic stem growth, abundant lenticels and adventitious roots

(arrows) on previouslysubmerged portionof the stem. The horizontal

bar indicates the flooding level.


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greater at 3 cm below the water level than at the water level.

The thickness of the inner bark was not affected by flooding;

however, abundant hyperhydric tissues, originating in the vi-

cinity of lenticels, formed over the surface of the flooded stems

(Figure 1).

Flooding stimulated the formation of adventitious roots,

which grew through the hyperhydric tissues around the len-

ticels (Figure 1). Adventitious roots formed after 14 days of

flooding and their numbers increased rapidly within 28 days

(Figure 4). By Day 70 after flooding, most of the adventitious

roots hadbent downward andpenetrated thesoil. Aerenchyma

tissues were also observed in thebark of theadventitious roots

(Figure 5).

Flooding reduced the rate of dry weight increment of the

root system even though abundant adventitious roots had

formed (Table 3). The reduction in total root biomass of the

flooded seedlings was not caused by root decay but occurred

as a result of the suppression of growth of normal roots.

Flooding slightly increased the biomass of leaves and stems.

Ethylene production

Flooding stimulated ethylene production in the submerged

portions of stems (Figure 6). Twelve hours after flooding was

initiated, theamount of ethylene releasedby thestem segments

at thewater level wassignificantly higherthan that released by

stem segments of the control plants (5.08 0.58 versus 3.39

0.71 nmol gDW1). Although ethylene production washigher in

flooded than in control seedlings throughout the 70-day flood-

ing treatment, ethylene production in flooded seedlings was

highest between Days 3 and 14.

Discussion

Fraxinus mandshuricaseedlings exhibited high tolerance to

soil flooding as shown by enhancedstem growth, development

of hyperhydric tissues (hypertrophied lenticels), and formation

of adventitious roots containing aerenchyma tissues.

In both woody angiosperms and coniferous species, the

effects of flooding on cambial growth are complex and vary

from inhibition to acceleration. In flooded coniferous species

such asPinus halepensis Mill. (Yamamoto et al. 1987),P. den-

sifloraSiebold & Zucc. (Yamamoto and Kozlowski 1987a)

FLOODING AND CHARACTERISTICS OFFRAXINUS MANDSHURICA 3

Figure 2. Effect of flooding on changes in stem diameter: weekly di-

ameter increment (upper), and cumulative diameter increment

(lower). Measurements were performed at the water level of flooded

seedlings and at a comparable stem height on control seedlings. Error

bars represent standard errors (n = 6). Symbols: * = significantly

different from control plants at the 5% level, ** = at the 1% level, and

*** = at the 0.1% level.

Table 1. Effect of flooding for 70 days on bark thickness, xylem increment and number of libriform wood fibers per radial file. Stem sections of

flooded seedlings were taken at the water level (WL) and 3 cm below the water level (3 cm WL). Stem sections of control seedlings were taken

at comparable stem heights. The values are means 1 SE (n= 6).

Treatment Bark thickness (mm) Xylem increment (mm) Number of wood fibers

Control 1.06 0.09 0.89 0.09 53.8 4.2

Flooded WL 1.10 0.10ns 1.91 0.21** 114.4 10.5***

3 cm WL 1.06 0.09ns 2.41 0.19*** 120.8 13.8**

Symbols: ** = significantly different from control seedlings at the 1% level, *** = at the 0.1% level, and ns = not significant.

Table 2. Effect of flooding on cell diameter and wall thickness of libriform wood fibers. The values are means 1 SE (n= 6).

Treatment Cell diameter Cell wall thickness

Tangential direction (m) Radial direction (m) Radial direction (m)

Control 27.3 1.6 36.8 1.0 4.9 0.2

Flooded WL 35.6 1.5** 38.3 1.6ns 4.0 0.1**

3 cm WL 37.9 1.3*** 43.6 1.5** 3.3 0.1***

Symbols: ** = significantly different from control seedlings at the 1% level, *** = at the 0.1% level, and ns = not significant.


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and Cryptomeria japonica (L.f.) D. Don. (Yamamoto and

Kozlowski 1987b), the increase in diameter of submerged

stems is mostly the result of increased bark thickness and

development of intercellular spaces. InThuja orientalis(L.)

Franco seedlings, flooding accelerated bark increment as well

as tracheid production in submerged stems (Yamamoto and

Kozlowski 1987c). Hypertrophic stem growth also occurs in

flooded woody angiosperms, for example,Nyssa aquaticaL.

(Penfound1934),Eucalyptus robusta Sm.(ClemensandPear-

son1977),E. camaldulensis Dehnh.,E. globulus Labill. (Tang

and Kozlowski 1984b),Acer rubrumL., Fraxinus pennsyl-

vanicaMarsh.,F. americanaL. (Hook 1984), Alnus rubra

Nutt. (Harrington 1987), and Gmelina arborea Roxb.

(Osonubi and Osundina 1987). However, there is little evi-

dence of increased cambial activity or accelerated xylem pro-

duction in hypertrophied stems of woody angiosperms. We

found that the increase in diameter of submerged stems of

F. mandshuricaseedlings was the result of an increased num-

ber and size of wood fibers rather than bark increment. Flood-

ing also greatly increased the size and number of wood fibers

in submerged portions of stems ofAlnus japonica(Thunb.)

Steud. seedlings (Yamamoto et al. 1995).

Flooding-induced adventitious root formation may be an

importantadaptation to flood tolerance in woody plants (Hook

1984). Sena Gomes and Kozlowski (1980a) found that

F. pennsylvanicaseedlings with adventitious roots had higher

water-absorbing efficiency than seedlings without adventi-


Figure 3. Effectof floodingfor 70 dayson xylem anatomy. Left = control seedling, andright = floodedseedling. The arrow shows xylem structure

at the time of initiation of flooding. Note enlarged wood fibers with thin walls in the flooded seedling. The sections were taken at the water level

of the flooded seedling and at a comparable stem height of the control seedling. The horizontal bar indicates 200 m.

Figure 4. Effect of length of flooding on number of adventitious roots

per tree. No adventitious roots formedon controlseedlings.Error bars

represent standard errors (n= 6).


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tious roots. In floodedMelaleuca quinquenervia(Cav.) S.T.

Blake seedlings, increased production of adventitious roots

was correlated with the reopening of stomata that had closed

shortly after flooding was initiated (Sena Gomes and Ko-

zlowski 1980b). Severing of flood-induced adventitious roots

from the submerged portions of stems ofPlatanus occidentalis

L. seedlings reduced height and diameter growth (Tsukahara

and Kozlowski 1985). These results indicate that adventitious

roots may increase the capacity for absorption of water and

compensate for loss of absorbing capacity in the original root

system.

We observed that flooding stimulated the formation of ad-

ventitious roots that contained aerenchymatous tissues. Grosse

and Schrder (1984, 1985) and Schrder (1989a, 1989b) re-

ported thatAlnus glutinosa (L.) Gaertn. increasedO2 supply to

the root systemby gas transport from the aerial parts of its stem


Figure 5. Transverse sections of an adven-titious root from a flooded seedling (up-

per) and a normal root from a control

seedling (lower). Note aerenchyma tissue

(arrows) in the outer bark of the adventi-

tious root. Details: P = phloem, C = cam-

bium, and X = xylem.

Figure 6. Ethylene production (nmol gDW1) by stem segments taken

at the water level of flooded seedlings and at a comparable stem height

of control seedlings. Error bars represent standard errors (n = 6).

Symbols: ** = significantly different from control plants at the 1%

level, and *** = at the 0.1% level.


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to the roots. Root aeration by gas transport has been observed

in several wetland tree species includingTaxodium distichum

(L.) L. Rich.,Betula pubescensJ.F. Ehrh.,Populus tremulaL.

(Grosse et al. 1992),A. japonicaandA. hirsuta(Spach) Rupr.

(Grosse et al. 1993). Thus, the enlarged, thin-walled wood

fibers in submerged portions of stems and hypertrophied len-

ticels may have improved the internal aeration of the floodedF. mandshuricaseedlings. We hypothesize that the flood-in-

duced adventitious roots probably function both as water-ab-

sorbing organsandas ventilatorsof theanaerobicrhizosphere.

Flooding substantially alters endogenous hormonal rela-

tions in plants (Reid and Bradford 1984). Several changes in

the morphology and anatomy of flooded woody plants have

been attributed to the effects of flood-induced ethylene pro-

duction, including reduced growth (Kozlowski 1984), leaf

epinasty, senescence and abscission (Sena Gomes and Ko-

zlowski 1986), developmentof hypertrophied lenticels (Ange-

les et al. 1986),production of aerenchyma tissue (Hook 1984),

hypertrophic stem growth (Newsome et al. 1982, Tang and

Kozlowski 1982a, 1982b, 1982c, 1984a, Yamamoto et al.

1987, Yamamoto and Kozlowski 1987a, 1987b, 1987c,

1987d), and formation of adventitious roots (Tang and Ko-

zlowski 1982b, Yamamoto and Kozlowski 1987b, 1987d).

Ethylene may also have an important regulatory role in certain

aspects of xylogenesis (Brown and Leopold 1973, Robitaille

and Leopold 1974, Savidge and Wareing 1984, Savidge 1988).

In our seedlings, hypertrophic stem growth and the formation

of abundant libriform wood fibers were associated with high

ethylene production by submerged portions of the stem. How-

ever, many plant responses attributed to ethylene involve inter-

actions with other plant hormones (Wample and Reid 1979,

Jaffe 1980, Sisler and Yang 1984).

Phillips (1964a, 1964b) found that, over a 14-day period of

waterlogging, the concentration of auxins in sunflower shoots

increased threefold. Wample and Reid (1979) found that soil

inundation inhibited basipetal transport of 14C-IAA (indo-

leacetic acid) and slowed its breakdown. According to Burg

and Burg (1967) and Beyer and Morgan (1969), elevated

ethylene concentrations in shoots of flooded plants slow the

movement of auxins from shoot to roots. Hall et al. (1977)

noted that the increase in IAA concentrations in leaves of

floodedVicia fabaL. occurred after the rise in ethylene evolu-

tion. We have observed that blocking basipetal auxin transport

with NPA (1-N-naphthylphthalamic acid) suppressed cambial

growth of floodedF. mandshuricaandA. japonicaseedlings

(unpublished data), suggesting that both ethylene and auxins

maybe essential in theactivation of cambial growthin flooded

F. mandshuricaseedlings.

Several investigations have indicated that ethylene directly

stimulates adventitious rooting in cuttings of plants (Riov and

Yang 1989, Bollmark and Eliasson 1990, Liu et al. 1990).

Graham and Linderman (1981) noted that low concentrations

of ethrel applied to roots of Douglas-fir seedlings stimulated

lateral root formation. Liu et al. (1990) suggested that the

contradictory reports of ethylene on rooting are probably be-

cause lowconcentrations of ethylene promote rooting whereas

high concentrations inhibit rooting. They concluded that an

increase in ethylene in thehypocotylsofHelianthus annuus L.

seedlings initiates the rooting process in cuttings and perhaps

in flooded plants. We have found that application of AOA

(aminooxy acetic acid), an inhibitor of ACC (1-aminocyclo-

propane-1-carboxylic acid, an ethylene precursor) synthesis,

to anaerobic roots of water-cultured F. mandshurica seedlings

inhibited adventitious root formation (unpublished data), sug-gesting that ethylenehasa primary role in adventitious rooting.

However, Reid et al. (1991) concluded that a basipetal flood-

induced increase in ethylene causes IAA accumulation in the

rooting zone and that this IAA is the factor that triggers root

initiation. Yamamoto and Kozlowski (1987d) reported that

blocking basipetal auxin transport with NPA reduced forma-

tion of adventitious roots in floodedAcer negundoL. seedlings

despite the presence of large amounts of ethylene in the sub-

merged stems, indicating that, in this species, auxins trans-

ported from the shoots have the major role in regulating

formation of adventitious roots.

Acknowledgments

The authors aresincerely grateful to Dr.T.T. Kozlowski forhis helpful

suggestions during this study.

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