Journal of Integrative Plant Biology 2008

Fragment Propagation and Colonization Ability Enhancedand Varied at Node Level after Escaping from Apical

Dominance in Submerged Macrophytes

Jinhui Jiang1,2, Shuqing An1,2,3∗, Changfang Zhou1,2, Baohua Guan1,2, Zhiyi Sun2,

Ying Cai2 and Fude Liu3

(1State Key Laboratory of Pollution Control and Resource Uses, Nanjing University, Nanjing 210093, China;2Institute of Wetland Ecology, School of Life Sciences, Nanjing University, Nanjing 210093, China;

3Laboratory of Forest Ecology and Global Changes, School of Life Sciences, Nanjing University, Nanjing 210093, China)

Abstract

Aquatic plants develop strong fragment propagation and colonization ability to endure the natural disturbances. However,detailed research of ability to endure the natural disturbances has been lacking to date. Therefore, reproduction (shoot) andcolonization (root) of shoot fragments of Potamogeton crispus L. with or without apices were investigated for the effect ofapical dominance, and the growth of decapitated shoot fragments at three lengths (2, 4, 6 cm) was compared. Meanwhile,fragment propagation at levels of bud position was studied for bud position effect after escaping from apical dominance.The results showed significant increases occurred in the outgrowth of lateral branches on fragments decapitated comparedwith the fragments with apices, implying that apical dominance exists. Different lengths of fragments showed little differencein biomass allocations, but significant differences were noted in their propagation. Meanwhile, the effect of bud positionwas verified, due to the significant difference of average reproduction per node among the three length groups. Thus, thepresent study has made progress in the current understanding of aquatic plant dispersion among natural systems andcontributes to improve methods of in vitro propagation for re-implantation purposes.

Key words: apical dominance; bud position effect; disturbed environment; fragment propagation; Potamogeton crispus.

Jiang J, An S, Zhou C, Guan B, Sun Z, Cai Y, Liu F (2008). Fragment propagation and colonization ability enhanced and varied at node level afterescaping from apical dominance in submerged macrophytes. J. Integr. Plant Biol. doi: 10.1111/j.1744-7909.2008.00732.x

Available online at www.jipb.net

Natural physical and biological disturbances, such as currentvelocity, floods, and fish grazing play an important role in vege-tation structures and distribution in aquatic ecosystems (Nilsson1987; Tremolieres et al. 1994; Bornette and Amoros 1996).Correspondingly, aquatic plants develop various strategies toendure these disturbances and survive. In these strategies,enhanced means of dispersal and ability to propagate playan important part (Santamarıa 2002). It is widely known thatmost aquatic plants exhibit asexual reproduction by forming

Received 14 May 2007 Accepted 13 Mar. 2008

Supported by the Hi-Tech Research and Development (863) Program

of China (2003AA06011000-04 and 2002AA601012-06).∗Author for correspondence.

Tel (Fax): +86 25 8359 4560;

E-mail: <anshq@nju.edu.cn>.

C© 2008 Institute of Botany, the Chinese Academy of Sciences

doi: 10.1111/j.1744-7909.2008.00732.x

specialized propagules, like stolons, rhizomes and turions, orunspecialized fragments (Van et al. 1978; Titus and Hoover1991; Barrat-Segretain 1996). Some early reports found thatthe scouring caused by flooding favored regeneration throughunspecialized fragments in aquatic plants and these fragmentscontributed to species maintenance (Combroux and Bornette2004). Then, if an unpredictable disturbance like flood orgrazing occurs, these plants, particularly the fragile submergedmacrophytes, may be fragmented and the fragments may bethen washed away by running water and dispersed to otherhabitats (Johansson and Nilsson 1993; Barrat-Segretain et al.1998). There they develop root systems and establish rapidly insediments (colonization) (Barrat-Segretain and Bornette 2000).In such events, different types (with or without apices) anddifferent lengths of fragments (e.g. shoot fragments) would cre-ate, survive and colonize a new habitat (Barrat-Segretain et al.1998). Therefore, all of these fragments formed were believedto contribute to distant dispersal and colonization according tothe early findings (Kimbel 1982; Sabol 1987; Campbell 2003).

2 Journal of Integrative Plant Biology 2008

Some reports believed that plant recovery could occur once thefragments were recruited (Hemminga and Duarte 2000).

Wu et al. (2007) found that fragments of Myriophyllum spi-catum with apices sank more rapidly than the ones withoutapices. It can then be deduced that fragments without apiceshave longer dispersal distances. It was also found that mid-stem fragments had stronger capability of regenerating lateralshoots than fragments with apices (Wu et al. 2007). Thismay be caused by apical dominance, which has been widelystudied in terrestrial plants (Cline 1991; Irwin and Aarssen 1996;Salemaa and Sievanen 2002). Most of these studies confirmedenhanced growth of lateral branches after escaping from apicaldominance by decapitation (Cline 1991, 1994, 1996; Bangerth1994). Although apical dominance was first reported to be foundin an aquatic species a decade ago (Terrados et al. 1997), littlenotice has since been taken in the studies that followed.

Early reports found that longer fragments sank slower, whichwould ensure longer dispersal distances and then affect theplant dispersal patterns (Wu et al. 2007). It was also foundthat longer fragments had stronger reproductive capability (Wuet al. 2007). This may be a result of more nodes (resting lateralbuds) on longer fragments and/or different reproduction abilityamong nodes from different positions. Some experts reportedthat buds at different positions on the same single shoot haddifferent re-growth abilities after decapitation (De Vries andDubois 1992). However, no consistent conclusion has beenmade. Bressan et al. (1982) concluded that the buds frommedial sections developed more rapidly than those of either theupper or basal positions, whereas Cline (1996) believed thatonly the highest lateral buds grew out following decapitation.De Vries and Dubois (1992) suggested that the effect of budposition accounted for approximately 30% of the differencesobserved in flower yield. Therefore, it was very interestingto investigate the different re-growth ability of fragments atdifferent lengths and of nodes from different positions after apexremoval.

In order to investigate the effect of apex removal, fragmentlength and bud position effect on fragment re-growth (includingreproduction and colonization) in submerged plants, Potamoge-ton crispus was chosen as a study model. This species is oftenused as a pioneer species in lake re-vegetation projects for itswide range of climatic habitats and effective nutrient reductionability (Ren et al. 1997; Zhou et al. 2000; Lauridsen et al.2003). Just like other aquatic macrophytes, it plays a great rolein many aquatic ecosystems (Vermaat et al. 2000; Kufel andKufel 2002). In the present study, aseptic environments andshoot fragments were used for excluding other biotic influences(Xie et al. 2005), and the following hypotheses were to betested: (i) fragment reproduction and colonization ability wouldbe greatly enhanced after apex removal; (ii) longer fragmentshad stronger reproduction and colonization ability; and (iii)nodes from different positions would have different re-growthcapabilities.

Results

Growth variations between shoot fragmentswith and without apices

There was great difference between the growth of shoot frag-ments with apices and those without apices (Table 1). Dryweight of shoot fragments without apices was significantlygreater than the ones with apices (P < 0.05). However, thetreatment of decapitation did not show a great effect on biomassallocation to below-ground and above-ground organs, as theroot ratios were not significantly different between fragmentswith and without apices (P > 0.05). Fragments without apiceshad a significantly greater shoot number compared with theones with apices (P < 0.05), implying that decapitation greatlyenhanced the reproduction ability of fragments. Root numberand total root length were significantly greater for the fragmentswithout apices (P < 0.05), which implied the enhanced coloniza-tion ability after decapitation.

Growth variation of decapitated shoot fragmentsat different length levels

Dry weight significantly increased with the increase of thefragment length among all treatments at the fragment level(Table 2). However, length treatment had little effect on biomassallocation (P > 0.05), including root ratio, stem ratio and leafratio. Shoot number showed significance at the fragment levelamong three length treatments (P < 0.05), and it was greatestfor fragments of 6 cm in length compared with the other twotreatments. Root number and total root length showed slightvariations among all length treatments (P > 0.05).

Average growth per node of decapitated shoot fragments

Average fresh weight, root number and shoot number per nodefor fragments at different lengths at different growth times werecalculated and statistically analyzed (Figure 1). At the 6th and12th d of growth, all of these traits showed no significanceamong all length treatments (P > 0.05). However, at the 9th d ofgrowth, the root number and shoot number varied significantly(P < 0.05). At the 15th or 18th d of growth, there was stillno significance for fresh weight per node among treatments(P > 0.05), whereas it was significant for root number and shootnumber (P < 0.05). With the increase of fragment length, therewas a great decrease in root or shoot number during this growthperiod.

The significant differences for average shoot number and rootnumber per node among length treatments at the final harvestwere supplements to the results above during the growingperiod (P < 0.01) (Figure 2). The average shoot number androot number per node both greatly decreased with increases

Apical Dominance Altered Fragment Re-growth 3

Table 1. Individual growth variations between shoot fragments with and without apices

Treatments Dry weight (mg) Root ratio (%) Shoot number (ind) Root number (ind) Total root length (cm)

Without apex 194.100 ± 15.200a 3.380 ± 0.760 14.000 ± 1.060 42.000 ± 3.600 65.970 ± 4.750

With apex 71.700 ± 5.300 2.720 ± 0.370 8.330 ± 0.760 25.970 ± 1.380 37.270 ± 3.770

P values 0.000 0.485 0.003 0.003 0.001

aMean ± SE; n = 5 for both treatments; root ratio calculated as root dry weight divided by dry weight of the whole individual. Independent-Samples T

test was used at the 0.05 significance level.

Table 2. Individual growth variations between shoot fragments with and without apice

Fragment lengths TestsDependent variables

2 cm 4 cm 6 cm df1 df2 P

Dry weight (g) 0.190 ± 0.020b 0.250 ± 0.030b 0.320 ± 0.020a 2 12 0.006

Root ratio (%) 3.380 ± 0.760 3.400 ± 0.070 3.610 ± 0.340 2 6 0.935

Stem ratio (%) 40.310 ± 1.330 43.390 ± 0.400 44.050 ± 2.050 2 6 0.223

Leaf ratio (%) 56.310 ± 0.580 53.210 ± 0.430 52.340 ± 1.700 2 6 0.085

Shoot number (ind) 14.000 ± 1.060b 17.330 ± 2.510b 22.750 ± 0.750a 2 12 0.036†

Root number (ind) 42.000 ± 3.600 51.200 ± 4.840 56.400 ± 5.390 2 12 0.129

Total root length (cm) 65.970 ± 4.750 76.100 ± 9.130 88.700 ± 7.460 2 12 0.132

Values are mean ± SE; df1, df2 represent degrees of freedom between groups and within groups, respectively. Root/stem/leaf ratio was calculated

as root dry weight divided by dry weight of the whole individual. The different upper case letters indicate significant differences among treatments by

Duncan’s test at the 0.05 significance level. † Shoot number was tested by Kruskal-Wallis H test at the 0.05 significant level as the homogeneity of

variances was not assumed by Levene’s test.

in the original fragment length. Average dry weight per nodealso showed significance and was greatest at 2 cm in length(P < 0.01). Length treatment showed a great effect on averagetotal root length per node (P < 0.01).

Discussion

Apical dominance regulated fragment reproductionand colonization ability

According to our results, fragment reproduction ability (shootnumber) was greatly enhanced after the apex removal, just likethe early reports in other terrestrial and aquatic plants (Terradoset al. 1997; Salemaa and Sievanen 2002). Therefore, we haveconvincing evidence that apical dominance does exist in P.crispus. Sadras and Fitt (1997) concluded that a large variabilityin the degree of apical dominance among cotton genotypesexisted that could influence resistance to herbivory. Apical dom-inance may also be one of the strategies used for adapting tounfavorable environments for this species, like fish herbivory ormechanical damage. The following enhanced outgrowth of lat-eral buds after decapitation increases the possibility of survivingat the original habitat. Moreover, the enhanced development ofroot systems favors the re-establishment of the plants. However,the results showed that the total biomass was also greatlyincreased after escaping from the apical dominance, which wasquite different from the early results (Terrados et al. 1997).

Fragments without apices had longer dispersal distances andit would help the species to explore new suitable habitats (Wuet al. 2007). Stronger capability of fragment re-growth after apexremoval would greatly promote the possibilities of colonization,and then it greatly affected the distribution of plants in naturalaquatic ecosystems. Furthermore, from the early reports, it isgenerally agreed that polar auxin transport plays a central role inthis phenomenon (Cline 1991, 1994), and other phyto-hormonesmay take part (Li et al. 1995; Wang et al. 2006). Therefore, afurther study is needed to investigate the active hormones forapical dominance in P. crispus.

Fragment re-growth of different lengths after apex removal

Different lengths of fragments had little variations on biomassallocation in our experiment. It may be because the sameresources were available for all of these fragments, as biomassallocation is very much related to the environmental resources(Xie et al. 2005). However, like other reports, longer fragmentshad stronger reproduction abilities (Wu et al. 2007). Earlyreports have found that fragment length had an effect on itsdispersal pattern and longer fragments had longer dispersaldistances (Santamarıa 2002; Wu et al. 2007). Therefore, thestronger ability for reproduction of longer fragments wouldfavor the wider distribution and better survival of plants atnew habitats. As we all know, P. crispus generates shootsfrom the nodes on stems. Therefore, more nodes (restingbuds) contained in longer fragments may ensure a stronger

4 Journal of Integrative Plant Biology 2008

Figure 1. Average fresh weight/root number/shoot number per node at

each measuring time.

Data at 6, 9, 12, 15 and 18 d of growth were compared. Different letters

a, b and c, above the columns at each measuring time indicate the

significant variations among the treatments. Kruskal-Wallis H test was

used as multiple comparisons for means of average shoot number per

node among all treatments at first measuring time, while the others were

carried out by Duncan’s test. The level of significance was 0.05.

reproduction ability. Moreover, such ability may be influencedby the node position effect, which has been discussed above(De Vries and Dubois 1992). In our experiment, no significantdifference in root parameters was found (root number and totalroot length) among different lengths of fragments, which impliedthat the colonization ability was not greatly varied by lengthtreatments. We may suppose that this was caused by differentre-growth ability of nodes from different positions on fragments.

Bud position effect affected the nodal propagationand colonization capability

Average nodal re-growth ability of fragments at different lengths,which represents the growth of nodes from different positions,was quite different after apex removal (Figures 1,2). Thisdifference may prove the existence of the bud position effectin this species. Some researchers have made a conclusionthat the buds from the upper side developed more rapidly thanthe basal side (Zieslin et al. 1976; Marcelis-van Acker 1994),and this was quite in accordance with our experiment. Theaverage nodal re-growth ability of fragments at 2 cm, whichrepresented the node from the upper section, had the greatestshoot number, root number and total root length at the finalharvest compared with the ones at 4 cm and 6 cm (Figure 2).However, such a significant difference was not shown until the15th d of growth (Figure 1), as it needed time for activationas reported elsewhere (Sadras and Fitt 1997). The differenceshown at 9 d growth might be caused by random outgrowthas there was no significant difference at the next measuringtime. Early reports have found that the shoots yield increasedbasipetally (De Vries and Dubois 1992). However, this was notthe same as the results in our experiment because average dryweight per node became greater with decreases in fragmentlength (Figure 2).

The existence of a bud position effect may imply an effectivestrategy for aquatic plants adapting to natural disturbances. Asthe upper section of the submerged plants would be easier tobe detached and washed away by running water, the strongerre-growth ability of nodes in upper sections may benefit thesurvival and colonization of the species at new habitats. On theother hand, stronger reproduction ability of nodes in the uppersections may favor the formation of canopies in this species, andthen benefit the light acquisition and population growth (Nicholsand Shaw 1986).

Perspectives of application for in vitro techniquesand ecosystem restoration

In most vegetation restoration work, transplantation of propag-ules or seedlings collected from donor ecosystems is commonlyused. This would evidently affect the donor ecosystems and riskbringing nuisance species into target ecosystems (Confer andNiering 1992; Brown and Bedford 1997). Hence, a new plantpropagation method has been developed to get large amountsof healthy plant materials for in vitro culture (Zhou et al. 2006).The method was mainly based on the fragment reproduction ofthese species (Barrat-Segretain et al. 1998; Zhou et al. 2006).According to the findings of apical dominance and bud positioneffect in the present study, an improved method of in vitro culturecan be suggested. In this method, the upper section of the stemis selected and the apex of the shoot fragment is removed.Therefore, we can take full advantage of the great re-growth

Apical Dominance Altered Fragment Re-growth 5

a

a

a

a

bb

b

b

bb

b

b

0

4

8

12

16

20

Mea

n ±

SE

(m

g·in

d–1

·cm

–1)

2 cm 4 cm 6 cm

Dry weight Shoot number Root number Total root length

Figure 2. Variations of the average growth per node at final harvest.

All of the parameters were at node level, which were calculated as data of fragments divided by node number contained. Dry weight was divided

by 10 for the readability of the figure. Different letters, a and b, above the columns of each parameter indicate the significant difference among the

treatments. Kruskal-Wallis H test was used as multiple comparisons for means of average shoot number per node among all treatments, while the

others were carried out by Duncan’s test. The level of significance was 0.05.

ability of lateral buds and greatly promote the effectiveness of avast scale of plant propagation. Moreover, based on the findingof apical dominance, we can manually clip the apex of plantsto speed up the process of establishment after colonization inre-vegetation projects. All of these findings would be beneficialto the success of eutrophication restoration programs.

Materials and Methods

Plant materials

The original plant materials of Potamogeton crispus L. werecollected from Taihu Lake (30◦5′–32◦8′N, 119◦8′–121◦6′E) inMarch, 2003. Turions were selected, then washed and incu-bated in tap water for several hours to remove dust and somebacteria on the surface. All turions were then disinfected with thecommon practice of tissue culture process (Bouman et al. 1995;Martin et al. 2003; Rout et al. 2006). Here 0.1% of mercuric chlo-ride was used for several minutes in the disinfection process,followed by the rinsing procedure in sterile distilled water fivetimes. Then all of the disinfected materials were transferredto autoclaved solid media based on Murashige and Skoog-based media (Murashige and Skoog 1962) plus 3% sucrose(MS). Sterile distilled water was used to cover the materials forprotecting them from drought over the solid media. After 15 dof incubation, aseptic seedlings were obtained. Then healthyones were selected and transferred into the autoclaved liquid

media which was also based on MS for clonal propagation.Enough aseptic seedlings were collected after culture for morethan six generations in a year. Shoots similar in size to thesame generation without roots were used for experiments from28 June to 25 July 2004. All of the procedures were undertakenin a tissue culture room and kept aseptic. A 12-h light period with30 μEm−2s−1 fluorescent lights were used in the tissue cultureroom and the temperature was kept at 25 ± 1 ◦C.

Experimental designs

Two experiments were undertaken to examine the apicaldominance (recorded as experiment 1), fragment growth andbud position effect (recorded as experiment 2) simultaneously(Table 3). In experiment 1, shoot fragments of 2 cm in length withapices were tested for the apical dominance effect contrasting tothe growth of 2 cm fragments without apices. All shoot fragmentswere cultured in 150-mL flasks with 80 mL autoclaved MS liquidmedium in the tissue culture room mentioned above. Five flasks(five replicates) were used for both treatments. Each flaskcontained three fragments. Therefore, 15 fragments altogetherwere used for both treatments. All of the media were renewedevery 3 d. In experiment 2, the growth of shoot fragmentsbeheaded at three length levels and the average growth pernode was compared. The fragments were at 2 cm, 4 cm and6 cm in length, which contained 4, 7 and 11 nodes, respectively.Three at 2 cm or 4 cm in length were taken as one group culturedin one flask, and two for 6 cm. Five replicates were also used for

6 Journal of Integrative Plant Biology 2008

Table 3. Experiment set-up

Apex treatment Fragment length (cm) Node contained (ind) Replicates Node positiona

Apical dominance experiment (experiment 1)

With apex 2 4 5

Without apex 2 4 5

Fragment growth and bud position effect experiment (experiment 2)

Without apex 2 4 5 Upper

Without apex 4 7 5 Middle

Without apex 6 11 5 Lower

aAverage growth per node in fragment of 2 cm represents the growth of nodes from relative upper sections in the shoot compared with the fragment

of 4 cm or 6 cm, for it has more percentage of upper-side nodes. Similarly, the average growth per node in fragments of 4 cm and 6 cm represent the

growth of the node from the relative middle and lower sections, respectively. Two fragments of 6 cm were taken as one group because of the limited

culture spaces.

each group; therefore, 15 fragments in total for both 2 cm and4 cm treatments, and 10 fragments for 6 cm treatments weretested. All of these shoots were also cultured in 150-mL flaskswith 80 mL autoclaved MS liquid medium, and the media wererenewed every 3 d until harvest. Shoots of 2 cm in length andwithout apices were shared in both experiments.

Plant harvest and data collection

For experiment 1, all individuals were harvested after 27 dof growth, then carefully washed in running tap water andmeasured. Shoot number and root number were counted. Thelength of each root was measured, and thus the total root lengthof each individual was calculated. Finally, three individuals ofboth treatments were randomly chosen from different flasks,and each was divided into roots, leaves and stems. Each partwas weighed freshly, and then oven dried at 60 ◦C with theremaining individuals. Dry weights were collected.

In experiment 2, shoot numbers and root numbers of eachindividual were counted every 3 d when the media was renewedexcept for the first time. Meanwhile, the fresh weight of eachgroup was obtained by weight differences of flasks with mediabefore and after transplantation after removing all of the surfacesolution of plants. After 18 d of growth, the media were stillrenewed without collecting any data until final harvest after 27 dof growth. Like experiment 1, all individuals were harvested andmeasured in the same way with the same parameters.

Dry (or fresh) weight, root ratio, stem ratio and leaf ratiowere used as the traits of growth in biomass accumulation andallocation. Shoot number was used as the trait of propagation.Root number and total root length were used as the traits ofcolonization ability.

Data analysis

Means of individual growth parameters, including dry weight,shoot number, root number and total root length in each

replicate for all treatments were calculated for later statisticalanalyses in SPSS 13.0, together with root ratio, stem ratio andleaf ratio. Normal distribution was confirmed by Kolmogorov-Smirnov Test. Levene’s test was carried out to examine thehomogeneity of variances. In experiment 1, all of the growthparameters were compared by independent-samples T testbetween the two treatments. In experiment 2, one-way ANOVA

was used to compare the variations among treatments. Whenthe requirement of homogeneity of variances was met, multiplecomparisons of the means of fresh weight/shoot number/rootnumber per node at each measuring time during growth werecarried out using Duncan’s test. However, when it was not, forexample, average shoot number per node at first measuringtime, Kruskal-Wallis H test (non-parameter test) was used asmultiple comparisons. Data of the final harvest at fragmentaland nodal levels were analyzed in the same way. All of the testswere at 0.05 significant levels.

Acknowledgements

The authors thank Wenwen Wang for assistance with somelaboratory work, and also express great thanks to Dr Li Zhangfor valuable suggestions for this paper.

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(Handling editor: Jianxin Sun)