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Nodulation Status andNitrogenase Activity of SomeLegume Tree Species inBangladeshUma K. Aryal a , M. K. Hossain b , Md. Amin U.Mridha c & Hui-Lian Xu aa International Nature Farming Research Center ,5632 Hata, Nagano, 390-1401, Japanb Institute of Forestry and Environmental Sciences ,University of Chittagong , Bangladeshc Department of Botany , University of Chittagong ,BangladeshPublished online: 20 Oct 2008.

To cite this article: Uma K. Aryal , M. K. Hossain , Md. Amin U. Mridha & Hui-Lian Xu(2001) Nodulation Status and Nitrogenase Activity of Some Legume Tree Species inBangladesh, Journal of Crop Production, 3:1, 325-335, DOI: 10.1300/J144v03n01_27

To link to this article: http://dx.doi.org/10.1300/J144v03n01_27

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Nodulation Status and Nitrogenase Activityof Some Legume Tree Species

in Bangladesh

Uma K. AryalM. K. Hossain

Md. Amin U. MridhaHui-lian Xu

SUMMARY. A study was conducted to observe the nodulation statusand measure nitrogenase activity of some important legume tree speciesin nursery. Of the thirteen species surveyed eight belong to Mimoceae,two Papilionaceae and three Caesalpiniaceae. All the species in Mimo-ceae and Papilionaceae were found nodulated whereas all the membersof Caesalpiniaceae were non-nodulated. Among nodulated seedlings,highest number of nodules per seedling was recorded in Leucaenaleucocephala (82) followed by Acacia auriculiformis (55), Acaciamangium (52), Albizia lebbeck (46), A. procera (41), Dalbergia sissoo(32) and Acacia catechu (29). Nitrogenase activity was highest in L.leucocephla (4913.59 nmole C2H4 h

−1) followed by Albizia procera

Uma K. Aryal is Visiting Microbiologist, International Nature Farming ResearchCenter, 5632 Hata, Nagano 390-1401, Japan.

M. K. Hossain is Associate Professor of the Institute of Forestry and Environmen-tal Sciences, University of Chittagong, Bangladesh.

Md. Amin U. Mridha is Professor, Department of Botany, University of Chitta-gong, Bangladesh.

Hui-lian Xu is Senior Crop Scientist, International Nature Farming ResearchCenter, Nagano 390-1401, Japan.

Address correspondence to: Uma K. Aryal at the above address.

[Haworth co-indexing entry note]: ‘‘Nodulation Status and Nitrogenase Activity of Some Legume TreeSpecies in Bangladesh.’’ Aryal, Uma K. et al. Co-published simultaneously in Journal of Crop Production(Food Products Press, an imprint of The Haworth Press, Inc.) Vol. 3, No. 1 (#5), 2000, pp. 325-335; and:Nature Farming and Microbial Applications (ed: Hui-lian Xu, James F. Parr, and Hiroshi Umemura) FoodProducts Press, an imprint of The Haworth Press, Inc., 2000, pp. 325-335. Single or multiple copies of thisarticle are available for a fee from The Haworth Document Delivery Service [1-800-342-9678, 9:00 a.m. -5:00 p.m. (EST). E-mail address: getinfo@haworthpressinc.com].

E 2000 by The Haworth Press, Inc. All rights reserved. 325

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NATURE FARMING AND MICROBIAL APPLICATIONS326

(2080 nmole C2H4 h−1). Seedling height, nodule fresh weight, root

fresh weight and nitrogenase activity (per nodule per h, per gram nod-ule fresh weight per h, per gram root fresh weight per h and per gramroot dry weight per h) were also highest in L. leucocephala. [Articlecopies available for a fee from The Haworth Document Delivery Service:1-800-342-9678. E-mail address: getinfo@haworthpressinc.com <Website:http://www.HaworthPress.com>]

KEYWORDS. Leguminous tree, nitrogenase activity, nitrogen fixa-tion, nodulation, Rhizobium, soil degradation

INTRODUCTION

Leguminosae is the third largest family of flowering plants with approxi-mately 750 genera and 20,000 species distributed worldwide (Dixon andWheeler, 1986). At present more than 640 tree species are known as nitrogen-fixing legumes (Halliday and Nakao, 1982). The ability of many tree speciesto form nodules and fix atmospheric nitrogen symbiotically in response toinfection by Rhizobium imparts considerable ecological and agronomic im-portance to the family (Mahmood, 1994). Nitrogen-fixing tree species (NFTS)are an ideal class of trees for afforestating degraded sites (Mac Dickens,1994) because they are able to establish and thrive in nitrogen deficient soils.In addition to their nitrogen-fixing capacity, NFTS grow quickly and toleratea variety of adverse soil conditions. It is widely believed that 75% of nitrogenis contributed by the root nodules of leguminous plants (Lawrie, 1981). Theeconomic utilization of NFTS is ranked with grasses in their importance(Allen and Allen, 1981; Mahmood, 1994) and the introduction of legumesinto forest ecosystems holds some promise for maintaining soil nitrogenwithout the use of inorganic nitrogenous fertilizer (Mishra and Prasad, 1980;Prichett, 1979). They may be useful for revitalization of impoverished soilsby incorporation of organic matter with wide carbon to nitrogen ratios and fortransfer of minerals from deep layers to the surface layers of the soil (Felkerand Bandurski, 1979).To increase the efficacy of biological nitrogen fixation (BNF), it is needed

to study the nodulation status and nitrogen-fixing ability of the existinglegume flora in different parts of the world (Mahmood, 1994). The globalstudy on nodulation compiled by Allen and Allen (1981) show that at thespecies level only 15% of the legumes have been examined and of them 30%of the species in Caesalpiniaceae, 90% in Mimoceae and 98% in Papiliona-ceae were found to be nodulated. Although tree legumes are used for a widerange of purposes and even planted extensively in the field, the nodulation

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Part II: Microbial Applications 327

potential of many tree legumes has not been studied Legumes have formed alarge part of the tree flora of Bangladesh and planted extensively for multi-purpose uses. Information about tree legumes in Bangladesh were scatteredin the literature; but now 68 tree species of Leguminosae in 34 genera havebeen listed consulting different literature (Khatun, 1987). However, the gapof knowledge about the nodulation potential and nitrogen-fixing ability oflegume tree species occurring in Bangladesh is immense and extensive studyis yet to be started. Therefore, the purpose of this study was to assess thenodulation potential and nitrogen-fixing ability of some promising legumetree species used extensively for afforestation programs in Bangladesh.

MATERIALS AND METHODS

Nodule Morphology

Seedlings were collected from the nursery of the Institute of Forestry andEnvironmental Sciences, Chittagong University (IFESCU) and BangladeshForest Research Institute (BFRI), Chittagong. Seedlings were randomly se-lected with the intact root systems, removed from the polyethylene bags, andwashed in running water to remove soil particles from the roots. Then amorphological study of nodules was conducted on five randomly-selectedseedlings of each species. Special care was taken to distinguish root nodulesfrom malformations such as those caused by nematodes, insects or otherpathogenic organisms. The presence or absence of nodules and degree ofnodulation on the root systems were recorded. The color, size, shape, struc-ture and distribution of the nodules were also noted. The degree of nodulationwas classified as sparse (1-30 nodules/seedling), moderate (31-50 nodules/seedling) and abundant (more than 50 nodules/seedling).

Measurement of Nitrogen Fixing Ability

Nitrogenase activity of the nodules of seven tree species, i.e., Acaciaauriculiformis, Acacia mangium, Dalbergia sissoo, Acacia catechu, Leucae-na leucocephala, Albizia procera and Albizia lebbeck was determined byassaying the reduction of acetylene as described by Hardy et al. (1968).Seedlings were grown in the nursery of the Institute of Forestry and Environ-mental Sciences, Chittagong University. Soil samples were collected fromthe bottom of the hills of the Chittagong University Campus at differentlocations, well-sieved (< 3 mm) and mixed with cow manure at a ratio of 3:1.These hills consist of moderate to strongly acidic soils of loam to sandy clayloam in texture (Osman et al., 1992) with an average pH of 5.5 (Badruddin et

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NATURE FARMING AND MICROBIAL APPLICATIONS328

al., 1989). Seeds were obtained from BFRI. Five seedlings of each species(six-month old) were randomly selected and removed from the culture bagsafter measuring plant height. Seedlings were washed in tap water and then indistilled water several times to remove soil particles. The root nodules werecounted with their fresh weight recorded, kept in Erlenmeyer flask with 10 mlof acetylene (C2H2) added and incubated for one hour. The ethylene formedby the reduction of acetylene was measured by removing 1 ml of the gasmixture from the flasks and analyzed by gas chromatography. The ethylenewas quantified from the peak height after reference to a standard ethylenegas. Fresh weight and dry weight of roots were also recorded (oven-dried at80_C for 48 hours). The nitrogenase activity was expressed in terms of nmoleC2H4 per plant per h, per nodule per h, per gram root fresh weight per h andper gram root dry weight per h.Seedlings of Cassia fistula, Cassia siamea and Delonix regia were also

raised in the nursery with the soil inoculated with Rhizobium broth at the rateof 10 ml per pot to study nodulation. Rhizobium strains were isolated fromthe nodules of A. procera, A. lebbeck, L. leucocephala, A. mangium, and A.auriculiformis in Yeast Extract Mannitol Agar (YEMA) media as describedby Vincent (1970). Then, these Rhizobium isolates were mixed together inYEM broth to produce inoculum and inoculated into the soil before seedswere sown. Fifteen-day old seedlings were again inoculated with the sameRhizobium broth at a rate of 10 ml per seedling. Seedlings were examined 45,60 and 90 days after inoculation, but no nodulation was observed.

RESULTS

The nodulation status, color, shape, size, structure and distribution ofnodules of the species surveyed are reported in Table 1 and measurements ofheight, nodule number, nodule fresh weight, root fresh and dry weight andnitrogenase activity are presented Table 2. All species of Mimoceae andPapilionacae were nodulated whereas all members of Caesalpiniaceae werenon-nodulated. Albizia procera, Albizia lebbeck and Dalbergia sissoo weremoderately-nodulated and sparse nodulation was only recorded in Acaciacatechu. In the other species, abundant nodules were found. Most of thenodules were brown to pink in color and the shape varied from globose tosemi-globose and elongate to elongate with branching. The size varied from2.1 mm× 3.2 mm in L. leucocephala to 5.1 mm× 7.6 mm in A. mangium.Variations in nodule structure and distribution were also observed among thespecies studied (Table 1).The highest number of nodules were recorded in L. leucocephala (82)

followed by A. auriculiformis (55), A. mangium (52), A. lebbeck (46), A.procera (41), D. sissoo (32) and A. catechu (29). Nitrogenase activity per

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329

TABLE

1.Nodulationstatus,color,shape,size(mm),structureanddistributionofnodulesofsomelegumetree

species.

No.

Botanicalname

Nodulation

Color

Shape

Size

Structure

Distribution

status

(mm)

FAMILYMIMOCEAE

1.Albizialebbeck(L.)Benth

Moderate

Browntowhite

Globose

3.1×

3.6

Advance

determinate

Secondaryroots

2.Albiziaprocera(Roxb.)Benth

Moderate

Brown

Sem

iglobose

2.9×

4.1

Advance

indeterminate

Secondaryroots

3.Sam

aniasaman

(Jacq.)Merr.

Abundant

Brownto

Elongateto

3.0×

4.2

Advance

indeterminate

Secondaryroots

darkbrow

nelongatewith

clusters

4.Albiziafalcataria(L.)Forsberg.

Abundant

Brown

Elongatetoelongate.

2.1×

4.3

Advancedindeterminate

Prim

aryroots

with

branching;some

aresemiglobose

type

5.Acaciamangium

Willd.

Abundant

Pink

Elongatetoelongate

5.1×

7.6

Advance

indeterminate

Secondaryroots

with

branching

6.AcaciaauriculiformisA.Cunn.

Abundant

Pink

Elongatetoelongate

5.0×

7.2

Prim

itive

indeterminate

Secondaryroots

Ex.Benth.

with

branching

toadvanced

indeterminate

7.AcaciacatechuWilld.

Sparse

Brown

Globose

to2.4×

2.9

Prim

itive

toadvanced

Secondaryroots

semi-globose

indeterminate

8.Leucaena

leucocephala(Lam

.)de

Wit

Abundant

Pink

Elongatetoelongate

2.1×

3.2

Prim

itive

toadvanced

Prim

aryand

with

cluster

indeterminate

secondaryroot

PAPILIONACEAE

9.Sesbaniasesban

(Linn.)Merr

Abundant

Pink

Globose

with

2.2×

2.6

Advanceddeterminate

Secondaryroots

reticulatesurface

10.Daibergiasissoo

(Roxb.)

Moderate

Brown

Globose,some

1.9×

2.3

Aeschynom

enoid

Secondaryroots

arecircular

CAESALP

INIACEAE

11.CassiafistulaLinn.

Notapplicable

12.Cassiasiam

ea(Lam

k.)

Notapplicable

13.DelonixregiaBolfRaf

Notapplicable

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330

TABLE

2.Plantheight,nodulenumber,nodulefreshweight,rootfreshweight,rootdryweightand

nitrogenaseactivity

(nmoleC2H

4produced)ofsevenlegumetree

species.

Plantandrootparameters

Nitrogenaseactivity

(nmoleC2H

4produced)

No.

Nam

eofspecies

Sub

family

Ht.

Nod.

Nod.Fr.

Rootfr.

Rootdry

Plant−1h−

1g−

1h−

1Nod.−

1h−

1g−

1h−

1g−

1h−

1

(cm)

num.

wt.(g)

wt.(g)

wt.(g)

(Fr.nod.)

(Fr.root)

(Dryroot)

1.A.auriculiformis

Mimoceae

79.6

551.34

16.4

6.1

1291

963

23.4

78.7

211.6

2.A.mangium

Mimoceae

75.3

521.22

12.7

4.9

1125

922

21.6

88.4

229.1

3.D.sissoo

Papilionaceae

66.8

320.82

15.4

8.7

366

447

11.5

23.8

42.0

4.L.leucocephala

Mimoceae

105.5

821.98

18.4

8.8

4914

2482

59.9

266.9

561.5

5.Albizialebbeck

Mimoceae

89.6

461.12

14.7

6.7

2080

1857

45.2

141.3

309.5

6.Albiziaprocera

Mimoceae

81.6

411.05

16.1

7.8

1888

1797

46.0

117.6

243.6

7.Acaciacatechu

Mimoceae

49.6

290.345

10.2

5.4

235

680

8.09

23.0

43.5

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Part II: Microbial Applications 331

plant was highest in L. leucocephala (4913.59 nmole h−1) and lowest in A.catechu (234.7 nmole h−1). Nitrogenase activity per gram nodule freshweight per h, per nodule per h, per gram root fresh and dry weight per h werealso highest in L. leucocephala.

DISCUSSION

Compared with the findings of other workers, the results of our study weresimilar to those of Allen and Allen (1981), Halliday and Nakao (1982) andFaria et al. (1989). The results of Singh and Pokhriyal (1998) and Tewari(1998) are also in agreement with our observations. The reports of Athar andMahmood (1990), Lim and Burton (1982), Mahmood and Athar (1985),Mahmood and Iqbal (1994) are very encouraging and support our results.Failure to find nodules on a given plant at any time does not necessarily

mean that the plant is always non-nodulated (Mahmood, 1994). The non-no-dulating habit of Cassia fistula, Cassia siamea and Delonix regia confirmsthe results of Allen and Allen (1981), Faria et al. (1989), and Mahmood andIqbal (1994). Ty (1996) has also reported the non-nodulating nature of Cassiaand Delonix.Nodule biomass plays an important role in the nitrogen-fixation activity of

the plants. Nitrogenase activity per plant in Leucaena was 280.6%, 336.8%,1242.3%, 136.2%, 160.3% and 1993.5% higher than A. auriculiformis, A.mangium, D. sissoo, A. lebbeck, A. procera and A. catechu. Pokhriyal et al.(1987) has also reported 221.7%, 262.5%, 133.3% higher nitrogenase activi-ty per plant in L. leucocephala than A. lebbeck, A. catechu and D. sissoo.They also found 64%, 62% and 785.7% higher nodule weight per plant inLeucaena compared with Albizia, Acacia andDalbergia. In the present study,nodule number per plant and nitrogenase activity per nodule were also mark-edly higher in Leucaena than other species. Tewari (1998) also found thehighest nitrogenase activity (nmole C2H4 per plant per h) in L. leucocephalaamong several species from a nodulation survey. L. leucocephala has beenfound to develop more effective and active nodules, which is in agreementwith the findings of Tewari (1998).Plant heights also showed a similar trend to that of nitrogenase activity per

plant in all seven species. The highest value for plant height was observed inLeucaena, which was 32.6%, 40.0%, 17.8%, 29.3%, 57.8% and 112.8%higher than A. auriculiformis, A. mangium, A. lebbeck, A. procera, D. sissooand A. catechu, respectively. These findings also support those of Pokhriyalet al. (1987) and Gibson (1976). Nitrogen is the major nutrient required forgrowth of tree crops. Bino (1998) has reported an increase in mean nitrogenfrom 0.48% to 0.53%, phosphorous from 6.65 mg per kg to 8.82 mg per kgand mean organic carbon from 6.79% to 6.81% in the surface soil after NFTS

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NATURE FARMING AND MICROBIAL APPLICATIONS332

were planted. Nitrogen-fixing efficiency of the legumes provides a substan-tial amount of fermentable organic matter for satisfactory microbial activity(Perera et al., 1992). Solubility of nitrogen is also an essential factor thatdetermines the rate of microbial activity (Hoover, 1986). Growing legumeplants in eroded and degraded lands increases the solubility rate of nitrogenand hence microbial activity. Greater nitrogen accretion due to legumes hasbeen reported recently by Singh and Pokhriyal (1998). Higher accretion ofnitrogen ensures higher photosynthetic rates and availability of more photo-synthates in roots results in more energy available for nitrogen fixation andnitrate assimilation in the root nodules (Tewari, 1998) and as a consequencegreater growth and nodulation.Gordon and Wheeler (1978) have reported a significantly positive correla-

tion of net rate of photosynthesis with both nodule fresh weight per plant andnitrogenase activity in Alnus glutinosa. The amount of photosynthates avail-able is considered to be one of the major factors controlling rates of nitrogen-fixation. Increases in height, nodulation and nitrogenase activity in Leucaenamay also be attributed to the availability of more effective strain of Rhizo-bium in the soil. The metabolites produced by these microorganisms increaseroot cell permeability resulting in enhanced root exudation (Barber and Mar-tin, 1976). Increased root exudation would also mean that compounds, suchas flavonoids that are involved in triggering nodulation activity in Rhizobium(Phillips et al., 1995), would be more readily available, leading to higherdensities of Rhizobium nodules per gram of root. In addition, increased leach-ing of root exudates implies that plants divert a greater proportion of theavailable photosynthates to the root systems (Andrade et al., 1998). Thiswould mean that more photosynthates would be available for the Rhizobiumpopulation infecting these roots. A higher nodulation could result in a higherturnover of nitrogen in Leucaena, a greater rhizobial activity in soil andgreater amounts of nitrogen and phosphorus to increase soil fertility. Thiscase may be reverses in other species showing poor performance.

CONCLUSION

The environmental benefits from using biological nitrogen-fixation areseen to be associated with the replacement of chemical based technologieswith a biological system. There is an increasing awareness in many areas thatthe development of ecologically-sustainable production systems are essentialfor maintenance of long-term production at sufficient levels to meet increas-ing demands from increasing populations. On the other hand, deforestation,soil erosion, monocropping, unplanned management of forest land and sever-al other factors have caused serious degradation of our forest lands. Re-searches have shown that declines in soil fertility due to land degradation can

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Part II: Microbial Applications 333

be checked and soil sustainability can be maintained by planting nitrogen-fix-ing tree species. Knowledge of the symbiotic association of different micro-organisms with tree legumes is still very limited and more extensive researchis needed to find ways and means of exploiting legume trees in afforestationprograms For achieving successful afforestation, we should screen and gradeall the nitrogen-fixing tree species depending upon their nitrogen-fixing ca-pacity at different sites. As the species included in the present study areextensively used in different forestry programs in Bangladesh, these findingswould be useful for successful afforestation.

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