Allelopathy in Australia: Bacterial Mediation - ACS Symposium Series

C h a p t e r 15

Allelopathy in Australia: Bacterial Mediation J. V. Lovett

Downloaded by UNIV OF MASSACHUSETTS AMHERST on May 29, 2018 | https://pubs.acs.org Publication Date: January 8, 1987 | doi: 10.1021/bk-1987-0330.ch015

Department of Agricultural Science, University of Tasmania, G.P.O. Box 252C, Hobart, Tasmania, 7001 Australia

Australian workers have reported allelopathic phenomena in native plant communities, both undisturbed and managed. In agriculture, allelochemicals have been identified with plant interference during l i f e and, from their residues, after death. Bacteria are involved in examples of allelopathy from these several milieux. Allelopathy i s currently gaining acceptance as a factor having ecological significance i n Australia, although reports of phenomena which contemporary workers would regard as a l l e l o p a t h i c may be found i n the l i t e r a t u r e over the past 30 years. Such examples represent several broad areas of current i n t e r e s t . Rovira (1) found that 27 amino acids, and various sugars, were excreted by roots of peas and oats and concluded that such excretions were important i n stimulating the growth of microorganisms i n the rhizosphere. Florence and Crocker ( 2 ) implicated antagonistic microbial a c t i v i t y i n autotoxicity of Eucalyptus p i l u l a r i s Sm., and Kimber (3) discussed phytotoxicity that may occur during decomposition of crop residues i n the f i e l d . So far as can be determined there are no early reports of allelopathy manifested by weed species. However, a l l 18 of the world's worst weeds, as i d e n t i f i e d by Holm et a l . (4) (Table I ) , are present i n Australia and many of them have been associated with allelopathy. More recent work can, for convenience, be divided into that dealing with plant species native to Australia (Table I I ) and plants which have, accidentally or d e l i b e r a t e l y , been introduced to the continent (Table I I I ) . Lovett (31) has reviewed these studies, and examples i n both categories w i l l be b r i e f l y discussed. Allelopathy and Native

Species

Rabotnov (32) considers that allelopathy contributes to maintaining homeostasis i n natural plant communities. Economically important losses may occur when the ecological balance i n such communities i s disturbed. For example, Booth and Barker (33) recorded l o s t grazing capacity due to invasion of pastoral lands by shrub species such as 0097-6156/87/0330-0156$06.00/0 © 1987 American Chemical Society

Waller; Allelochemicals: Role in Agriculture and Forestry ACS Symposium Series; American Chemical Society: Washington, DC, 1987.

15.

LOVETT

Allelopathy

in Australia:

Bacterial


Table I The World's Worst Weeds

Botanical Name 1. Cyperus rotundus 2. Cynodon dactylon 3. Echinochloa c r u s - g a l l i 4. Echinochloa colonum 5. Eleusine indica 6. Sorghum halepense 7. Imperata c y l i n d r i c a 8. Eichhornia crassipes 9. Portulaca oleracea 10. Chenopodium album 11. D i g i t a r i a sanguinalis 12. Convolvulus arvensis 13. Avena fatua, et a l . 14. Amaranthus hybridus 15. Amaranthus spinosus 16. Cyperus esculentus 17. Paspalum conjugatum 18. Rottboellia exaltata

157

Mediation

(4)

Common Name Australia nutgrass couch grass barnyard grass awnless barnyard grass crowsfoot grass Johnson grass blady grass water hyacinth pigweed fat hen summer grass bindweed wild oats slim amaranth p r i c k l y amaranth nutgrass sour grass kokoma grass

U.S.A. purple nutsedge Bermuda grass barnyard grass jungle r i c e goosegrass Johnson grass cogon grass water hyacinth common purslane lamb's-quarters large crab grass f i e l d bindweed wild oats smooth amaranth spiny amaranthus yellow nutsedge sour paspalum Raoul grass

Eremophila s t u r t i i R.Br, and Dodonaea attenuata A.Cunn. i n western New South Wales (Table IV). Overgrazing by introduced domestic livestock and the r e l a t i v e absence of f i r e since European settlement are implicated i n the development of this situation which, i n several respects, resembles that of the C a l i f o r n i a n chaparral communities (34). Allelopathy i s a possible contributing factor. Many Eucalyptus species are economically important for t h e i r timber, their essential o i l content, or their contribution to reafforestation in tropical and subtropical countries. Monoterpenoids, which have been linked with allelopathy by several workers, including Muller (34) and Lovett (24)> are common constituents of Eucalyptus o i l s . These and other compounds may contribute to a l l e l o p a t h i c manifestations by Eucalyptus baxteri ssp. (9), E. regnans F.Muell. (1^3) and E. globulus ssp. (8"). Allelopathy and Introduced Species Examples of allelopathy between weeds and crop or pasture species i n Australia have been documented within the past decade. Lovett and Lynch (17) discussed the association of Salvia reflexa Hornem. (mintweed), an annual member of the family Lamiaceae introduced to Australia from North America (35)· This species produces aromatics as well as water-soluble compounds that may be i n h i b i t o r y to species such as wheat and sorghum. Kloot and Boyce (_21) documented i n h i b i t o r y effects of allelochemicals produced by Polygonum aviculare L. (wireweed) on the annual Medicago species, important leguminous components of annually regenerating pastures i n southern Australia.



(12)

Ashton and W i l l i s

Willis

Lange and Reynolds

(13)

(11)

1982

198Ο

Eucalyptus regnans

Eucalyptus microcarpa

Nothof agus ninghami i and other r a i n f o r e s t species

Eucalyptus b i c o s t a t a

Pinus sp., A r a u c a r i a sp. F l i n d e r s i a sp.

C a l l i t r i s calcarata Eucalyptus crebra E. dawsoni i E. m e l l i o d o i a Not elaea microcarpa

Casuarina leuhmanii

Acacia pendula

Eucalyptus mol] uccana

Eucalyptus p i l u l a r i s

A l l e l o p a t h i c species

H I i s et al . (10)

19 S3

1976

1 *•>02

Eucalyptus b a x t e r i i

(7)

(2)

repens

Seedlings of E. regnans

Gonocarpus elatus

Seedlings of E. regnans

Leptospermum myrsinoides Casuarina

Festuca rubra var. fa"l lax

Trifolium

Bothriochloa ambigua Eragrosti s J eptostachya Sporobolus elongatus

Seedlings of E. pi 1 u l a r i s

Species a f f e c t e d

Lipids

Lipids

Gentisic,ellagic g a l l i c , sinapic, caffeic acids Phenolic aglycones Glycosides Terpenoids

Alleiochemicals present

Chemicals from f o l i a r and l i t t e r leachates i n h i b i t ory i n bioassays

Frass from Paropsis atomaria r e s u l t e d i n growth inhibition

Sensitive to s o i l type

'Halo' e f f e c t v i s i b l e on a e r i a l photographs

Microorganism antagonism implicated

NH3/NO4 balance c r i t i c a l f o r seed ling survival. Mature t r e e s strongly mycorrhizal competition w i t h microorganisms f o r NH3. A n t a g o n i s t i c s o i l f a c t o r s may be a f f e c t e d by root exudates

Suppression of G. e l a t u s under E. microcarpa

Dieback of mature trees; i n h i b i t i o n of r e g e n e r a t i o n by seedlings

Suppression of L. myrsinoides and C. p u s i l l a Feneath canopy of E. b a x t e r i i

E x c l u s i o n from zone around E. b i c o s t a t a

Species compos i t i o n within 'circle' effect of t r e e s d i f f e r ent t o o u t s i d e

Grasses statistically sparser beneath t r e e canopies

"Prima f a c i e " evidence

Difference i n F a i l u r e of seedabundance of r h i 20- l i n g s t o r e sphere fungus, generate i n Cylindrocarpon absence of f i r e destructans, between healthy and unhealthy roots of s e e d l i n g s

I n h i b i t i o n of growth

I n h i b i t i o n of growth

Blackening of radicle tips

Seedling t i p necrosi s, chlorosi s

A f f e c t s root and root h a i r development and shoot growth

Effects

Reports of Allelopathic Phenomena i n A u s t r a l i a — Native Species

Del Moral et a l . (9)

(8)

and S i lander

S i l a n d e r et a l .

Trenbath

A uthor* s ) Florence and Crocker

Table I I .


70

Ά

m

70

m > Z D *n Ο

70

n c r H G

> ο

ο

70

>

m g ο

χ

r r m r Ο ο

>


(20)

K l o o t and Boyce (21)

Lovett et a l .

1982 Polygonum a v i c u l a r e

1981 Datura stramonium

Medicago

truncatula

Linum u s i t a t i s s i m u m

Linum u s i t a t i s s i m u m

198l Camelina s a t i v a

Lovett and D u f f i e l d (19)

T r i t i c u m aestivum

1979 S a l v i a r e f l e x a


Tropane alkaloids

benzlyamine

Carduus pycnocephalus Cirsium vulgare C. arvense Hordeum d i s t i c h u m LOT ium perenne T r i f o l i u m subterraneum Silybum marianum



T r i t i c u m aestivum Avena s a t i v a

Lovett and Speak (18)

1975 C i r s i u m arvense

1973b T r i t i c u m aestivum (residuesl

Secale c e r e a l e Pisurn sativum (residues )

1973a Hordeum v u l g a r e Avena s a t i v a

1967 T r i t i c u m aestivum (residuesl

Year A l l e l o p a t h i c species Species a f f e c t e d

1979 S a l v i a r e f l e x a

(3)

Allelochemicals present

Reduced germination and i n h i b i t i o n of r a d i c l e growth Causes m o r p h o l o g i c a l deformities i n germinating medic s e e d l i n g s by i n t e r fering with c e l l d i v i s i o n and e a r l y growth o f meristems

High c o n c e n t r a t i o n s of benzylamine inhibited radicle elongation

I n h i b i t i o n o f germin a t i o n and e a r l y growth

I n h i b i t i o n o f germin a t i o n and e a r l y growth

I n h i b i t i o n o f seed germination and s e e d l i n g growth

Reduction o f germin a t i o n , growth and ultimate y i e l d

I n h i b i t i o n o f root growth

Root growth reduced

Water s o l u b l e allelochemicals present i n green l e a v e s and stems

Phyllosphere bact e r i a - Pseudomonas f l u o r e s c e n s and Enterobacter cloacae convert benzyl i s o t h i o c y a n ate t o benzylamine and hydrogen sulphide

Continued on next page

F a i l u r e o f medic pastures to s e l f - r e g e n e r a t e i n paddocks dominated by Polygonum

A noxious weed, e s p e c i a l l y of summer crops

F i e l d e f f e c t s noted by e a r l i e r workers

Trichomes i m p l i c a t ed as r e s e r v o i r s for allelochemicals

S o i l type shown t o a f f e c t expression of a l l e l o p a t h y

C. arvense i s autot o x i c - both r o o t s r o o t s and f o l i a g e i n h i b i t growth o f seeds and s e e d l i n g s

E f f e c t diminished w i t h time. Ν immobilization may be i n v o l v e d

Toxic e f f e c t i s o f an ephemeral nature

Phytotoxic effect d i m i n i s h e d with time, depended on previous weathering and v a r i e d w i t h v a r i e t y of wheat

Comments

Species

Observed c o m p e t i t i v e a b i l i t y i n the f i e l d

F a i l u r e o f C. seedlings

Proximity o f new wheat straw r e s i d u e s t o sown wheat seed

Germination, p l a n t growth and u l t i m a t e y i e l d affected

"Prima f a c i e " evidence

Reports of A l l e l o p a t h i c Phenomena i n Australia—Introduced

Lovett and Lynch ( .17)

Kimber

Table I I I .



1985 Brassica napus Sorghum bicolor Pisum sativum Helianthus annuus Triticum aestivum (residuesl

Imperata cylindrica (L.) Beauv.

1984 Datura stramoni'

Avena fatua Avena ludoviciana

subterraneum Calopogonium mucunoides

nthus annuus

et al. (30)1986 Brassica campestris Triticum aestivum B. juncea B. napus B. nigra

Purvis et al.

Levitt et al. (27)

Helianthus annuus

Calotropis procer;

1984 Cenchrus ciliaris

Levitt and Lovett (26) 1984 Datura stramonium

Triticum aestivum

1983 Salvia reflexa

Songlei

Inhibition of radicle growth

Suppression of root, stem and leaf growth of Calotrope seedlings Inhibition of radicle growth

Germination and seed ling growth adversely affected

A noxious weed which colonizes large areas to the virtual exclusion of other species

Calotrope seedlings fail to establish in well grown buffel grass areas

Crop residues may have a deleterious affect on the following crop and may also affect weed growth

"Prima facie" evidence

Variable inhibition of Effects persisted through growth to final grain yield

£-hydroxyDelay of germination benzoic acid and inhibition of vanillic acid radicle growth £-coumaric acid ferulic acid Germination and growth of wild oats differ entially affected by crop residues

Tropane alkaloids

Tropane alkaloids

Monoterpenes

Crop residues affect early growth of wheat by affecting germination emergence, coleoptile height and length of longest seminal root

Allelochemicals present Year Allelopathic species Species affected Inhibitioi of early 1982 Camelina sativ, Linum usitatissimum Benzylamine growth

Continued

Lovett and Jessop (23) 1982 Pisui Vicia faba c Glycine max Lupinum angustifolius Cicer arietinum Carthamus kinctorius Helianthus annuus Brassica napus Sorghum bicolor Avena sativa Hordume vulgare Triticum aestivum

Table I I I .


Effects documented in the field

Implications for crop rotation development

Primary effect of allelochemicals on metabolism of food reserves. Effect documented in the field Soil type shown to affect expression of allelopathy

Unidentified but active watersoluble compound(s) also present

Comments Indirect effect of benzylamine through creation of hydro phobic conditions in soil Phytotoxic effect increased when crop residues were incorporated into the soil

70

H 70

tn C/3

70

D Ο

> z

ο c r H G 70 m

> ο

ο

70

>

m g

χ

r m r Ο π

ON Ο

15.

LOVETT

Grazing

Allelopathy

Capacity

in Australia:

Bacterial

Table IV Loss Due to Shrub Invasion on Located West of Wanaaring (33)


Lost grazing capacity Property A Β C D Mean a

161

Mediation

C were inspected

Properties

Lost grazing capacity

(1978X56)

(1968-70)(36)^ 1 4 6 9 5

Properties A, Β and

Four

8

10 22 15 14 i n 1968

and

property

D in

1970.

An example of allelopathy by a useful, introduced pasture grass against a weed i s provided by Cheam (25, 36) who has studied the effects of Cenchrus c i l i a r i s L. (buffel grass) on Calotropis procera (Ait.) W.T. A i t (calotrope), also an import to Australia LMeadly (37)]. Sixand 9-week old b u f f e l grass plants s i g n i f i c a n t l y suppressed the growth and development of calotrope seedlings, which were also i n h i b i t e d when grown i n s o i l which previously supported a b u f f e l grass stand (Table V). Cheam (36, 38) considers that planting of b u f f e l grass w i l l prevent ingress by calotrope i n areas that are now free of the weed, that introduction of b u f f e l grass on land already infested should lead to a steady decline i n the calotrope population, and that the bioactive compound may prove useful as a 'natural herbicide' for C. procera and other species. Table V Germination and Growth of Calotrope i n S o i l i n which Buffel Grass Had Grown for 6 Weeks Previously [The treated s o i l was free from b u f f e l grass roots.] (25) Cumulative germination(%) Growth response Weeks a f t e r sowing Plant F i r s t pair of true leaves Treatment 1 week 2 weeks height(mm) Length(mm) Breadth(mm) Control s o i l EÔ7Ô W7j 49.6 3075 Γ8Τ5 Treated s o i l 83.3 90.0 32.8 21.7 12.8 Level of significance N.S. N.S. Ρ = 0.001 Ρ = 0.001 Ρ = 0.001 This example illustrates the benefits and costs of introducing plants to new l o c a l i t i e s . Over the mere two hundred years of European settlement i n Australia many of the World's most important crop and pasture plants and a l l of the World's worst weeds (Table I) have been introduced to the continent. The l a t t e r have attained problem status and several other introductions, such as Echium plantagineum L. (Paterson's Curse) from the Mediterranean region, freed from those organisms which maintain them i n balance i n their native communities, have posed threats to agriculture.


162

ALLELOCHEMICALS: ROLE IN AGRICULTURE AND

FORESTRY

Parthenium hysterophorus L. (parthenium weed), native to North and Central America and introduced into Queensland as recently as I960 (39)> is contemporary example. It i s aggressive, persistent and lowers crop y i e l d through interference, a component of which i s a l l e l o p a t h i c (40). a


Allelopathy and Microorganisms The production of compounds which may act as allelochemicals i s not r e s t r i c t e d to higher plants. For example, Heisey, DeFrank and Putnam (41) have discussed substances produced by soil microorganisms which may have h e r b i c i d a l a c t i v i t y . Bacteria may also mediate a l l e l o p a t h i c a c t i v i t y i n economically important situations such as forest regeneration (Line, personal communication); crop/weed associations (42), and reduced c u l t i v a t i o n systems where plant residues are retained (43). Cruciferous species, i n which the glucosinolates are b i o l o g i c a l l y active compounds (44), have been studied i n both of the latter categories. In A u s t r a l i a , allelopathy has been associated with introduced c r u c i f e r s such as Brassica t o u r n e f o r t i i Gouan (wild turnip) and a more complete study has been made of Camelina sativa (L.) Crantz (false f l a x ) . Grummer and Beyer (45) reported allelopathy between Linum usitatissimum L. and Camelina species i n the f i e l d , providing that r a i n f e l l during a c r i t i c a l (unspecified) period of growth. Lovett and Sagar (42), working i n the United Kingdom, established that the presence of bacteria i n the phyllosphere of C. sativa was necessary for allelopathy to be manifested. The organisms were f r e e - l i v i n g , motile, Gram-negative rods representative of the bacteria which tend to predominate i n the phyllosphere (46) and were i d e n t i f i e d as Enterobacter cloacae (Jordan) Hormaeche and Edwards. In subsequent work, carried out i n A u s t r a l i a , Pseudomonas fluorescens (Trevisan) Migula has been i d e n t i f i e d as playing a similar role (47)· Typically, bacteria are recovered from aqueous washings of fresh f o l i a g e of C. sativa. I f foliage washings are incubated at +23 C for 24 h the washings become strong smelling and cloudy i n appearance. I f bacteria are removed from the washings a f t e r c o l l e c t i o n , by f i l t r a t i o n , no change i s noted. GC/MS analyses have shown that organic acids of the c i t r i c acid cycle are present i n fresh washings but are much depleted a f t e r 24 h incubation with bacteria (Figure 1, Figure 2). Similar results are obtained by inoculation of l e a f washings, freed of bacteria by M i l l i p o r e f i l t r a t i o n , with either of the two bacteria i d e n t i f i e d (19)» Lovett and Jackson (47) observed that C. sativa l e a f washings exhibited allelopathic activity in bioassay after incubation for as l i t t l e as 12 h and demonstrated that during this period of time there was exponential growth of the b a c t e r i a l population (Figure 3). Benzyl isothiocyanate was i d e n t i f i e d i n aqueous extracts of C. sativa f o l i a g e by Lovett and D u f f i e l d (19). Tang, Bhothipaksa and Frank (48) showed that E. cloacae was capable of degrading benzyl isothiocyanate to hydrogen sulfide and benzylamine. Tests were, accordingly, carried out with incubated l e a f washings of Camelina and showed the presence of hydrogen sulfide and



LOVETT

Allelopathy

in Australia:

Bacterial

163

Mediation

100"

50-

-l 100

1 2 0 0

1

1

1

I

3 0 0

4 0 0

500

6 0 0

Scan number

Figure 1. Total i o n current of η-butyl esters of the a c i d i c f r a c t i o n from non-sterile leaf washings of C. sativa. Key: 1 = oxalic acid; 2 = malonic acid; 3 = maleic acid; 4 = succinic acid; 5 = fumaric acid; 6 = alpha-ketoglutaric acid; 7 = c i s - a c o n i t i c acid; 8 = c i t r i c acid (19)«



ALLELOCHEMICALS: ROLE IN AGRICULTURE AND FORESTRY

ι oo-i

50-

Scan number

F i g u r e 2. T o t a l i o n c u r r e n t o f n - b u t y l e s t e r s o f t h e a c i d i c f r a c t i o n f r o m s t e r i l e l e a f w a s h i n g s o f C. s a t i v a . Key: 1 = oxalic acid; 2 = malonic acid; 3 = maleic acid; 4 = succinic acid; 5 = fumaric acid; 6 = malic acid; 7 = alpha-ketoglutaric a c i d ; 8 = c i s - a c o n i t i c a c i d ; 9 = c i t r i c a c i d . (Reproduced w i t h p e r m i s s i o n f r o m r e f e r e n c e 19. C o p y r i g h t 1981 B l a c k w e l l Scientific Publications Ltd.)



15.

LOVETT

A llelopathy

in A ustralia: Bacterial

165

Mediation

F i g u r e 3. I n c r e a s e i n b a c t e r i a l c o l o n y numbers incubation period. (Reproduced w i t h permission C o p y r i g h t 1980 The New P h y t o l o g i s t . )

d u r i n g a 24-h from reference


47.


166

ALLELOCHEMICALS: ROLE IN AGRICULTURE AND

FORESTRY

benzylamine (19). The l e v e l of the l a t t e r component, i n p a r t i c u l a r , i s variable depending on age of the plant and season of the year. This observation accords with the report of Griimmer and Beyer (45) that allelopathy i n the f i e l d occurred only at a p a r t i c u l a r time of the year. Our data (43) have demonstrated that bacteria are most p r o l i f i c on senescent leaves, a f i n d i n g which agrees with that of E t t l i n g e r and Kjaer (49), namely that i n j u r y to plants containing glucosinolates r e s u l t s i n the l i b e r a t i o n of isothiocyanates from those substances. Thus, the presence of available quantities of isothiocyanate and large numbers of bacteria during senescence of the weed could explain f i e l d observations of allelopathy. Two e f f e c t s of benzylamine as an allelochemical have been documented. When L. usitatissimum i s used i n bioassay, germination i s impaired but only at r e l a t i v e l y high concentrations of the allelochemical ( i n excess of 500 ppm). Radicle length of germinating L. usitatissimum i n bioassay i s increased at low concentrations of benzylamine (less than 200 ppm) but is increasingly i n h i b i t e d as concentration increases. In soil, however, i n h i b i t i o n may occur even at low concentrations (Figure 4), probably as a result of improved contact between germinating seedlings and substrate. In addition to direct effects on the plant, benzylamine may induce hydrophobic (water repellent) conditions i n s o i l (Figure 4 ) . These data indicate a l i n e a r increase i n moisture content as benzylamine content increases, a t t r i b u t a b l e to the development of a lower unsaturated hydraulic conductivity i n the surface s o i l , which thus became less able to transfer water from depth i n response to evaporative demand. McGhie (50) suggests that poor germination of crop and pasture plants may be related to the development of hydrophobic conditions, the affected s o i l being unable to supply water to the germinating seed. Strains of E. cloacae are known to f i x nitrogen (51). An additional component of the complex Camelina/Linum/bacteria association was the f i n d i n g by Lovett and Sagar (42) that E. cloacae cultured from C. sativa f o l i a g e washings gave indications (through acetylene-ethylene assays) of a nitrogen-fixing c a p a b i l i t y . It i s not known whether such nitrogen contributes to the nitrogen economy of the plant, although Jones (52) suggests several means by which nitrogen fixed i n the phyllosphere of conifers may aid the growth of these trees. Both E. cloacae and P. fluorescens are capable of a c t i v i t y i n the phyllosphere and i n s o i l . This may be of significance i n r e l a t i o n to the findings of E l l i o t t and Lynch (53) and Lynch and Clarke (54) that pseudomonads, i n large numbers, are a dominant feature of the microflora of the rhizosphere and straw of some temperate cereals. Among the plant growth-promoting rhizobacteria that are being tested for commercial applications, Burr and Caesar (55) have found the most e f f e c t i v e strains to be fluorescent Pseudomonas species. Lynch and Clarke (54) suggested that some strains of pseudomonads stimulate root and shoot extension and dry matter production of barley, a species that shows variable s e n s i t i v i t y to benzylamine (Figure 5)· However, E l l i o t t and Lynch (53) indicated that pseudomonads antagonistic towards seedling growth colonize roots of wheat, their i n h i b i t o r y effects also


Allelopathy in Australia: Bacterial Mediation


LOVETT

CONCENTRATION (ppm, A

WATER

•

LENGTH

CONTENT

OF

OF RADICLE

l o g

e

OF

BENZYLAMTNE

scale)

SOIL (r

0.*Q2;

ρ

Allelopathy in Australia: Bacterial Mediation - ACS Symposium Series

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