ROCZNIKI GLEBOZNAWCZE T. XLIV NR 3/4, WARSZAWA 1993:45-53 J Ó Z E F K O B U S , JA N C Z A B A N , A N N A G A J D A , D A N U T A M A S IA K , A N D R Z E J K S IĘ Ż N I A K
W H E A T R H IZ O S P H E R E M IC R O F L O R A A N D ITS E F F E C T ON
P L A N T N U T R IT IO N A N D S O M E P A T H O G E N IC FU N G I.
P A R T I. C H A N G E S O F R H IZ O B A C T E R IA L P O P U L A T IO N S
W IT H D E V E L O P M E N T OF W IN T E R W HEA T*
D e p a rtm e n t A g ric u ltu ra l M ic ro b io lo g y . In s tiu te o f S o il S c ie n c e a n d P la n t C u ltiv a tio n a t P u ła w yIN T R O D U C T IO N
Several studies on bacterial population within the root environment of plants
have shown that the fluorescent Pseudom onas constitute a major group of
rhizobacteria [7,12,18,30]. Certain isolates of these fluorescent Pseudom onas,
mainly P . fluorescens and P. putida strains, can stimulate the growth o f several
crops and thereby significantly increase their yield. These bacteria were termed
plant growth promoting rhizobacteria (PGPR) by Kloepper et al.[13].
In some cases, the biological activities of inoculants were screening for their
bio-control pontency. Some of the isolated rhizosphere different genera have
been examined for the presence of antifungal secondary metabolites [1,4-
6,10,16,23-26].
The results obtained by different authors demonstrate that there is still a
considerable need for extensive inventory studies on rhizobacterial populations
to understand changes in their composition under different environmental
factors [14,15,17,26-29].
In this connection the aim of present studies is to recognize: 1) variations
o f bacterial populations during the growing seasons on winter wheat and 2)
* T h is study w as supported by the grant No M R/USDA-89-3 for the D epartm ent of Agricultural M icrobiology o f Institute of Soil Science and Plant Cultivation in Puławy. We thank Prof. W . M yśków for helpful suggestions in the interpretations o f the presented results.
46
J. Kobus, J. Czaban
,
A. Gajda, D. Ma siak, A. Księżni ak
composition of bacterial populations in soil adhering to roots, on root surface
and in the root inside.
S O IL A N D P L A N T M A T E R IA L
Winter wheat Tviticum aestivum L. cv. Gama, sown on 10 September 1989,
was grown on the Experimental Station Field of the Institute of Soil Science
and Plant Cultivation in Puławy. The soil was loess, content of С - about 0.8%,
N - 0.082%, pH (H20 ) - 7.2
S A M P L IN G
Samples of soil with growing wheat plants were taken on: October 10,1989
- at the 2 leaves stage, April 27, 1990 at the 4 leaves stage, June 5, 1990 at the
flowering stage, and July 20, 1990 at the full ripeness stage.
P R E P A R A T IO N O F P L A N T R O O T S W IT H S O IL F O R A N A L Y S E S
The roots of wheat were gently removed from soil, and then excess of soil,
were shaken off, leaving only the thin layer of soil on the root surface.
Ten grams of wet roots with adherent soil were transferred to the bottle
containing 100 ml o f sterile water and shaken for 30 minutes. The soil
suspension obtained by shaking was the 1st fraction of the rhizosphere.
Another part of wheat roots, removed from soil at the same manner as above,
was washed with tap water.The washed roots were rinsed 10 times with sterile
water by hand shaking. The roots samples without soil residues were transferred
to the bottles containing 100 ml of sterile water and 30 g of coarse sand. This
mixture was shaken for 30 minutes. The suspension of the external parts of the
wheat roots, removed during shaking with sand-water mixture was the 2nd
fraction of what rhizosphere (rhizoplane).
After preparation of 2nd fraction, the wheat roots were rinsed with sterile distilled
water several times, then divided into two parts. One of the parts was sterilized with
70%; ethanol and next with 3% H
2O
2, both for 15 minutes. The 2nd part of the wheat
roots was non sterile. Both parts were homogenized in glass Potter homogenizer,
containing 25 cm3 of sterile distilled water. Homogenate of the unsterilized roots
was the 3rd fraction (total endorhizosphere and possibly some not determined
residues of rhizoplane). The homogenate of the sterilized roots was the 4th wheat
rhizosphere fraction (endorhizosphere or some part of it, because we do not know if
ethanol or H
2O
2penetrate root cells, and sterilize to some extent the root inside). The
4th rhizosphere fraction was a part of the 3rd fraction.
M E D I A
“Total num bers” of bacteria were determined on King, Ward and Raney
medium [11], and total number of non-symbiotic nitrogen fixing bacteria on
Burk's medium as described by Brotonegore [3].
Wheat rliizospliere microflora
.
47
Identification o f bacteria are described in “Laboratory Methods in M icro
biology” [8]. The isolated bacteria were identified according to Bergey s
Manual of Systematic Bacteriology [2].
R E S U L T S A N D D ISC U SSIO N
B a c te ria l C o m m u n itie s O f W in te r W h e a t R h iz o s p h e re
Bacterial communities associated with winter roots system (Triticum aesti-
vum L. cv. Gama) were evaluated 4 times from early stage of plant growth to
full ripeness under field conditions. The distribution of bacterial populations
in the examined rhizosphere fractions: in soil adhering to roots, on the roots
surface (rhizoplane) and in the roots inside (endorhizosphere) were studied as
well (Tables 1-3).
No marked differences were pronounced in the numbers of bacteria isolated
with the use of K ing ’s medium at the following periods: the 2nd leaf (October
10,1989), the 4th leaf (April 27,1990) and flowering (June 5,1990). However
at full ripeness period (July 20, 1990) distinct increase of numbers of these
bacteria, especially in the roots inside (endorhizosphere), was observed (Tables
1, 2). This phenomenon was certainly caused by decrease of resistance o f the
dying roots against microorganisms penetrations. The augmentation of rhizo-
bacterial populations with the progressing of plant growth was also reported
by Iswandi et al. [9]. On the other hand Liljeroth and Baath [19] have noticed
in the research on barley rhizosphere the decrease of bacteria number in the
older plants.
Tabela 1
N um bers of bacteria in w inter wheat rhizosphere fractions on K ing's medium (x 1()6 g '1) per g d.m. of soil ( 1 ) or roots (2-4)
Fractions
Whe at growth stages
2nd leaf 4th leaf flowering full ripeness 1. Soil adherent to roots 2529.9a 2187.4 2662.9 3103.6 2. Roots surface (rhizoplane) 806.9b 1345.5 1336.5 1269.8 3. E ndorhizosphere + rhizoplane 9690 919.4 1088.0 2016.7
4. Endorhizosphere 3.05 2.93 2.36 262.1
Total roots fractions
2+3 1775.8 2264.9 2424.5 3286.5
Л T h e n u m b e r o f b a c te ria (c fu ) in g o f soil a d h e re n t to ro o ts (fra c tio n s 1). T h e n u m b e r o f b a c te ria (c fu ) in g o f ro o ts (fra c tio n s 2, 3 a n d 4).
48
J. Kobus, J. Czaban, A. Gajda, D. Ma siak, A. Księżniak
The studied bacterial populations varied singificantly as influenced by the
kind of rhizosphere fraction. The numbers of these bacteria prevauled in the
soil adhering to the roots (81-96%) with the decreasing value at the older plants
(Table 2). This phenomenon might be explained by gradual decrease of ratio
of rhizosphere soil: roots in the examined samples. The populations of bacteria
found in the endorhizosphere (4th fraction) were only the minute part of the
rhizobacterial numbers (0.007 - 1.5%, Table 2). It is worth to mention that the
numbers of determined bacteria, colonizing the roots surface and roots inside
during plant growth, calculated per 1 g of roots d. m . , were in the same range
as the numbers of these bacteria in the rhizosphere soil (from about 2 x 109 to
3 x l 0 9, Table 1).
Tabela 2
Distribution of bacteria in wheat rhizosphere
l 'raclions
2nd leaf :stage 4th leaf stage Flowering stage Full ripeness stage
x 106 % x 106 % x 106 % x 106 % 1 16545.5 95.9 14799.95 94.S 14060.1 86.6 16799.8 81.0 2 321.1 1.9 487.1 3.1 1202.85 7.4 1523.8 7.3 3 3S5.7 2.2 332.8 2.1 979.2 6.0 2420.0 11.7 4 1.21 0.007 1.06 0.007 2.2 0.013 314.5 1.5 Total 17252.3 15619.85 16242.15 20743.6
T h e v a lu e s w e r e c a lc u la te d by m u ltip lic a tio n o f th e dry w e ig h t o f soil o r ro o ts ( i n g ) in w h o le 10 g o f fresh ro o ts + a d h e re n t so il s a m p le s by th e b a c te ria n u m b e rs (c fu ) in g soil (fra c tio n 1) o r ro o t ( fr a c tio n s 2 , 3 , 4 ).
Tabela 3
N um bers of bacteriai in winter wheat rhizosphere on B u rk 's N-fri•e medium (x 106 g"1 of soil or roots)
Fourth leaf stage Full ripeness stage
Fractions
numbers
in per cent of the total number of bacteria on the
K ing’s medium
in per cent of the total . number of bacteria on the numbers Kjng s medium 1 1167.6 53.4 2095.0 67.5 2 678.6 50.4 550.8 43.4 3 685.2 74.3 1714.2 85.0 4 2.35 80.3 63.3 25.5 E x p la n a tio n s as in T a b le 1.
Table 4
Qualitative composition o f bacterial populations in the exam ined fractions of wheat rhizosphere at different stages o f the plant growth, isolated w'ith the use of K ing’s medium (per cent)
2nd leaf stage 4th leaf stage Flowering stage Full ripeness stage
Genus or groups o f bacteria fractions
1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4
G ra m -n e g a tiv e b a c te ria :
Pseudom onas (producing fluoroscent pigments) 22.8 25.5 29.6 12.1 18.8 34.2 33.3 42.1 2.6 3.9 3.2 82.7 0 3.1 6.2 3.5
Pseudom onas - like (not producing fluoroscent
pigments) 3.5 9.5 1.85 0 7.25 5.1 6.9 1.7 2.6 10.7 6.4 1.3 4.9 3.1 4.2 3.5
A lcaligenes-like 7.0 2.0 1.85 0 1.5 0 1.2 0 2.6 2.9 6.4 0 13.1 4.1 18.7 12.3
E nvinia (about 2/3 E. carotovora, 1/3 E.
herbicoid) 19.3 17.6 27.8 69.8 0 0 0 0 0 0 0 0 14.8 2.0 0 3.5
J anthinobacterium 0 0 0 0 0 0 0 0 2.6 0 0 0 0 0 0 0
X anthom onas - like 1.75 5.9 7.4 3.0 0 1.2 2.3 0 5.3 8.7 7.1 5.3 3.3 7.1 2.1 7.0
Others - motile, colourless oxidase negative
bacteria 5.3 25.5 13.0 3.0 0 5.1 3.4 5.3 2.6 14.6 7.1 2.7 4.9 3.1 14.6 5.3
Klebsiella 1.75 2.0 1.85 0 0 0 0 0 0 0 0 0 0 0 0 0
F lexibacter - like 8.8 2.0 3.7 0 21.7 17.7 27.6 14.0 26.4 23.3 33.3 0 9.8 10.2 0 1.8
A cinetobacter - like 10.5 2.0 0 0 7.25 3.8 3.4 0 0 6.8 4.5 0 1.6 2.0 4.2 1.8
Others - non motile, colourless, oxidase positive 3.5 2.0 3.7 0 10.1 5.1 1.2 0 7.9 8.7 7.1 0 9.8 5.1 12.5 8.8 G ra m - po sitiv e b a c te ria : B acillus 1.75 2.0 0 3.0 1.5 2.5 0 12.3 7.9 1.9 8.3 8.0 4.9 9.2 0 5.3 M icrococcus 3.5 2.0 1.85 3.0 0 6.3 0 0 5.3 1.0 0.6 0 1.6 9.2 2.1 1.8
W
he
a
t
rh
iz
os
ph
er
e
m
ic
r
o
ß
o
r
a
...
2nd leaf stage 4th leaf stage Flowering stage Full ripeness stage
Genus or groups of bacteria fractions
1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4
Coryneform group (various Gram-positive rods) 7.0 2.0 7.4 6.1 31.9 19.0 20.7 24.6 26.3 17.5 16.0 0 31.3 41.8 35.4 45.4
Actinomyces 3.5 0 0 0 0 0 0 0 7.9 0 0 0 0 0 0 0 Numbers of isolates 57 51 54 33 69 79 87 57 38 103 156 75 61 98 48 57
J.
K
o
b
u
s,
J.
C
za
b
a
n
,
A
.
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,
D
.
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.
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Wheat rhizosphere microflora.
51
The size o f bacterial populations growing on the B urk’s N-free medium
changed also as influenced by the growth stage of winter wheat and the kind
o f rhizosphere fraction. In general, the number of examined bacteria showed
the similar pattern to the bacterial numbers on the K ing ’s medium (Table 3).
Similar results in the researches on rhizobacteria of grass plants were obtained
by Lawley et al. [17]. It is worth to notice that some o f the mentioned bacteria,
belonging to K lebsiella and Erwinia genera, were able to fix N
2.
Bacterial genera o f winter wheat rhizosphere
Azotobacter cells were found only in the soil adhering to the roots of winter
wheat.
The majority of bacteria isolated from rhizosphere and roots surface on winter
wheat belonged to the Pseudomonas, Etwinia and Flexibacter genera (Table 4).
It is worth to refer to results of Kleeberger et al. [12] who have found the
predominance of pseudomonads in the rhizospheres of wheat. Etwinia was
numerous only at the
2nd leaf stage, and fluorescent pseudomonads at the two first
stages in all studied rhizosphere fractions, moreover in the roots inside at the
flowering. Flexibacter was abundant at 4th leaf and flowering stages, except the
roots inside (4th fraction). Also Gram-positive rods - Coryneform group were
relative numerous. This group occurred in larger numbers starting from the 2nd
stage of plant growth. At full ripeness Coryneform bacteria reached the maximal
value, becoming the predominant group of the isolated bacteria in all rhizosphere
fractions. It should be emphasized that, in general, fluorescent pseudomonads and
Erwinia spp. were prevailed on the roots and in their inside, opposed to Coiyneform
bacteria which were the main group of rhizosphere soil. Other genera of bacteria
as: Xanthom onas, Alcaligenes, Klebsiellay Acinetobacter, Janthinobaclcrium,
Bacillus, M icrococcus and non-fluorescent pseudmonads occurred in the exami
ned rhizosphere fractions in smaller quantités (Table 4).
The rhizobacteria isolated in younger growth stages of winter wheat indicated,
more often, Gram-negative reaction (e. g. Erwinia, Pseudomonas, Xanthomonas,
Flexibacter, Klebsiella), but at ripeness stage the contribution of Gram-positive
bacteria distinctly increased (e. g. Coryneform bacteria, Bacillus). Similar results
were obtained by Miller et al. [21, 22] and by Turner et al. [28].
It is worth to add, that at all exam ined wheat growth stages, the share number
o f motile bacteria gradually increased from 24-56% (average 42%) in the first
rhizosphere fraction (soil adherent to roots) to 67-94% (average 81%) in the
fourth fraction (endorhizosphere).
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52
J. Kobus, J. Czaban, Л. Ga/Wa, Z). Ma siak, A. Księżni а к
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Wheat rhizosphere micro flor a .
53
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i n f lu e n c e o f p la n ts . T ra n s . X III C o n g re s s Int. S o c. Soil S e i., 13-20 A u g u s t, H a m b u rg , II: 6 3 2-653.
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c h a r a c te r iz a tio n o f flu o re s c e n / P seu d o m o n a s a s so c ia te d w ith th e ro o ts o f r ic e an d b a n a n a g ro w n in S ri L a n k a . P la n t a n d S o il. 145: 51-63. J . K o b u s , J . C z a b a n , A . G a jd a , D . M a s ia k , A . K s ię ż n ia k M I K R O F L O R A R Y Z O S F E R Y P S Z E N I C Y I J E J W P Ł Y W N A O D Ż Y W I A N I E R O Ś L I N I N I E K T Ó R E G R Z Y B Y P A T O G E N I C Z N E . C Z . I Z M I A N Y W P O P U L A C J I B A K T E R I I W R Y Z O S F E R Z E P S Z E N I C Y O Z I M E J Z a k ła d M ik ro b io lo g ii R o ln ic z e j In sty tu t U p ra w y i N a w o ż e n ia G le b y w P u ła w a c h S T R E S Z C Z E N I E
C e le m p ra c y b y ło ilo ś c io w e i ja k o ś c io w e p o z n a n ie p o p u la c ji b ak terii w ry z o s f e r z e p s z e n ic y o z im e j w r ó ż n y c h fa z a c h je j ro z w o ju , w u p ra w ie p o lo w e j na g le b ie b ru n a tn e j w y tw o rz o n e j z le ssu . B a d a n o n a s tę p u ją c e f ra k c je ry z o s fe ry : 1) g le b ę p rz y le g a ją c ą d o k o rz e n i, 2) p o w ie rz c h n ię k o rz e n i ( ry z o p la n a ), 3 )h o m o g e n a t k o rz e n i n ie s te ry liz o w a n y c h (c a łk o w ita e n d o ry z o s fe ra + n ie z n a n a p o z o s ta ło ś ć ry z o p la n y ), 4) h o m o g e n a t k o rz e n i ste ry liz o w a n y c h p o w ie rz c h n io w o (e n d o ry z o s fe ra lu b je j c z ę ś ć ). P o p u la c je b a d a n y c h b a k te rii z m ie n ia ły się w a n a liz o w a n y c h fa z a c h ro z w o ju r o ś lin ,o s ią g a ją c m a k s y m a ln e w a rto ś c i w fa z ie d o jrz a ło śc i. L ic z e b n o śc i b ak terii w 1 g s . m . g le b y lu b l g s . m . k o rz e n i b y ły z b liż o n e i w a h a ły się w g r a n ic a c h 2 -3 x 10°, je d n a k ż e z p o w o d u z n a c z n ie w ię k s z e g o u d z ia łu m a s y g le b y n iż m a s y k o rz e n i w b a d a n y c h p ró b k a c h r y z o s lc ry , 8 1 -9 6 % ty c h d r o b n o u s tr o jó w w y s tę p o w a ło w e fra k c ji 1. B a k te rie z n a le z io n e w e n d o r y z o s fe rz e (fra k c ja 4) s ta n o w iły ty lk o n ie w ie lk i u ła m e k ( 0 ,0 0 7 -1 ,5 % ) p o p u la c ji d ro b n o u s tro jó w ry z o s fe ry . W ię k s z o ś ć w y iz o lo w a n y c h s z c z e p ó w b a k te rii n a le ż a ła d o ro d z a jó w : P seudom onas, E rw inia i F lexib a cter o ra z d o g ru p y
C o tyn e fo rm . N a o g ó ł f lu o ry z u ją c e b a k te rie z ro d z a ju P seu d o m o n a s, ja k ró w n ie ż E rw in ia s p p ., p r z e w a ż a ły lic z e b n ie na k o rz e n ia c h i w ich w n ę trz u w m ło d sz y c h fa z a c h ro z w o ju p s z e n ic y , n a to m ia s t
F le xib a c te r s p p . b y ł s to s u n k o w o lic z n y w fa z ie c z w a rte g o liśc ia i k w itn ie n ia . B a k te rie z g ru p y
C o tyn e fo rm s ta n o w iły g łó w n ą p o p u la c ję w fa z ie d o jrz a ło śc i p sz e n ic y .
P r o f dr. J ó z e f K obus Praca wpłynęła do redakcji w listopadzie 1992 r. Zakład M ikrobiologii Rolniczej
1UNG w Puław ach
