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Uptake and Partitioning of Nitrogen by Maize Infected withStriga hermonthica
Annals of Botany 81 : 287–294, 1998
Uptake and Partitioning of Nitrogen by Maize Infected with Striga hermonthica G. K. S. A F L A K P UI*†, P. J. G R E G O RY* and R. J. F R O U D-W I L L I A M S‡ * Department of Soil Science, The Uniersity of Reading, P.O. Box 233, Whiteknights, Reading, RG6 6DW and ‡ Department of Agricultural Botany, The Uniersity of Reading, 2 Earley Gate, Reading, RG6 6AU Received : 12 May 1997
Returned for revision : 7 August 1997
Accepted : 13 October 1997
The uptake and partitioning of nitrogen (N) by maize infected with the parasitic angiosperm, Striga hermonthica was investigated in sand culture in a glasshouse. The purpose was to determine the effect of Striga on N uptake and partitioning in maize. Maize was grown at 22, 66 and 133 mg N per plant and sampled five times. There was no significant Striga¬N interaction in any measured response. Leaf dry matter of Striga-infected maize, averaged over all N treatments, was 92 % that of uninfected maize at the four-leaf stage but by the 18-leaf stage it had decreased to 58 %. Similarly, stem dry matter of infected maize which was 91 % that of uninfected maize at the four-leaf stage was only 42 % at the 18-leaf stage. Root dry matter was similar for infected and uninfected maize. N concentration in the leaf, stem and root declined asymptotically from the first to the last sampling date for both infected and uninfected maize. The asymptotic value of N concentration in Striga-infected maize was 16 % greater in the leaf, 55 % in the stem, and 21 % in the root than in uninfected maize. The concentration of N in Striga was higher than in maize at the 16- and 18-leaf stages. Uptake of N was similar for infected and uninfected plants at the four–eight leaf stage but at the eight–12 leaf stage, N uptake by infected maize was 52 % that of uninfected maize. However, the proportion of total plant nitrogen partitioned to the root was greater (P ! 0±001) for Striga-infected maize. These results showed that the extent to which S. hermonthica reduced maize growth and N uptake, but increased the proportion of N partitioned to the roots, did not depend on the rate of N fertilizer applied. # 1998 Annals of Botany Company Key words : Maize, nitrogen, partitioning, Striga hermonthica, uptake.
INTRODUCTION Striga hermonthica (Del.) Benth. (Scrophulariaceae) is an angiosperm root hemiparasite of the C crops, maize, % sorghum, millet and the C crop, rice, in the semi-arid $ tropics. Striga species mainly thrive in soils of low fertility. Field and laboratory studies on the effect of nitrogen on the infestation levels of Striga are inconclusive. In field studies, Agabawi and Younis (1965), Bebawi (1981) and Farina, Thomas and Channon (1985) reported that increasing the supply of nitrogen fertilizer reduced the infection of Striga and increased host yield. Similarly, the addition of nitrogen fertilizers reduced Striga emergence on fertile soils but increased emergence on infertile soils (Doggett, 1988). In other studies, high concentrations of nitrogen in the soil enhanced the growth of both the host and parasite (Egley, 1971 ; Parker, 1984 ; Cechin and Press, 1994). Raju et al. (1990) observed that, in pot experiments, increased soil N reduced the infestation of Striga asiatica and increased shoot dry matter of sorghum. Cechin and Press (1993) showed that biomass of infected sorghum plants grown at 0±5, 1 and 2 mol N m−$ was reduced by 22, 30 and 66 %, respectively, compared to uninfected sorghum plants after 140 d. At 3 and 4 mol N m−$, however, there was little difference in biomass of infected and uninfected sorghum plants. A recent field study by Gurney, Press and Ransom † For correspondence. Fax 44 (0) 1734 316557, e-mail G.K.S.Aflakpui!reading.ac.uk
0305-7364}98}02028708 $25.00}0
(1995) indicated that nitrogen fertilizer neither affected cereal growth nor photosynthesis, nor did it influence the response of maize and sorghum to Striga. Earlier studies on Striga-infected crops have only reported foliar N concentration measured at specific times during the growth of host and parasite. Hibberd et al. (1996) reported that although the concentrations of nitrogen and phosphorus were smaller in leaves of infected plants compared to control plants, the differences were not significant. Cechin and Press (1993) observed that S. hermonthica infection of sorghum did not result in smaller foliar nitrogen concentrations, but reduced the total amount of N partitioned into leaves as a consequence of its effects on allometry. In the above studies, no information was provided on the nitrogen uptake and partitioning characteristics of the host plants. McCullough, Aguillera and Tollenaar (1994) in an investigation of N stress on N uptake in an old and new maize hybrid showed that the uptake of N, measured as the mean specific root N uptake per unit of root dry weight (SRNU), was greater at the four–eight leaf stage than at the eight–12 leaf stage. Similarly, SRNU was increased with increased rate of N supply at both growth stages in the old hybrid. They also reported that apart from the highest N supply, SRNU in the new hybrid supported the contention that N uptake capacity is improved as N supply diminished. McCullough et al. (1994) also showed that the proportion of N partitioned to the leaf (LNPC) increased with development and N supply, whilst partitioning to the root (RNPC) decreased with development and N supply. To explain the
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action of nitrogen in changing the response of host plants to Striga infestation, an understanding of the N uptake and N partitioning characteristics of host plants is required. The objective of this study was to determine the effect of nitrogen on the response of maize to Striga infection by investigating the uptake and partitioning of nitrogen by maize infected with Striga hermonthica. The hypothesis tested was that at low additions of N, a maize plant infected with S. hermonthica partitions a greater proportion of nitrogen to the roots (to support the requirements of Striga).
MATERIALS AND METHODS Experimental site The experiment was conducted in a glasshouse at the University of Reading (51°27« N, 00°56« W), UK between May and September 1995. Day and night temperatures in the glasshouse were maintained at 30}20 °C. The experimental design was a completely randomized 3 (N rates)¬2 (Striga infection) factorial, replicated four times.
Conditioning Striga seed Seed of S. hermonthica collected by Dr P. Y. K. Sallah on a maize host in 1993 at Nyankpala, Ghana was used. A 5 g portion of Striga seed was added to 1 kg of sand in a polythene bag and mixed thoroughly by shaking for 10 min. Acid-washed sand (100 g) was weighed into pots (7±5 cm diameter) and 5 g of the sand : seed mixture added (approx. 3500 Striga seeds per pot). Another 95 g sand was added to cover the Striga seed and 50 ml water added. The pots were covered with a black polythene sheet and placed in a seed propagator box at 30 °C for 2 weeks to condition the Striga seed. After 2 weeks, during which the pots were monitored daily to ensure that the sand was moist, the content of each pot was air dried, thoroughly mixed, and used to infect maize plants.
Measurements Plants were sampled at the 4, 8, 12, 16 and 18 leaf stages (12, 29, 61, 90 and 104 DAP). At each harvest, maize plants were divided into leaves, stem and root and dried at 80 °C to constant weight. The concentrations of N in the leaf, stem and root fractions were determined on finely ground portions with a mass spectrometer [Roboprep CN Biological Sample Converter (Europa Scientific, Crewe, UK)]. Additionally concentrations of N in the leaf and stem of Striga were determined at 90 and 104 DAP. Mean specific root N uptake of maize (SRNU, mg N g−" root d−") was calculated for the four–eight and eight–12 leaf stages using the formula (McCullough et al., 1994) : SRNU ¯ (N ®N )}(t ®t )¬(ln(RW }RW )}(RW ®RW ) # " # " # " # " (1) where N , N , RW and RW are total N contents and root " # " # weights at times t and t , respectively. The mean leaf, stem " # and root N partitioning coefficients (LNPC, SNPC and RNPC) were calculated as the ratio of the N accumulation of the particular plant part to the whole plant N uptake.
Statistical analysis All data were subjected to analysis of variance and the nitrogen effect on all parameters partitioned into linear and quadratic components using orthogonal polynomials with SAS (GLM Procedure). The concentration of N over the five sampling times was further analysed to describe the asymptotic exponential curves (SAS NLIN Procedure). The general form of equation used was N ¯ AijBij exp[®kij(t®12)]
where Aij is the asymptotic value ; Bij, the difference between the maximum N concentration value and the asymptotic value ; kij, the shape (curvature) parameter ; t, time of sampling in days and 12, the number of days from planting to first sampling. RESULTS
Growing the host crop The content of each 7±5 cm pot (200 g sand : seed mixture) was added to 1±3 kg washed river sand in 20 cm diameter pots and covered with 500 g sand to give a total of 2 kg sand per pot. Seed of maize (Zea mays L. cv. Okomasa) was surface sterilized with 1 % sodium hypochlorite, washed with water and planted at a depth of about 2±5 cm. Two seeds were sown in each pot and subsequently thinned to one after expansion of the first leaf. At the same time, seeds were also planted in 2 kg sand uninfected with Striga. Plants were watered with 200 ml full strength, nitrogen-free Long Ashton nutrient solution three times a week ; on other days the plants were watered with tap water. Nitrogen was applied at 22±2, 66±6 and 133±2 mg per plant (equivalent to 20, 60, 120 kg N ha−") as NH NO dissolved in water at the % $ three leaf stage (9 d after planting, DAP). The rates of N supply were chosen for their agronomic relevance.
(2)
There was no significant Striga¬N interaction in any measured response. Consequently, only the main effects of Striga and N are presented.
Maize growth Figure 1 shows that dry matter of S. hermonthica-infected maize, averaged across all N rates, was smaller compared to uninfected controls. S. hermonthica reduced leaf dry matter of maize at all sampling times (P ! 0±001) (Fig. 1 A). The leaf dry matter of infected plants ranged from 92 % of that of uninfected plants at the four-leaf stage (12 DAP) to 57 % at the 18-leaf stage (104 DAP). Dry matter of the stem was similar for infected and uninfected maize at the four-leaf stage, but at subsequent harvests stem dry matter of infected maize varied from 79 % (P ! 0±001) of that of uninfected
Aflakpui et al.—Nitrogen Uptake by Striga-infected Maize 15
15 B
Stem d. wt per plant (g)
A
Leaf d. wt per plant (g)
289
10
5
0
20
40 60 80 Days after planting (DAP)
100
120
10
5
0
20
40 60 80 Days after planting (DAP)
100
120
F. 1. Effect of Striga hermonthica infection on leaf (A) and stem (B) dry matter of maize. Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times. Some s.e. bars are smaller than the symbols. E, Infected ; D, uninfected. 20
20 A
B 16 Root d. wt per plant (g)
Leaf d. wt per plant (g)
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12
8
8
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4
0
12
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40 60 80 Days after planting (DAP)
100
120
0
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40 60 80 Days after planting (DAP)
100
120
F. 2. Effect of the rate of nitrogen fertilizer on leaf (A) and root (B) dry matter of maize. Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times. Some s.e. bars are smaller than the symbols. ^, 20 kg N ha−" ; D, 60 kg N ha−" ; _, 120 kg N ha−".
maize at the eight-leaf stage to 42 % (P ! 0±001) at the 18leaf stage (Fig. 1 B). However, S. hermonthica did not affect the root dry matter of maize at any sampling time (data not shown). The application of nitrogen increased leaf (Fig. 2 A) and root (Fig. 2 B) dry matter, averaged across Striga infection levels, at all sampling times (P ! 0±001). Data for stems are not shown because they showed a similar pattern to that of the leaf. N concentration in maize and Striga The concentration of N in the leaf, stem and root of both infected and uninfected maize declined asymptotically from the first to the last sampling date. Generally, N concentration in the Striga-infected maize was higher than in the uninfected
maize. Figure 3 A shows the concentration of N in the root of maize plants over the five sampling times. The curves for the stem and leaf are not shown because they were similar in shape to that of the root. The asymptotic value of N concentration in the leaf was about 16 % greater (P ! 0±05) in Striga-infected maize than in the uninfected maize (Table 1) ; for stems it was 55 % and for roots 21 %. Striga infection affected neither Bij (the difference between the maximum N concentration value and the asymptotic value) nor kij (the shape parameter) in all plant parts of maize (Table 1). However, Bij increased with increased N application whilst Aij and kij decreased. The concentration of nitrogen in the leaf, stem and root of maize, averaged across Striga infection levels, increased with increased N application (P ! 0±001) at the four- and
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60 A
B 50 N concentration (mg g–1)
N concentration (mg g–1)
16
12
8
4
0
40
30
20
10
20
40 60 80 Days after planting (DAP)
100
0
120
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40 60 80 Days after planting (DAP)
100
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F. 3. A, Effect of Striga hermonthica infection on root nitrogen concentration of maize. E, Infected ; D, uninfected. B, Effect of the rate of nitrogen fertilizer on leaf nitrogen concentration of maize. ^, 20 kg N ha−" ; D, 60 kg N ha−" ; _, 120 kg N ha−". Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times. Some s.e. bars are smaller than the symbols.
T 1. Parameters (asymptotic N concentration, Aij ; difference between asymptotic N and highest N, Bij ; and shape, kij) describing nitrogen concentrations in maize grown at three rates of N and infected with Striga hermonthica N rate (kg ha−")
Infected
Uninfected
Leaf N 20 60 120 95 % CI* Stem N 20 60 120 95 % CI Root N 20 60 120 95 % CI
Aij 8±21 7±10 7±03 5±59–8±82
Bij 26±44 36±62 47±17 22±6–57±4
kij ®0±096 ®0±061 ®0±052 ®0±10–0±11
Aij 7±15 6±04 5±97 5±59–8±82
Bij 26±44 34±62 47±17 22±6–57±4
kij ®0±096 ®0±061 ®0±052 ®0±10–0±11
Aij 3±13 3±13 2±56 1±36–3±68
Bij 30±12 32±08 43±69 25±7–57±4
kij ®0±109 ®0±109 ®0±061 ®0±11–0±13
Aij 2±09 2±09 1±52 1±36–3±68
Bij 30±12 32±08 47±17 25±7–57±4
kij ®0±071 ®0±071 ®0±055 ®0±11–0±13
Aij 4±80 4±80 2±76 0±69–6±41
Bij 9±86 12±86 17±31 6±76–19±7
kij ®0±054 ®0±054 ®0±029 ®0±06–0±09
Aij 4±08 4±08 2±04 0±69–6±41
Bij 9±86 11±04 17±31 6±76–19±7
kij ®0±054 ®0±054 ®0±029 ®0±06–0±09
*, 95 % confidence interval for values in each column. Data are means of four replicates.
eight-leaf stages (Fig. 3 B). By the 12- to 18-leaf stages, nitrogen concentrations in all plant parts were similar for all three nitrogen rates. Figure 3 B shows the relationship between concentration of N in the leaf with time for the different nitrogen rates. Data for stem and root are not shown because they were similar in pattern to the leaf N concentration. Table 2 shows the effect of N application rate on N concentration in Striga 90 and 104 d after planting maize (about 50 and 64 d after emergence of Striga shoots). The rate of N applied did not affect N concentration in either the stem or leaf of Striga. There was, however, a slight decrease in N concentration in the leaf with time and an increase in
the stem. The N concentration in Striga at these times was greater than that in both infected and uninfected maize. Total plant N content in maize and Striga Table 3 shows the effect of N application rate on total N content of maize and Striga 90 and 104 DAP. In maize, total N content increased with increased N rate but it decreased in Striga because of the relatively greater dry weight at lower N. The total N content of Striga varied from 20 % that of maize at 20 kg N to 3 % at 120 kg N at 90 DAP, and from 30 to 6 % at 104 DAP. Total N content in both Striga and maize increased with time at all N rates
Aflakpui et al.—Nitrogen Uptake by Striga-infected Maize T 2. Effect of N application on N concentration of S. hermonthica infecting maize grown in sand culture at 90 and 104 d after planting (DAP) maize 90 DAP
104 DAP
Leaf Stem Leaf Stem Concentration of nitrogen (mg g−") Nitrogen (kg ha−") 20 60 120 s.e. Contrasts Linear Quadratic
22±5 23±1 25±1 1±48
14±5 10±5 9±6 2±29
19±2 19±6 20±4 1±31
12±7 11±9 11±5 1±06
n.s. n.s.
n.s. n.s.
n.s. n.s.
n.s. n.s.
Data are means of four replicates. s.e. is for means in each column ; n.s., contrasts for means in each column not significant.
T 3. Effect of N application rate on total plant N content of maize and S. hermonthica infecting maize grown in sand culture at 90 and 104 d after planting (DAP) maize 90 DAP Maize mg per plant Nitrogen (kg ha−") 20 60 120 s.e. Contrasts Linear Quadratic
104 DAP
Striga Maize Nitrogen content mg per mg per pot plant
Striga mg per pot
54±3 114±8 212±2 19±79
11±0 9±1 6±9 0±52
64±3 143±0 196±9 16±53
19±4 12±8 12±0 1±11
** n.s.
n.s. n.s.
** n.s.
n.s. n.s.
Data are means of four replicates. s.e. is for means in each column ; **, contrasts for means in each column differ at P ! 0±01 ; n.s., not significant.
except for maize at 120 kg N because of a reduced concentration of N in maize root at 104 DAP. N uptake and partitioning The mean specific root N uptake (SRNU) was not affected by Striga at the four–eight leaf stage. By the eight–12 leaf stage however, Striga reduced (P ! 0±001) SRNU from 0±485 to 0±254 mg g−" root d−" (Fig. 4 A). At the four–eight leaf stage, SRNU increased (P ! 0±001) as N supply was increased, but at the eight–12 leaf stage the reverse was observed as SRNU declined (P ! 0±05) with increased N application (Fig. 4 B). There was no significant Striga¬N interaction on SRNU at both growth stages. The partitioning of N to the leaf (LNPC) (Fig. 5 A) was greater (P ! 0±01) for infected maize than for uninfected maize at the four–eight leaf stage but at the eight–12 leaf
291
stage LNPC was unaffected by Striga infection. The proportion of total N partitioned to the stem (SNPC) was neither affected by Striga infection nor N fertilizer application at any growth stage (data not shown). Although the proportion of total N partitioned to the root (RNPC) was greater for infected maize than uninfected maize at the four–eight leaf stage, the difference was not signifcant (Fig. 5 B). At the eight–12 leaf stage, however, RNPC was greater (P ! 0±001) for infected maize than for uninfected maize. The rate of N applied did not affect RNPC at the four–eight leaf stage (Fig. 5 C) but RNPC increased (P ! 0±01) with increased N application at the eight–12 leaf stage. There was no effect of N application rate on LNPC at the four–eight leaf stage but LNPC declined with increased N application at the eight–12 leaf stage (data not shown). DISCUSSION Striga hermonthica reduced leaf and stem dry matter of its maize host but did not affect root dry matter. The reduced maize growth caused by S. hermonthica was not entirely alleviated by N fertilizer at the rates applied in this experiment. This result contrasts with the observation by Cechin and Press (1993) that the extent to which the parasite influenced host performance depended critically on the concentration of nitrogen supplied to the plants ; large differences in performance resulted from small differences in nitrogen supply. The non-significant Striga¬N interaction observed in this study compared with the significant interaction reported by Cechin and Press (1993) might be attributed to the higher levels of N applied by Cechin and Press. The highest rates of N applied in this study (60, 120 kg N) are only equivalent to the two lower levels used by Cechin and Press. The concentration of N in the leaf, stem and root of both infected and uninfected maize declined asymptotically from the first to the last sampling date. The asymptotic values of N were greater in all parts of Striga-infected maize than in uninfected plants. Though there are no values of tissue nitrogen concentration with time for similar studies of Striga-infected host crops for comparison, the general trend in N concentration in dry matter with time is similar to that reported by Greenwood et al. (1991) and Gregory, Crawford and McGowan (1979). The differences in the results of Cechin and Press (1993) and Hibberd et al. (1996) on the one hand and the results of this study on the other, might be a consequence of analysing foliar nutrient concentration at a particular time during growth but not at different periods of growth. However, a recent study by Frost et al. (1997) showed that the concentration of nitrogen in Striga-infected sorghum measured at a single time during growth was greater than that in control plants. The concentrations of nitrogen in the leaf and stem of Striga were greater than that in maize at 90 and 104 DAP ; a time at which N concentrations in both infected and uninfected maize were in the deficiency range. There was, however, no effect of applied nitrogen on N concentrations in Striga. The non-significant effect of N rate on Striga N concentration contrasts with the results of Cechin and Press (1993) who found not only higher leaf N concentrations in
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10 A
B 8 N uptake (mg N g–1 root d–1)
N uptake (mg N g–1 root d–1)
5
4
3
2
1
0
4–8 leaf 8–12 leaf Growth stage of maize
6
4
2
0
8–12 leaf 4–8 leaf Growth stage of maize
F. 4. A, Effect of Striga hermonthica infection on the mean specific nitrogen uptake by maize. +, Infected ; 8, uninfected. B, Effect of the rate of nitrogen fertilizer on the mean specific nitrogen uptake by maize. +, 20 kg N ha−" ; 8, 60 kg N ha−" ; *, 120 kg N ha−". Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times.
S. hermonthica than in sorghum, but also a greater increase in N concentration with increased rate of N in Striga than for sorghum. Total plant N content in maize was greater than that in Striga because of the very big differences in dry weight. Total dry weight in Striga ranged from 3 % that of maize at 20 kg N to 0±44 % at 120 kg N at 90 DAP, and from 5 to 0±77 % at 104 DAP. The data from this study indicated that SRNU was similar for infected and uninfected maize at the four–eight leaf stage, but at the eight–12 leaf stage SRNU by infected maize was only 52 % that of uninfected maize. During the early growth stages (four–eight leaf stage) N application increased SRNU. By the later growth stages (eight–12 leaf stage) however, increased N application resulted in reduced SRNU ; a result that is inconsistent with those of McCullough et al. (1994) for an old maize hybrid. McCullough et al. (1994) explained that SRNU as calculated in their study (and in this) cannot show whether the enhanced SRNU in the new hybrid was due to a greater proportion of the root mass that is actively taking N up or whether certain N uptake enzymes were more efficient. Robinson, Linehan and Caul (1991) have shown through calculations that the mean fractions of the root systems of wheat likely to be involved in nitrate uptake were 11 % of the measured total root length for 0 kg N ha−" compared with 3±5 % for 200 kg N ha−". All the nitrogen in this experiment was applied at the three leaf stage hence there was more N available to be taken up coupled with increasing crop growth rate at the early stages of growth. Mumera and Below (1993) and Yaduraju, Hosmani and Probhakara (1979) observed that repeated applications of N were more effective in depressing Striga performance and stimulating host growth than a single initial application. The rate of nitrogen applied did not affect the partitioning of N taken up at the early growth stages to any of the plant parts. At the later growth stages,
increased N supply increased N partitioning to the root (RNPC) and decreased the proportion partitioned to the leaf (LNPC) which contrasts with the results of McCullough et al. (1994). Conversely, Striga infection resulted in higher LNPC at the early growth stages but not at the later stages of growth. There was, however, higher RNPC due to Striga infection at the later stages of growth. The higher LNPC in Striga-infected maize at the early stages of growth might occur because of a reduced growth rate of infected maize leading to a smaller dry matter and consequently greater nitrogen concentration. McCullough et al. (1994) applied nitrogen throughout the duration of their experiment ; once daily from planting until the eight-leaf stage, and from the eight- to the 12-leaf stage nutrient solution was added to plastic saucers beneath the pots. The hypothesis tested in this study was that at low N rates, a maize plant infected with S. hermonthica partitions a greater proportion of nitrogen to the roots (to support the requirements of Striga). The data from the study did not establish any significant interaction between N fertilizer rate and Striga infection in any measured responses. However, we observed that the proportion of total plant N partitioned to the root of a maize plant was greater for Striga-infected plants than for uninfected plants. The mechanistic bases for this partitioning are unknown and need to be examined. In addition, the asymptotic concentration of N in infected plants (leaf, stem, root) was greater than in uninfected plants and the concentration of N in Striga was also greater than that in maize at 90 and 104 DAP. A C K N O W L E D G E M E N TS We thank Dr P. Y. K. Sallah for providing the Striga seed and Dr S. G. Gilmour for statistical help. G. K. S. Aflakpui thanks the Crops Research Institute of the Council for Scientific and Industrial Research, Ghana for study leave ;
Aflakpui et al.—Nitrogen Uptake by Striga-infected Maize 1.00
1.00 A
B
N partitioning coefficient
N partitioning coefficient
0.80
0.60
0.40
0.20
0.00
293
0.80
0.60
0.40
0.20
8–12 leaf 4–8 leaf Growth stage of maize
0.00
8–12 leaf 4–8 leaf Growth stage of maize
1.00
N partitioning coefficient
C 0.80
0.60
0.40
0.20
0.00
8–12 leaf 4–8 leaf Growth stage of maize
F. 5. Effect of Striga hermonthica infection on leaf (A) and root (B) nitrogen partitioning coefficient of maize. +, Infected ; 8, uninfected. C, Relationship between the rate of nitrogen fertilizer and root nitrogen partitioning coefficient. +, 20 kg N ha−" ; 8, 60 kg N ha−" ; *, 120 kg N ha−". Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times.
the Ghana-CIDA Grains Development Project and the University of Reading for financial support. LITERATURE CITED Agabawi KA, Younis AE. 1965. Effect of nitrogen application on growth and nitrogen content of Striga hermonthica Benth. and Sorghum ulgare Lur. grown for forage. Plant and Soil 23 : 295–304. Bebawi FF. 1981. Response of sorghum cultivars and Striga population to nitrogen fertilisation. Plant and Soil 59 : 261–267. Cechin I, Press MC. 1993. Nitrogen relations of the sorghum-Striga hermonthica host parasite association : growth and photosynthesis. Plant, Cell and Enironment 16 : 237–247. Cechin I, Press MC. 1994. Influence of nitrogen on growth and photosynthesis of a C cereal, Oryza satia, infected with the root $ hemiparasite Striga hermonthica. Journal of Experimental Botany 45 : 925–930.
Doggett H. 1988. Witchweed (Striga). In : Sorghum 2nd edn. Singapore : Longman Scientific and Technical, 368–404. Egley GH. 1971. Mineral nutrition and the parasite–host relationships of witchweed. Weed Science 19 : 528–533. Farina MPW, Thomas PEL, Channon P. 1985. Nitrogen, phosphorus and potassium effects on the incidence of Striga asiatica (L.) Kuntze in maize. Weed Research 25 : 443–447. Frost DL, Gurney AL, Press MC, Scholes JD. 1997. Striga hermonthica reduces photosynthesis in sorghum : the importance of stomatal limitations and a potential role for ABA ? Plant, Cell and Enironment 20 : 483–492. Greenwood DJ, Gastal F, Lemaire G, Draycot A, Millard P, Neeteson JJ. 1991. Growth rate and %N of field grown crops : Theory and experiments. Annals of Botany 67 : 181–190. Gregory PJ, Crawford DV, McGowan M. 1979. Nutrient relations of winter wheat. 1. Accumulation and distribution of Na, K, Ca, Mg, P, S and N. Journal of Agricultural Science, Cambridge 93 : 485–494. Gurney AL, Press MC, Ransom JK. 1995. The parasite angiosperm
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Striga hermonthica can reduce photosynthesis of its sorghum and maize hosts in the field. Journal of Experimental Botany 46 : 1817–1823. Hibberd JM, Quick WP, Press MC, Scholes DJ. 1996. The influence of the parasitic angiosperm Striga gesnerioides on the growth and photosynthesis of its host, Vigna unguiculata. Journal of Experimental Botany 47 : 507–512. McCullough DE, Aguillera A, Tollenaar M. 1994. N uptake, N partitioning and photosynthetic N-use efficiency of an old and a new maize hybrid. Canadian Journal of Plant Science 74 : 479–484. Mumera LM, Below FE. 1993. Role of nitrogen in resistance to Striga parasitism of maize. Crop Science 33 : 758–763. Parker C. 1984. The influence of Striga species on sorghum under varying nitrogen fertilisation. In : Parker C, Musselman LJ, Polhill
RM, Wilson AK, eds. Proceedings of the Third International Symposium on Parasitic Weeds. ICARDA}International Parasitic Seed Plant Research Group, 7–9 May, 1984, Aleppo, Syria, P.O. Box 5466, Aleppo, Syria, 90–98. Raju PS, Osman MA, Soman P, Peacock JM. 1990. Effects of N, P, and K on Striga asiatica (L.) Kuntze seed germination and infestation of sorghum. Weed Research 30 : 139–144. Robinson D, Linehan DJ, Caul S. 1991. What limits nitrate uptake from the soil ? Plant, Cell and Enironment 14 : 77–85. Yaduraju NT, Hosmani MM, Probhakara TK. 1979. Effect of time and dose of nitrogen applications on Striga asiatica on Sorghum. In : Musselman LJ, Worsham AD, Eplee RE. Proceedings of the Second International Symposium on Parasitic Weeds. Raleigh, NC, USA, 285–289.
Uptake and Partitioning of Nitrogen by Maize Infected with Striga hermonthica G. K. S. A F L A K P UI*†, P. J. G R E G O RY* and R. J. F R O U D-W I L L I A M S‡ * Department of Soil Science, The Uniersity of Reading, P.O. Box 233, Whiteknights, Reading, RG6 6DW and ‡ Department of Agricultural Botany, The Uniersity of Reading, 2 Earley Gate, Reading, RG6 6AU Received : 12 May 1997
Returned for revision : 7 August 1997
Accepted : 13 October 1997
The uptake and partitioning of nitrogen (N) by maize infected with the parasitic angiosperm, Striga hermonthica was investigated in sand culture in a glasshouse. The purpose was to determine the effect of Striga on N uptake and partitioning in maize. Maize was grown at 22, 66 and 133 mg N per plant and sampled five times. There was no significant Striga¬N interaction in any measured response. Leaf dry matter of Striga-infected maize, averaged over all N treatments, was 92 % that of uninfected maize at the four-leaf stage but by the 18-leaf stage it had decreased to 58 %. Similarly, stem dry matter of infected maize which was 91 % that of uninfected maize at the four-leaf stage was only 42 % at the 18-leaf stage. Root dry matter was similar for infected and uninfected maize. N concentration in the leaf, stem and root declined asymptotically from the first to the last sampling date for both infected and uninfected maize. The asymptotic value of N concentration in Striga-infected maize was 16 % greater in the leaf, 55 % in the stem, and 21 % in the root than in uninfected maize. The concentration of N in Striga was higher than in maize at the 16- and 18-leaf stages. Uptake of N was similar for infected and uninfected plants at the four–eight leaf stage but at the eight–12 leaf stage, N uptake by infected maize was 52 % that of uninfected maize. However, the proportion of total plant nitrogen partitioned to the root was greater (P ! 0±001) for Striga-infected maize. These results showed that the extent to which S. hermonthica reduced maize growth and N uptake, but increased the proportion of N partitioned to the roots, did not depend on the rate of N fertilizer applied. # 1998 Annals of Botany Company Key words : Maize, nitrogen, partitioning, Striga hermonthica, uptake.
INTRODUCTION Striga hermonthica (Del.) Benth. (Scrophulariaceae) is an angiosperm root hemiparasite of the C crops, maize, % sorghum, millet and the C crop, rice, in the semi-arid $ tropics. Striga species mainly thrive in soils of low fertility. Field and laboratory studies on the effect of nitrogen on the infestation levels of Striga are inconclusive. In field studies, Agabawi and Younis (1965), Bebawi (1981) and Farina, Thomas and Channon (1985) reported that increasing the supply of nitrogen fertilizer reduced the infection of Striga and increased host yield. Similarly, the addition of nitrogen fertilizers reduced Striga emergence on fertile soils but increased emergence on infertile soils (Doggett, 1988). In other studies, high concentrations of nitrogen in the soil enhanced the growth of both the host and parasite (Egley, 1971 ; Parker, 1984 ; Cechin and Press, 1994). Raju et al. (1990) observed that, in pot experiments, increased soil N reduced the infestation of Striga asiatica and increased shoot dry matter of sorghum. Cechin and Press (1993) showed that biomass of infected sorghum plants grown at 0±5, 1 and 2 mol N m−$ was reduced by 22, 30 and 66 %, respectively, compared to uninfected sorghum plants after 140 d. At 3 and 4 mol N m−$, however, there was little difference in biomass of infected and uninfected sorghum plants. A recent field study by Gurney, Press and Ransom † For correspondence. Fax 44 (0) 1734 316557, e-mail G.K.S.Aflakpui!reading.ac.uk
0305-7364}98}02028708 $25.00}0
(1995) indicated that nitrogen fertilizer neither affected cereal growth nor photosynthesis, nor did it influence the response of maize and sorghum to Striga. Earlier studies on Striga-infected crops have only reported foliar N concentration measured at specific times during the growth of host and parasite. Hibberd et al. (1996) reported that although the concentrations of nitrogen and phosphorus were smaller in leaves of infected plants compared to control plants, the differences were not significant. Cechin and Press (1993) observed that S. hermonthica infection of sorghum did not result in smaller foliar nitrogen concentrations, but reduced the total amount of N partitioned into leaves as a consequence of its effects on allometry. In the above studies, no information was provided on the nitrogen uptake and partitioning characteristics of the host plants. McCullough, Aguillera and Tollenaar (1994) in an investigation of N stress on N uptake in an old and new maize hybrid showed that the uptake of N, measured as the mean specific root N uptake per unit of root dry weight (SRNU), was greater at the four–eight leaf stage than at the eight–12 leaf stage. Similarly, SRNU was increased with increased rate of N supply at both growth stages in the old hybrid. They also reported that apart from the highest N supply, SRNU in the new hybrid supported the contention that N uptake capacity is improved as N supply diminished. McCullough et al. (1994) also showed that the proportion of N partitioned to the leaf (LNPC) increased with development and N supply, whilst partitioning to the root (RNPC) decreased with development and N supply. To explain the
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action of nitrogen in changing the response of host plants to Striga infestation, an understanding of the N uptake and N partitioning characteristics of host plants is required. The objective of this study was to determine the effect of nitrogen on the response of maize to Striga infection by investigating the uptake and partitioning of nitrogen by maize infected with Striga hermonthica. The hypothesis tested was that at low additions of N, a maize plant infected with S. hermonthica partitions a greater proportion of nitrogen to the roots (to support the requirements of Striga).
MATERIALS AND METHODS Experimental site The experiment was conducted in a glasshouse at the University of Reading (51°27« N, 00°56« W), UK between May and September 1995. Day and night temperatures in the glasshouse were maintained at 30}20 °C. The experimental design was a completely randomized 3 (N rates)¬2 (Striga infection) factorial, replicated four times.
Conditioning Striga seed Seed of S. hermonthica collected by Dr P. Y. K. Sallah on a maize host in 1993 at Nyankpala, Ghana was used. A 5 g portion of Striga seed was added to 1 kg of sand in a polythene bag and mixed thoroughly by shaking for 10 min. Acid-washed sand (100 g) was weighed into pots (7±5 cm diameter) and 5 g of the sand : seed mixture added (approx. 3500 Striga seeds per pot). Another 95 g sand was added to cover the Striga seed and 50 ml water added. The pots were covered with a black polythene sheet and placed in a seed propagator box at 30 °C for 2 weeks to condition the Striga seed. After 2 weeks, during which the pots were monitored daily to ensure that the sand was moist, the content of each pot was air dried, thoroughly mixed, and used to infect maize plants.
Measurements Plants were sampled at the 4, 8, 12, 16 and 18 leaf stages (12, 29, 61, 90 and 104 DAP). At each harvest, maize plants were divided into leaves, stem and root and dried at 80 °C to constant weight. The concentrations of N in the leaf, stem and root fractions were determined on finely ground portions with a mass spectrometer [Roboprep CN Biological Sample Converter (Europa Scientific, Crewe, UK)]. Additionally concentrations of N in the leaf and stem of Striga were determined at 90 and 104 DAP. Mean specific root N uptake of maize (SRNU, mg N g−" root d−") was calculated for the four–eight and eight–12 leaf stages using the formula (McCullough et al., 1994) : SRNU ¯ (N ®N )}(t ®t )¬(ln(RW }RW )}(RW ®RW ) # " # " # " # " (1) where N , N , RW and RW are total N contents and root " # " # weights at times t and t , respectively. The mean leaf, stem " # and root N partitioning coefficients (LNPC, SNPC and RNPC) were calculated as the ratio of the N accumulation of the particular plant part to the whole plant N uptake.
Statistical analysis All data were subjected to analysis of variance and the nitrogen effect on all parameters partitioned into linear and quadratic components using orthogonal polynomials with SAS (GLM Procedure). The concentration of N over the five sampling times was further analysed to describe the asymptotic exponential curves (SAS NLIN Procedure). The general form of equation used was N ¯ AijBij exp[®kij(t®12)]
where Aij is the asymptotic value ; Bij, the difference between the maximum N concentration value and the asymptotic value ; kij, the shape (curvature) parameter ; t, time of sampling in days and 12, the number of days from planting to first sampling. RESULTS
Growing the host crop The content of each 7±5 cm pot (200 g sand : seed mixture) was added to 1±3 kg washed river sand in 20 cm diameter pots and covered with 500 g sand to give a total of 2 kg sand per pot. Seed of maize (Zea mays L. cv. Okomasa) was surface sterilized with 1 % sodium hypochlorite, washed with water and planted at a depth of about 2±5 cm. Two seeds were sown in each pot and subsequently thinned to one after expansion of the first leaf. At the same time, seeds were also planted in 2 kg sand uninfected with Striga. Plants were watered with 200 ml full strength, nitrogen-free Long Ashton nutrient solution three times a week ; on other days the plants were watered with tap water. Nitrogen was applied at 22±2, 66±6 and 133±2 mg per plant (equivalent to 20, 60, 120 kg N ha−") as NH NO dissolved in water at the % $ three leaf stage (9 d after planting, DAP). The rates of N supply were chosen for their agronomic relevance.
(2)
There was no significant Striga¬N interaction in any measured response. Consequently, only the main effects of Striga and N are presented.
Maize growth Figure 1 shows that dry matter of S. hermonthica-infected maize, averaged across all N rates, was smaller compared to uninfected controls. S. hermonthica reduced leaf dry matter of maize at all sampling times (P ! 0±001) (Fig. 1 A). The leaf dry matter of infected plants ranged from 92 % of that of uninfected plants at the four-leaf stage (12 DAP) to 57 % at the 18-leaf stage (104 DAP). Dry matter of the stem was similar for infected and uninfected maize at the four-leaf stage, but at subsequent harvests stem dry matter of infected maize varied from 79 % (P ! 0±001) of that of uninfected
Aflakpui et al.—Nitrogen Uptake by Striga-infected Maize 15
15 B
Stem d. wt per plant (g)
A
Leaf d. wt per plant (g)
289
10
5
0
20
40 60 80 Days after planting (DAP)
100
120
10
5
0
20
40 60 80 Days after planting (DAP)
100
120
F. 1. Effect of Striga hermonthica infection on leaf (A) and stem (B) dry matter of maize. Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times. Some s.e. bars are smaller than the symbols. E, Infected ; D, uninfected. 20
20 A
B 16 Root d. wt per plant (g)
Leaf d. wt per plant (g)
16
12
8
8
4
4
0
12
20
40 60 80 Days after planting (DAP)
100
120
0
20
40 60 80 Days after planting (DAP)
100
120
F. 2. Effect of the rate of nitrogen fertilizer on leaf (A) and root (B) dry matter of maize. Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times. Some s.e. bars are smaller than the symbols. ^, 20 kg N ha−" ; D, 60 kg N ha−" ; _, 120 kg N ha−".
maize at the eight-leaf stage to 42 % (P ! 0±001) at the 18leaf stage (Fig. 1 B). However, S. hermonthica did not affect the root dry matter of maize at any sampling time (data not shown). The application of nitrogen increased leaf (Fig. 2 A) and root (Fig. 2 B) dry matter, averaged across Striga infection levels, at all sampling times (P ! 0±001). Data for stems are not shown because they showed a similar pattern to that of the leaf. N concentration in maize and Striga The concentration of N in the leaf, stem and root of both infected and uninfected maize declined asymptotically from the first to the last sampling date. Generally, N concentration in the Striga-infected maize was higher than in the uninfected
maize. Figure 3 A shows the concentration of N in the root of maize plants over the five sampling times. The curves for the stem and leaf are not shown because they were similar in shape to that of the root. The asymptotic value of N concentration in the leaf was about 16 % greater (P ! 0±05) in Striga-infected maize than in the uninfected maize (Table 1) ; for stems it was 55 % and for roots 21 %. Striga infection affected neither Bij (the difference between the maximum N concentration value and the asymptotic value) nor kij (the shape parameter) in all plant parts of maize (Table 1). However, Bij increased with increased N application whilst Aij and kij decreased. The concentration of nitrogen in the leaf, stem and root of maize, averaged across Striga infection levels, increased with increased N application (P ! 0±001) at the four- and
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60 A
B 50 N concentration (mg g–1)
N concentration (mg g–1)
16
12
8
4
0
40
30
20
10
20
40 60 80 Days after planting (DAP)
100
0
120
20
40 60 80 Days after planting (DAP)
100
120
F. 3. A, Effect of Striga hermonthica infection on root nitrogen concentration of maize. E, Infected ; D, uninfected. B, Effect of the rate of nitrogen fertilizer on leaf nitrogen concentration of maize. ^, 20 kg N ha−" ; D, 60 kg N ha−" ; _, 120 kg N ha−". Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times. Some s.e. bars are smaller than the symbols.
T 1. Parameters (asymptotic N concentration, Aij ; difference between asymptotic N and highest N, Bij ; and shape, kij) describing nitrogen concentrations in maize grown at three rates of N and infected with Striga hermonthica N rate (kg ha−")
Infected
Uninfected
Leaf N 20 60 120 95 % CI* Stem N 20 60 120 95 % CI Root N 20 60 120 95 % CI
Aij 8±21 7±10 7±03 5±59–8±82
Bij 26±44 36±62 47±17 22±6–57±4
kij ®0±096 ®0±061 ®0±052 ®0±10–0±11
Aij 7±15 6±04 5±97 5±59–8±82
Bij 26±44 34±62 47±17 22±6–57±4
kij ®0±096 ®0±061 ®0±052 ®0±10–0±11
Aij 3±13 3±13 2±56 1±36–3±68
Bij 30±12 32±08 43±69 25±7–57±4
kij ®0±109 ®0±109 ®0±061 ®0±11–0±13
Aij 2±09 2±09 1±52 1±36–3±68
Bij 30±12 32±08 47±17 25±7–57±4
kij ®0±071 ®0±071 ®0±055 ®0±11–0±13
Aij 4±80 4±80 2±76 0±69–6±41
Bij 9±86 12±86 17±31 6±76–19±7
kij ®0±054 ®0±054 ®0±029 ®0±06–0±09
Aij 4±08 4±08 2±04 0±69–6±41
Bij 9±86 11±04 17±31 6±76–19±7
kij ®0±054 ®0±054 ®0±029 ®0±06–0±09
*, 95 % confidence interval for values in each column. Data are means of four replicates.
eight-leaf stages (Fig. 3 B). By the 12- to 18-leaf stages, nitrogen concentrations in all plant parts were similar for all three nitrogen rates. Figure 3 B shows the relationship between concentration of N in the leaf with time for the different nitrogen rates. Data for stem and root are not shown because they were similar in pattern to the leaf N concentration. Table 2 shows the effect of N application rate on N concentration in Striga 90 and 104 d after planting maize (about 50 and 64 d after emergence of Striga shoots). The rate of N applied did not affect N concentration in either the stem or leaf of Striga. There was, however, a slight decrease in N concentration in the leaf with time and an increase in
the stem. The N concentration in Striga at these times was greater than that in both infected and uninfected maize. Total plant N content in maize and Striga Table 3 shows the effect of N application rate on total N content of maize and Striga 90 and 104 DAP. In maize, total N content increased with increased N rate but it decreased in Striga because of the relatively greater dry weight at lower N. The total N content of Striga varied from 20 % that of maize at 20 kg N to 3 % at 120 kg N at 90 DAP, and from 30 to 6 % at 104 DAP. Total N content in both Striga and maize increased with time at all N rates
Aflakpui et al.—Nitrogen Uptake by Striga-infected Maize T 2. Effect of N application on N concentration of S. hermonthica infecting maize grown in sand culture at 90 and 104 d after planting (DAP) maize 90 DAP
104 DAP
Leaf Stem Leaf Stem Concentration of nitrogen (mg g−") Nitrogen (kg ha−") 20 60 120 s.e. Contrasts Linear Quadratic
22±5 23±1 25±1 1±48
14±5 10±5 9±6 2±29
19±2 19±6 20±4 1±31
12±7 11±9 11±5 1±06
n.s. n.s.
n.s. n.s.
n.s. n.s.
n.s. n.s.
Data are means of four replicates. s.e. is for means in each column ; n.s., contrasts for means in each column not significant.
T 3. Effect of N application rate on total plant N content of maize and S. hermonthica infecting maize grown in sand culture at 90 and 104 d after planting (DAP) maize 90 DAP Maize mg per plant Nitrogen (kg ha−") 20 60 120 s.e. Contrasts Linear Quadratic
104 DAP
Striga Maize Nitrogen content mg per mg per pot plant
Striga mg per pot
54±3 114±8 212±2 19±79
11±0 9±1 6±9 0±52
64±3 143±0 196±9 16±53
19±4 12±8 12±0 1±11
** n.s.
n.s. n.s.
** n.s.
n.s. n.s.
Data are means of four replicates. s.e. is for means in each column ; **, contrasts for means in each column differ at P ! 0±01 ; n.s., not significant.
except for maize at 120 kg N because of a reduced concentration of N in maize root at 104 DAP. N uptake and partitioning The mean specific root N uptake (SRNU) was not affected by Striga at the four–eight leaf stage. By the eight–12 leaf stage however, Striga reduced (P ! 0±001) SRNU from 0±485 to 0±254 mg g−" root d−" (Fig. 4 A). At the four–eight leaf stage, SRNU increased (P ! 0±001) as N supply was increased, but at the eight–12 leaf stage the reverse was observed as SRNU declined (P ! 0±05) with increased N application (Fig. 4 B). There was no significant Striga¬N interaction on SRNU at both growth stages. The partitioning of N to the leaf (LNPC) (Fig. 5 A) was greater (P ! 0±01) for infected maize than for uninfected maize at the four–eight leaf stage but at the eight–12 leaf
291
stage LNPC was unaffected by Striga infection. The proportion of total N partitioned to the stem (SNPC) was neither affected by Striga infection nor N fertilizer application at any growth stage (data not shown). Although the proportion of total N partitioned to the root (RNPC) was greater for infected maize than uninfected maize at the four–eight leaf stage, the difference was not signifcant (Fig. 5 B). At the eight–12 leaf stage, however, RNPC was greater (P ! 0±001) for infected maize than for uninfected maize. The rate of N applied did not affect RNPC at the four–eight leaf stage (Fig. 5 C) but RNPC increased (P ! 0±01) with increased N application at the eight–12 leaf stage. There was no effect of N application rate on LNPC at the four–eight leaf stage but LNPC declined with increased N application at the eight–12 leaf stage (data not shown). DISCUSSION Striga hermonthica reduced leaf and stem dry matter of its maize host but did not affect root dry matter. The reduced maize growth caused by S. hermonthica was not entirely alleviated by N fertilizer at the rates applied in this experiment. This result contrasts with the observation by Cechin and Press (1993) that the extent to which the parasite influenced host performance depended critically on the concentration of nitrogen supplied to the plants ; large differences in performance resulted from small differences in nitrogen supply. The non-significant Striga¬N interaction observed in this study compared with the significant interaction reported by Cechin and Press (1993) might be attributed to the higher levels of N applied by Cechin and Press. The highest rates of N applied in this study (60, 120 kg N) are only equivalent to the two lower levels used by Cechin and Press. The concentration of N in the leaf, stem and root of both infected and uninfected maize declined asymptotically from the first to the last sampling date. The asymptotic values of N were greater in all parts of Striga-infected maize than in uninfected plants. Though there are no values of tissue nitrogen concentration with time for similar studies of Striga-infected host crops for comparison, the general trend in N concentration in dry matter with time is similar to that reported by Greenwood et al. (1991) and Gregory, Crawford and McGowan (1979). The differences in the results of Cechin and Press (1993) and Hibberd et al. (1996) on the one hand and the results of this study on the other, might be a consequence of analysing foliar nutrient concentration at a particular time during growth but not at different periods of growth. However, a recent study by Frost et al. (1997) showed that the concentration of nitrogen in Striga-infected sorghum measured at a single time during growth was greater than that in control plants. The concentrations of nitrogen in the leaf and stem of Striga were greater than that in maize at 90 and 104 DAP ; a time at which N concentrations in both infected and uninfected maize were in the deficiency range. There was, however, no effect of applied nitrogen on N concentrations in Striga. The non-significant effect of N rate on Striga N concentration contrasts with the results of Cechin and Press (1993) who found not only higher leaf N concentrations in
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10 A
B 8 N uptake (mg N g–1 root d–1)
N uptake (mg N g–1 root d–1)
5
4
3
2
1
0
4–8 leaf 8–12 leaf Growth stage of maize
6
4
2
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8–12 leaf 4–8 leaf Growth stage of maize
F. 4. A, Effect of Striga hermonthica infection on the mean specific nitrogen uptake by maize. +, Infected ; 8, uninfected. B, Effect of the rate of nitrogen fertilizer on the mean specific nitrogen uptake by maize. +, 20 kg N ha−" ; 8, 60 kg N ha−" ; *, 120 kg N ha−". Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times.
S. hermonthica than in sorghum, but also a greater increase in N concentration with increased rate of N in Striga than for sorghum. Total plant N content in maize was greater than that in Striga because of the very big differences in dry weight. Total dry weight in Striga ranged from 3 % that of maize at 20 kg N to 0±44 % at 120 kg N at 90 DAP, and from 5 to 0±77 % at 104 DAP. The data from this study indicated that SRNU was similar for infected and uninfected maize at the four–eight leaf stage, but at the eight–12 leaf stage SRNU by infected maize was only 52 % that of uninfected maize. During the early growth stages (four–eight leaf stage) N application increased SRNU. By the later growth stages (eight–12 leaf stage) however, increased N application resulted in reduced SRNU ; a result that is inconsistent with those of McCullough et al. (1994) for an old maize hybrid. McCullough et al. (1994) explained that SRNU as calculated in their study (and in this) cannot show whether the enhanced SRNU in the new hybrid was due to a greater proportion of the root mass that is actively taking N up or whether certain N uptake enzymes were more efficient. Robinson, Linehan and Caul (1991) have shown through calculations that the mean fractions of the root systems of wheat likely to be involved in nitrate uptake were 11 % of the measured total root length for 0 kg N ha−" compared with 3±5 % for 200 kg N ha−". All the nitrogen in this experiment was applied at the three leaf stage hence there was more N available to be taken up coupled with increasing crop growth rate at the early stages of growth. Mumera and Below (1993) and Yaduraju, Hosmani and Probhakara (1979) observed that repeated applications of N were more effective in depressing Striga performance and stimulating host growth than a single initial application. The rate of nitrogen applied did not affect the partitioning of N taken up at the early growth stages to any of the plant parts. At the later growth stages,
increased N supply increased N partitioning to the root (RNPC) and decreased the proportion partitioned to the leaf (LNPC) which contrasts with the results of McCullough et al. (1994). Conversely, Striga infection resulted in higher LNPC at the early growth stages but not at the later stages of growth. There was, however, higher RNPC due to Striga infection at the later stages of growth. The higher LNPC in Striga-infected maize at the early stages of growth might occur because of a reduced growth rate of infected maize leading to a smaller dry matter and consequently greater nitrogen concentration. McCullough et al. (1994) applied nitrogen throughout the duration of their experiment ; once daily from planting until the eight-leaf stage, and from the eight- to the 12-leaf stage nutrient solution was added to plastic saucers beneath the pots. The hypothesis tested in this study was that at low N rates, a maize plant infected with S. hermonthica partitions a greater proportion of nitrogen to the roots (to support the requirements of Striga). The data from the study did not establish any significant interaction between N fertilizer rate and Striga infection in any measured responses. However, we observed that the proportion of total plant N partitioned to the root of a maize plant was greater for Striga-infected plants than for uninfected plants. The mechanistic bases for this partitioning are unknown and need to be examined. In addition, the asymptotic concentration of N in infected plants (leaf, stem, root) was greater than in uninfected plants and the concentration of N in Striga was also greater than that in maize at 90 and 104 DAP. A C K N O W L E D G E M E N TS We thank Dr P. Y. K. Sallah for providing the Striga seed and Dr S. G. Gilmour for statistical help. G. K. S. Aflakpui thanks the Crops Research Institute of the Council for Scientific and Industrial Research, Ghana for study leave ;
Aflakpui et al.—Nitrogen Uptake by Striga-infected Maize 1.00
1.00 A
B
N partitioning coefficient
N partitioning coefficient
0.80
0.60
0.40
0.20
0.00
293
0.80
0.60
0.40
0.20
8–12 leaf 4–8 leaf Growth stage of maize
0.00
8–12 leaf 4–8 leaf Growth stage of maize
1.00
N partitioning coefficient
C 0.80
0.60
0.40
0.20
0.00
8–12 leaf 4–8 leaf Growth stage of maize
F. 5. Effect of Striga hermonthica infection on leaf (A) and root (B) nitrogen partitioning coefficient of maize. +, Infected ; 8, uninfected. C, Relationship between the rate of nitrogen fertilizer and root nitrogen partitioning coefficient. +, 20 kg N ha−" ; 8, 60 kg N ha−" ; *, 120 kg N ha−". Vertical bars indicate s.e. of a 2¬3 factorial experiment replicated four times.
the Ghana-CIDA Grains Development Project and the University of Reading for financial support. LITERATURE CITED Agabawi KA, Younis AE. 1965. Effect of nitrogen application on growth and nitrogen content of Striga hermonthica Benth. and Sorghum ulgare Lur. grown for forage. Plant and Soil 23 : 295–304. Bebawi FF. 1981. Response of sorghum cultivars and Striga population to nitrogen fertilisation. Plant and Soil 59 : 261–267. Cechin I, Press MC. 1993. Nitrogen relations of the sorghum-Striga hermonthica host parasite association : growth and photosynthesis. Plant, Cell and Enironment 16 : 237–247. Cechin I, Press MC. 1994. Influence of nitrogen on growth and photosynthesis of a C cereal, Oryza satia, infected with the root $ hemiparasite Striga hermonthica. Journal of Experimental Botany 45 : 925–930.
Doggett H. 1988. Witchweed (Striga). In : Sorghum 2nd edn. Singapore : Longman Scientific and Technical, 368–404. Egley GH. 1971. Mineral nutrition and the parasite–host relationships of witchweed. Weed Science 19 : 528–533. Farina MPW, Thomas PEL, Channon P. 1985. Nitrogen, phosphorus and potassium effects on the incidence of Striga asiatica (L.) Kuntze in maize. Weed Research 25 : 443–447. Frost DL, Gurney AL, Press MC, Scholes JD. 1997. Striga hermonthica reduces photosynthesis in sorghum : the importance of stomatal limitations and a potential role for ABA ? Plant, Cell and Enironment 20 : 483–492. Greenwood DJ, Gastal F, Lemaire G, Draycot A, Millard P, Neeteson JJ. 1991. Growth rate and %N of field grown crops : Theory and experiments. Annals of Botany 67 : 181–190. Gregory PJ, Crawford DV, McGowan M. 1979. Nutrient relations of winter wheat. 1. Accumulation and distribution of Na, K, Ca, Mg, P, S and N. Journal of Agricultural Science, Cambridge 93 : 485–494. Gurney AL, Press MC, Ransom JK. 1995. The parasite angiosperm
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