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35Russian Journal of Nematology, 2016, 24 (2), 77 - 88
Host response of drought-tolerant aerobic Asian rice genotypes to infection of the rice root-knot nematode Meloidogyne graminicola
Judith Galeng-Lawilao1' 2, Arvind Kumar2 and Dirk De Waele 1 2' 3
'Laboratory of Tropical Crop Improvement, Department of Biosystems, Faculty of Bioscience Engineering, University of Leuven (KU Leuven), Willem de Croylaan 42, B-3001, Heverlee, Belgium 2International Rice Research Institute (IRRI), Dapo Box 7777, Metro Manila, Philippines 3Unit for Environmental Sciences and Management, North-West University, Private Bag X6001, 2520, Potchefstroom, South
Africa, e-mail: dirkdewaele@pandora.be
Accepted for publication 15 April 2016
Summary. Twenty-five progenies (either F4 or F6) derived from crosses between the drought-tolerant Indian upland rice cv. Vandana and the drought-sensitive Indonesian upland rice cv. Way Rarem (both Asian rice) were examined for their host response to Meloidogyne graminicola infection under aerobic conditions in a field experiment at IRRI, Los Baños, Philippines. The host response was compared with the host response of the susceptible references UPLRi-5 and IR64 (both Asian rice), and the resistant reference CG14 (African rice). None of the aerobic progenies was classified as resistant. Compared with UPLRi-5 on the basis of the number of second-stage juveniles (J2) (root system)1, 22 progenies were classified as partially resistant and three as susceptible. Based on the number of J2 (g roots)1, 13 progenies were classified as partially resistant and 12 as susceptible. Compared with IR64 and based on both J2 (root system)1 and J2 (g roots)1, 13 progenies were classified as partially resistant and 12 as susceptible. The aerobic progenies showed a wide variation in terms of tolerance to M. graminicola infection. Fresh root weight was the plant growth trait most affected and percentage filled grains per panicle the yield-contributing trait most affected. On the basis of percentage reduction in yield/plant, seven progenies were classified as tolerant (< 10% yield reduction), nine progenies as less sensitive (1020% yield reduction), eight progenies as sensitive (21-30% yield reduction) and one genotype as highly sensitive (36% yield reduction). Of the eight progenies classified as tolerant, three progenies (IR84984-83-15-862-B, IR90019:6-86 and IR90020:22-265) were also partially resistant. Cultivar Vandana was partially resistant and less sensitive, whilst cv. Way Rarem was partially resistant/susceptible and tolerant to M. graminicola infection.
Key words: aerobic rice, breeding, damage potential, reproductive potential, plant traits, resistance, sensitivity, susceptibility, tolerance, yield loss.
Aerobic rice is a water-saving rice production system for water-short environments with favourable soils and adapted, potentially high-yielding varieties that are direct dry-seeded in well-drained, non-puddled and non-saturated soils without ponded water. Soils remain aerobic but supplementary irrigation is applied as necessary (Bouman, 2001; Bouman et al., 2005). The rice varieties used in this system usually combine the drought resistance of upland varieties and the high-yielding ability of lowland varieties (Lafitte et al., 2002).
Continuous cropping of aerobic rice in the same field can result in yield decline (Peng et al., 2006), rapid yield losses (George et al., 2002; Pinheiro et
al., 2006; Nie et al., 2012) and even yield failure (Kreye et al., 2009). The rice root-knot nematode Meloidogyne graminicola Golden & Birchfield, 1965 was identified as one of the soil-borne pathogens limiting yield of aerobic rice (Kreye et al., 2009). During the past decades, this sedentary endoparasitic nematode species has emerged as one of the most important biotic constraints to rice production in Asia (De Waele & Elsen, 2007). It is present in all South Asian and Southeast Asian countries surveyed so far (Jain et al., 2012) and can cause significant yield losses of Asian rice grown in all rice-based production systems: lowland as well as upland, irrigated as well as rainfed, and deepwater rice (Bridge & Page, 1982; Prot et al.,
1994; Padgham et al., 2004; Bridge et al., 2005; Win et al., 2011). In upland conditions and shallow intermittently flooded land, M. graminicola is considered to be by far the most damaging Meloidogyne species on rice (De Waele & Elsen 2007). In M. graminicola-infested upland rice fields, nematicide application resulted in a yield increase of 12-33% in Thailand (Arayarungsit, 1987) and 28-87% in Indonesia (Netscher & Erlan, 1993).
Management options for M. graminicola include crop rotation, prolonged flooding and the use of nematicides (De Waele et al., 2013). Crop rotation can be effective (Ventura et al., 1981; Rahman, 1990) but is seldom adopted by farmers unless there is an additional benefit, such as a marketing-for-cash-income opportunity, beyond nematode management (Starr et al., 2002). Also, Echinocloa spp., which are dominant weed species in aerobic rice fields, are good hosts of M. graminicola (Chauhan & Johnson, 2011). Prolonged or permanent flooding is not feasible in areas that are experiencing water scarcity. The use of nematicides is limited to smallholder farmers because of their high cost and toxicity to humans and the environment. In this context, the use of resistant or tolerant cultivars offers a promising alternative for the effective, economic and environment-friendly management of M. graminicola.
The objective of our study was to examine the host response to M. graminicola infection of aerobic Asian rice (Oryza sativa L.) genotypes with improved tolerance to drought. These aerobic genotypes were either F4 or F6 progenies of cvs Vandana x Way Rarem crosses. Cultivar Way Rarem is a drought-sensitive Indonesian upland rice cultivar, whilst cv. Vandana is a drought-tolerant Indian upland rice cultivar. Following the terminology of Bos & Parlevliet (1995), resistance/susceptibility and
tolerance/sensitivity are defined as independent, relative qualities of a host plant based on comparison between genotypes. A host plant may either suppress (resistance) or allow (susceptibility) nematode development and reproduction; it may suffer either little injury (tolerance), even when heavily infected with nematodes, or much injury (sensitivity), even when relatively lightly infected with nematodes. Resistance/susceptibility can be determined by measuring the nematode population densities on and in the roots, whereas tolerance/sensitivity can be determined by measuring the effect of the nematode population on plant growth, yield-contributing traits and/or yield (Cook & Evans, 1987).
MATERIAL AND METHODS
Plant material. Twenty-five aerobic rice progenies and the two parents, cvs Vandana and Way Rarem, were included in our study (Table 1). These progenies have an improved tolerance to drought based on field drought screening done at the International Rice Research Institute (IRRI) in Los Baños, Philippines (Kumar, pers. comm.). CG14R (African rice) was included as the resistant reference rice genotype while IR64S and UPLRi-5S (both Asian rice) were included as susceptible reference rice genotypes to M. graminicola infection.
Field experiment. The experiment was carried out in a nematode-infested field (a so-called 'hot spot') under aerobic rice growing conditions at IRRI, Los Baños, Philippines (14°11' N, 121°15' E, 21 m above sea level) during the 2012 dry season (January-May). The soil of the IRRI upland farm is a Maahas clay loam soil (isohyperthermic mixed Tropudalf) (Zhao et al., 2006). The infested field has been developed as a so-called hotspot for experiments with M. graminicola. For 2 years, the field was continuously planted with UPLRi-5S to build up the M. graminicola population densities. Prior to the commencement of the experiment, soil sampling was done to determine the nematode population densities. On average, the field was infested with 87 second-stage juveniles (J2) (200 ml soil)-1. Despite continuous planting of the susceptible cultivar, the nematode density was not equally distributed throughout the field; thus, to ensure a more uniform distribution in half of the field, nematode-infected UPLRi-5S roots were chopped in 1-cm-pieces and 180 g infected roots were incorporated (3-5 cm deep) along each 3-m single row plot just before seeding. On average, 180 g roots were infected with 34,000 J2 and 170 females. In the other half of the field, solarisation and nematicide application was applied to kill the nematodes. The soil was covered with a black plastic sheet for 15 days before seeding after which carbofuran (Furadan®, 10 g) was applied at 4.5 kg a.s. ha-1.
In both field halfs, the experimental layout was a three-replicated alpha lattice design with 3-m single row plots. The rows were spaced 0.25 m apart. Seeds of each rice genotype were dry direct-seeded using a seeding density of 1.5 g per linear meter of row. Basal fertiliser applications equivalent to 40 P and 40 K kg ha-1 in the form of single super phosphate and potassium chloride, and 120 kg ha-1 of N in the form of ammonium sulphate were applied in three even splits around 21, 42, and 61 days after seeding. After seeding, irrigation through evenly placed sprinklers was done daily for 5 days
to keep the field saturated to allow good germination of the seeds. After germination, the plants were grown under aerobic rice growing conditions (i.e., in a well-drained, non-saturated soil) for the duration of the experiment. They were irrigated twice weekly until maximum tillering of the plants, then three times weekly until harvest. Irrigation was not applied during rainy days. Manual weeding was done when necessary.
Assessment of the severity of root galling and M. graminicola population densities. Eighteen sample plants of each rice genotype (six from each replicate) were carefully removed from the soil, washed with tap water to remove all adhering soil particles and the fresh root weight of each root system recorded. The severity of root galling (root galling index) was visually assessed for each uprooted plant by rating the percentage of roots with root tip galls per root system on a 0-5 scale, according to the rice root-knot rating chart of Hussey & Janssen (2002). After recording so-called root gall indices, roots were cut into about 0.5 cm pieces and placed on a labelled sieve contained in a plastic cup (8 cm diam., 12 cm high). Cups were placed in a mistifier at 27°C that produced a fine mist of water for 90 s every 10 min (Seinhorst, 1950; Hooper et al., 2005). The nematodes in water suspension were collected at 7 and 14 days after the roots were placed in the mistifier. The suspension was homogenised by gentle blowing and a 1 ml sub-sample was taken (pipetted) for counting the J2 in a counting dish using a stereomicroscope. The average of two counts was used to calculate the final nematode population density (Pf = J2 (root system)-1). Pf divided by the root weight gave the number of J2 per root unit (i.e., 1 g fresh roots).
To measure the level of resistance to M. graminicola infection of each progeny, the number of J2 per root system and per g roots of nematode-infected plants were compared to UPLRi-5S and IR64S, and CG14r based on the method described by Dochez et al. (2005) (Table 1).
Assessment of plant growth and yield-contributing traits. The phenotype of eighteen sample plants from each genotype (six plants from each replicate) was recorded. Plant height was measured at the seedling stage, maximum tillering and at the mature grain stage (harvest) of the plants. Plant height at seedling and maximum tillering stage was measured from the soil surface to the tip of the tallest leaf. Plant height at harvest was measured from the soil surface to the tip of the panicle of the main tiller. Days to flowering was noted when 50% of the plants of each genotype in a plot had flowering tillers. At harvest, fresh shoot and root weight were recorded. Dry shoot and root weight were recorded after oven drying at 70°C for 72 h.
Grains were manually threshed. Filled and unfilled grains in one panicle of 18 plants per genotype were counted. On the basis of this count, the total number of spikelets per panicle was determined. Yield per plant was calculated by weighing the totally filled grains of each plant. Yield per plot was determined by measuring the weight of all filled grains of all plants in a plot. The weight of 100 filled seeds of each genotype was also noted. Grain yield is reported at 14% moisture content.
To measure the level of tolerance to M. graminicola infection of each genotype, the yield of nematode-infected plants was compared with the yield of non-infected plants and the percentage reduction
Statistical difference with IR64S or UPLRi-5S Statistical difference with CG14R Host response
Significant(*) Not significant Resistant (R)
Significant Significant Partially resistant (PR)
Not significant (ns) Significant Susceptible (S)
Not significant Not significant Inconclusive (I)
* Significant according to LSD (P < 0.05).
Table 1. Classification of the host response of 25 aerobic rice progenies derived from cvs Vandana x Way Rarem crosses to Meloidogyne graminicola infection based on a comparison with the host response of the susceptible parents UPLRi-5S and IR64S, and the resistant parent CG14R.
calculated. The scale in Table 2 was used to determine the level of tolerance. It is based on the outcome of experiments conducted during a decade at IRRI (De Waele, pers. comm.).
Table 2. Level of tolerance of rice genotypes to Meloidogyne graminicola infection based on the percentage yield reduction between nematode-infected and non-infected plants.
% yield reduction Level of tolerance
< 10 Tolerant
10-20 Less sensitive
21-30 Sensitive
> 30 Highly sensitive
Data analysis. All data were analysed using the mixed model analysis in IRRI CropStat 7.2. Nematode population densities were log10(x+i) transformed prior to analysis. Plant growth and yield-contributing traits, yield and nematode population densities were analysed by ANOVA. The progenies were considered as a fixed effect, while block and replicates were considered as a random effect. The model was genotype + replication + block (replication) + error. Combined analysis was used to determine the effect of nematode infection on the plant traits measured compared with the non-infected plants. The infested and non-infested field plots were treated as trial and the model was trial + trial (rep) + trial (rep) (block) + genotype + trial (genotype) + residuals. Trial (rep) and trial (rep) (block) were considered as random effect and trial (genotype) was considered as fixed effect. Least significance difference (LSD) was used to compare nematode population densities and plant traits of progenies in the nematode-infested and non-infested field plots. The percentage reduction of the plant growth and yield-contributing traits, and yield of nematode-infected plants compared with non-infected plants were computed using this formula:
infected plants infected plants
RESULTS
Severity of root galling. The 25 aerobic progenies had an average root gall rating of 3 (2650% root tips with galls). Gall rating in CG14R averaged 1, and in UPLRi-5S and IR64S 4 and 5, respectively (Table 3).
Meloidogyne graminicola population densities.
The host response of the aerobic progenies to infection of M. graminicola in terms of susceptibility is presented in Table 3. None of the progenies was classified as resistant. When compared with UPLRi-5S and CG14R, and based on the number of J2 (root system)-1, 22 progenies were classified as partially resistant and three as susceptible. Based on the number of J2 (g roots)-1, 13 progenies were classified as partially resistant and 12 as susceptible. When compared with IR64S and CG14R, 13 progenies were identified as partially resistant and 12 as susceptible based on J2 (root system)-1 while also 13 progenies were classified as partially resistant and 12 as susceptible based on J2 (g roots)-1. The susceptible and resistant reference genotypes showed the expected host response.
Nematode population densities in the progenies averaged 2,407 J2 (root system)-1 and 314 J2 (g roots)-1. Among the progenies, the lowest (936) number of J2 (root system)-1 was observed in IR900: 16-3 and the highest (4,514) number of J2 (root system)-1 in IR84984-21-19-41-B. In UPLRi-5s and IR64S, nematode reproduction was 15,470 and 9,524 J2 (root system)-1 and 1,426 and 1,301 J2 (g roots)-1, respectively. The lowest nematode reproduction was observed in CG14R (184 J2 (root system)-1 and 29 J2 (g roots)-1).
Cultivar Vandana was classified as partially resistant based on both J2 (root system)-1 and J2 (g roots)-1. With the exception of CG14R, cv. Vandana had the lowest number of J2 (root system)-1 (839) and only 75 J2 (g roots)-1 of all genotypes examined. Of the 25 progenies, 12 (44.4%) were consistently partially resistant in both comparisons. Cultivar Way Rarem was classified as partially resistant when compared with UPLRi-5S on the basis of J2 (root system)-1 but as susceptible on the basis of J2 (g roots)-1. It was classified as susceptible when compared with IR64S on the basis of both J2 (root system)-1 and J2 (g roots)-1.
Effect of M. graminicola infection on plant growth and yield-contributing traits, and yield.
The effect of infection with M. graminicola on the plant traits measured is presented in Tables 4 and 5. Nematode infection did not significantly affect plant height (data not shown). Fresh and dry root and shoot weights of nematode-infected plants of the progenies combined were on average reduced with 43.1, 19.5, 15.8 and 14.0%, respectively. The percentage reduction in fresh root weight in most progenies (22) was significant (P < 0.05). The percentage reduction in dry shoot weight was significant (P < 0.05) in only two progenies. In cv. Vandana only fresh root weight was significantly
Table 3. Fresh root weight, root population densities of Meloidogyne graminicola, host response (in terms of susceptibility) and severity of root gall rating of drought-tolerant progenies derived from cvs Vandana x Way Rarem
crosses at harvest.
Root wt. (g) Per root system Per g/roots Root gall rating
No Progeny designation No. of J2 Host response* (IR64S/ CG14R) Host response* (UPLRi-5S/ CG14R) No. of J2 Host response* (IR64S/ CG14R) Host response* (UPLRi-5S/ CG14r)
1 IR 84984-83-15-828-B 8.0 2999 S PR 373 S S 3
2 IR 84984-21-19-78-B 6.9 1757 PR PR 254 PR PR 2
3 IR 84984-83-15-110-B 7.6 4346 S PR 573 S S 3
4 IR 84984-83-15-837-B 9.3 1808 PR PR 195 PR PR 3
5 IR 84984-83-15-862-B 8.8 1879 PR PR 213 PR PR 3
6 IR 84984-21-19-685-B 9.2 1692 PR PR 183 PR PR 2
7 IR 84984-83-15-330-B 7.0 1513 PR PR 217 PR PR 2
8 IR 84984-83-15-151-B 7.2 1629 PR PR 226 PR PR 2
9 IR 84984-83-15-608-B 8.2 3227 S PR 395 S S 3
10 IR 84984-21-19-41-B 8.0 4514 S PR 566 S S 4
11 IR 84984-83-15-481-B 6.3 2912 S PR 460 S S 3
12 IR 90019:6-86 12.2 1726 PR PR 142 PR PR 3
13 IR 90019:16-8 7.6 2536 S S 335 PR PR 3
14 IR 90018:19-97 7.0 2466 S PR 352 S S 3
15 IR 90019:17-15 10.7 4192 S PR 391 S S 3
16 IR 90018:19171 11.4 3783 S S 331 S S 3
17 IR 90019:17156 7.6 1513 PR PR 198 PR PR 2
18 IR 90019:17159 5.3 2343 S S 443 S S 3
19 IR 90023:23-1 6.5 1744 PR PR 267 PR PR 3
20 IR 90023:23181 8.4 1214 PR PR 145 PR PR 3
21 IR 90020:22283 4.8 2039 PR PR 425 S S 4
22 IR 90019:16-34 7.2 2535 S PR 350 S S 3
23 IR 90020:22-81 5.7 3052 S PR 535 S S 3
Table 3 (continued). Fresh root weight, root population densities of Meloidogyne graminicola, host response (in terms of susceptibility) and severity of root gall rating of drought-tolerant progenies derived from Vandana x Way Rarem crosses at harvest.
Per root system Per g/root Root
No. Progeny designation Root wt. (g) No. of J2 Host response (IR64S/ CG14R) Host response (UPLRi-5S/ CG14R) No. of J2 Host response (IR64S/ CG14R) Host response (UPLRi-5S/ CG14r) gall ratin g
24 IR 90019:16-3 6.8 936 PR PR 137 PR PR 2
25 IR 90020:22-265 11.0 1,82 1 PR PR 165 PR PR 2
Average 8.0 2407 314 2.8
27 26 28 Way Rarem Vandana CG14r 6.0 11.2 6.4 2461 839 184 S PR R PR PR R 409 75 29 S PR R S PR R 2 3 1
29 UPLRi-5S 10.8 1547 S S 1,42 6 S S 4
30 IR64S 7.3 9524 S S 1,30 1 S S 5
LSD (5%) 1 0.73 1.3
Data represent the average of 18 replicates. J2 = second-stage juveniles.
* Host response based on a comparison with IR64S and CGR, and UPLRi-5S and CG14R R: resistant; PR: partially resistant; S: susceptible based on LSD (P < 0.05).
Root galling rated by 0 = no galls, 1 = 1 < 10% galls, 2 = 11-25% galls, 3 = 26-50% galls, 4 = 51-75% galls and 5 = > 70% of the root system galled.
Table 4. Fresh and dry root and shoot weight, and percentage reduction of drought-tolerant progenies derived from cvs Vandana x Way Rarem crosses at harvest grown in non-infested (U) and Meloidogyne graminicola-infested (I)
fields.
Fresh root wt. Dry root wt. Fresh shoot wt. Dry shoot wt.
Progenies designation U I % Reduction U I % Reduction U I % Reduction U I % Reduction
IR 84984-21-19-41-B 11.7 6.1 48.1 * 1.5 1.2 21.4 ns 39.0 38.7 0.7 ns 15.3 14.0 8.3 ns
IR 84984-21-19-685-B 10.2 5.6 44.8 * 1.4 1.0 29.9 ns 41.8 35.5 15.2 ns 13.6 12.5 7.9 ns
IR 84984-21-19-78-B 8.8 7.3 16.9 ns 1.4 1.3 6.7 ns 43.8 33.6 23.1 ns 16.4 15.4 6.3 ns
IR 84984-83-15-110-B 10.3 5.6 45.3 * 1.5 1.2 19.9 ns 41.2 36.4 11.8 ns 17.8 12.7 28.5 ns
IR 84984-83-15-151-B 9.7 5.3 45.1 * 1.5 1.2 18.6 ns 40.9 36.8 10.1 ns 18.5 13.5 27.3 ns
IR 84984-83-15-330-B 12.8 6.1 52.3 * 1.4 1.2 14.5 ns 46.8 37.0 20.9 ns 16.7 12.8 23.4 ns
IR 84984-83-15-481-B 9.2 4.8 47.7 * 1.4 1.2 13.4 ns 41.2 26.1 36.6 * 14.4 11.2 21.9 ns
IR 84984-83-15-608-B 14.2 5.9 58.8 * 1.3 1.1 13.3 ns 40.3 35.6 11.7 ns 16.6 16.1 2.7 ns
IR 84984-83-15-828-B 10.6 6.3 40.5 * 1.4 1.2 19.3 ns 45.2 36.8 18.6 ns 16.0 14.6 8.7 ns
IR 84984-83-15-837-B 9.1 5.9 35.0 * 1.6 1.2 25.5 ns 42.4 34.5 18.6 ns 19.2 15.7 18.6 ns
IR 84984-83-15-862-B 8.0 5.4 32.8 ns 1.4 1.1 19.1 ns 50.6 48.2 4.8 ns 19.8 18.6 6.1 ns
IR 90018:19171 10.1 5.4 46.4 * 1.4 1.1 23.0 ns 39.5 35.9 9.3 ns 20.3 15.4 24.2 ns
IR 90018:19-97 9.9 5.0 49.1 * 1.4 1.0 29.0 ns 49.8 44.4 10.7 ns 26.3 20.7 21.1 ns
IR 90019:16-3 10.4 5.3 49.1 * 1.5 1.2 17.6 ns 39.3 35.1 10.8 ns 14.4 15.3 +6.3 ns
IR 90019:16-34 8.8 4.8 44.8 * 1.5 1.1 23.5 ns 33.5 28.8 14.0 ns 16.0 12.2 23.5 ns
IR 90019:16-8 10.1 4.9 51.3 * 1.4 1.1 18.7 ns 35.1 31.3 10.8 ns 15.4 15.5 +0.5 ns
IR 90019:17-15 9.9 5.5 44.2 * 1.5 1.2 23.7 ns 40.5 31.9 21.3 ns 17.9 16.7 6.9 ns
IR 90019:17156 8.6 5.5 36.0 * 1.4 1.3 6.9 ns 33.0 25.3 23.4 ns 12.2 12.6 +2.7 ns
IR 90019:17159 10.0 5.0 50.0 * 1.5 1.1 25.3 ns 39.0 37.4 4.3 ns 15.5 14.4 7.5 ns
IR 90019:6-86 8.2 5.5 33.2n s 1.5 1.1 23.2 ns 30.4 30.3 0.5 ns 11.9 12.1 +1.1 ns
IR 90020:22265 10.7 5.5 48.2 * 1.4 1.1 21.9 ns 38.8 35.2 9.2 ns 12.3 11.8 3.7 ns
IR 90020:22283 9.4 6.9 26.1 ns 1.5 1.1 26.3 ns 48.6 33.8 30.4 * 18.8 14.6 22.6 ns
IR 90020:22-81 9.0 5.3 41.3 * 1.4 1.2 14.8 ns 48.1 47.8 0.6 ns 20.6 13.7 33.5 *
IR 90023:23-1 9.7 5.8 40.0 * 1.5 1.3 11.9 ns 51.4 30.0 41.7 * 20.9 14.5 30.7 *
IR 90023:23181 10.3 5.2 49.8 * 1.5 1.2 20.6 ns 43.9 27.9 36.5 * 18.8 13.6 27.7 ns
Table 4 (continued). Fresh and dry root and shoot weight, and percentage reduction of drought-tolerant progenies derived from Vandana x Way Rarem crosses at harvest grown in non-infested (U) and Meloidogyne graminicola-infested (I) fields.
Progenies designation Fresh root wt. Dry root wt. Fresh shoot wt. Dry shoot wt.
U I % Reduction U I % Reduction U I % Reduction U I % Reduction
Average 10.0 5.6 43.1 1.4 1.2 19.5 41.8 35.0 15.8 17.0 14.4 14.0
cv. Vandana 10.1 5.4 47.1 * 1.2 1.2 2.9 ns 43.4 37.2 14.3 ns 14.4 10.3 28.5 ns
cv. Way Rarem 11.0 8.0 27.5 * 1.5 1.3 13.8 ns 58.4 31.4 46.2 * 13.4 10.1 24.9 ns
CG14r 7.0 6.4 8.2 1.3 1.2 7.7 ns 44.1 41.8 5.2 ns 14.2 13.7 3.7 ns
UPLRi-5S 15.0 10.8 27.7 * 2.7 1.2 55.6 * 31.8 20.3 36.2 * 8.8 5.5 37.5 *
IR64S 12.0 7.3 39.0 * 2.3 1.1 52.2 * 47.4 22.0 53.6 * 10.4 4.2 59.4 *
LSD (0.05) 3.2 0.9 14.3 6.5
Data represent the average of 18 replicates.
*: significantly different; ns: not significantly different between plants grown in non-infested (U) and nematode-infested (I) field according to LSD (P<0.05). "+" indicates an increase in dry shoot weight.
Table 5. Percentage filled grains/panicle, weight of 100 seeds, yield/plant, percentage reduction in yield/plant and host response (in terms of sensitivity) of 27 drought-tolerant progenies derived from cvs Vandana x Way Rarem crosses at harvest grown in non-infested (U) and Meloidogyne graminicola-infested (I) fields.
Progenies designation Percentage filled grains/ panicle Wt. of 100 seeds Yield/ plant Percentage yield reduction Host
U I U I U I response
IR 84984-21-19-41-B 84.2 78.4 2.4 2.3 8.2 7.3 11 ns LS
IR 84984-21-19-78-B 85.1 82.4 2.5 2.4 9.0 7.5 17 ns LS
IR 84984-21-19-685-B 81.5 85.9 2.5 2.4 9.0 7.7 14 ns LS
IR 84984-83-15-110-B 79.4 78.8 2.4 2.4 8.8 7.1 19 ns LS
IR 84984-83-15-151-B 85.4 79.1 2.5 2.4 10.1 7.4 27 * S
IR 84984-83-15-330-B 81.5 77.4 2.3 2.3 8.6 6.8 21 ns S
IR 84984-83-15-481-B 81.5 78.4 2.4 2.4 9.4 6.0 36 * HS
IR 84984-83-15-608-B 85.7 77.0 2.5 2.4 9.4 7.4 21 ns S
IR 84984-83-15-828-B 73.4 72.8 2.4 2.3 9.7 6.8 30 * S
IR 84984-83-15-837-B 79.4 79.7 2.3 2.4 9.6 7.2 25 * S
IR 84984-83-15-862-B 77.5 74.6 2.5 2.3 9.1 8.3 9 ns T
IR 90018:19-97 80.6 74.4 2.5 2.4 9.2 9.2 0 ns T
IR 90018:19-171 82.1 81.5 2.4 2.4 7.9 7.9 0 ns T
IR 90019:6-86 77.1 72.4 2.5 2.5 7.7 7.0 9 ns T
IR 90019:16-3 78.5 79.8 2.4 2.4 9.3 7.7 17 ns LS
IR 90019:16-8 78.4 75.2 2.5 2.4 8.7 8.5 2 ns T
IR 90019:16-34 80.3 76.7 2.4 2.3 8.1 7.3 10 ns LS
IR 90019:17-15 80.4 72.0 2.4 2.3 8.3 7.0 15 ns LS
IR 90019:17-156 87.3 78.1 2.5 2.4 7.8 6.3 20 ns LS
IR 90019:17-159 80.3 78.7 2.4 2.3 9.2 7.9 14 ns LS
IR 90020:22-81 77.6 70.8 2.5 2.4 8.3 8.4 +2 T
IR 90020:22-265 80.8 65.9 2.6 2.5 7.8 8.0 +3 T
IR 90020:22-283 80.4 75.2 2.5 2.5 9.8 6.9 30* S
IR 90023:23-1 79.5 79.7 2.5 2.5 9.9 7.0 30* S
IR 90023:23-181 82.5 73.3 2.6 2.5 10.0 7.0 30* S
Average 80.8 76.7 2.5 2.4 8.9 7.4 16
Vandana 81.3 78.9 2.5 2.4 8.4 7.0 18 ns LS
Way Rarem 78.7 66.0 2.5 2.5 6.6 6.1 7 ns T
CG14r 92.7 84.0 2.5 2.4 8.3 7.2 13 ns LS
UPLRi-5S 43.0 39.3 2.3 2.3 11.0 3.0 72 * HS
IR64S 67.2 62.8 2.4 2.4 14.4 4.1 72 * HS
LSD(0.05) 2.3
Data represent the average of 18 replicates.
*: significantly different; ns: not significantly different between plants grown in non-infested (U) and nematode-infested (I) field according to LSD (P < 0.05). +: indicates an increase in yield.
T: tolerant (< 10% yield reduction); LS: less sensitive (10-20% yield reduction); S: sensitive (21-30% yield reduction) and HS: highly sensitive (> 30% yield reduction).
(P < 0.05) reduced, while in cv. Way Rarem fresh root and shoot weight were significantly (P < 0.05) reduced. In nematode-infected plants of UPLRi-5S and IR64S, the percentage reduction in fresh and dry root and shoot weight was always significant (P < 0.05) but never in CG14R.
Yield reduction in the progenies ranged from 0 to 30% and averaged 16% (Table 5). Of the 25 progenies, seven progenies were classified as tolerant, nine progenies as less sensitive, eight progenies as sensitive and one progeny as highly sensitive to M. graminicola infection. Cultivars Vandana and Way Rarem were classified as less sensitive and tolerant, respectively. CG14r was classified as less sensitive and both UPLRi-5S and IR64S as highly sensitive. The highest percentage yield reduction (72%) was observed in both UPLRi-5S and IR64S.
Of the eight progenies identified as tolerant, three progenies were partially resistant, whilst five were susceptible to M. graminicola infection. Of the nine less sensitive genotypes, four were partially resistant and five were susceptible to M. graminicola infection. Four of the tolerant progenies (IR90018:19-97, IR90019:16-8, IR90020:22-81 and IR84984-83-15-862-B) were high-yielding in both the non-infested and the infested field halfs.
DISCUSSION
The host response of the susceptible and resistant parents included in our study in terms of nematode infection levels at harvest shows that the establishment of the field as a 'hot spot' was successful and that the results obtained are reliable. These results show a variation in host response to M. graminicola infection among the aerobic progenies examined, as well in susceptibility as in sensitivity.
No resistance comparable to the resistance of CG14r was found but many of the aerobic progenies were found to be partially resistant, i.e., less susceptible compared with either IR64S or UPLRi-5s or both. The number of J2 (root system)-1 recovered from the aerobic progenies was 4.0 and 6.4 times lower compared with the average number of J2 (root system)-1 recovered from IR64S and UPLRi-5S, respectively. This observation also suggests that the partial resistance, especially of the parent cv. Vandana, was inherited by the progenies and that the reproductive potential of M. graminicola on the aerobic progenies is lower. The number of partially resistant progenies was higher when UPLRi-5S was used as the susceptible reference genotype (both based on J2 (root system)-1 and J2 (g roots)-1) than when IR64S was used as the susceptible reference genotype. This difference is
due to the difference in degree of susceptibility between the two susceptible reference genotypes. Using IR64S is more rigorous in identifying resistant and partially resistant genotypes.
Among the plant growth traits examined, fresh root weight was the trait most affected. One should expect that drought-tolerant rice genotypes have a root system that allows them to withstand adverse soil conditions but our results show that as well the drought-tolerant parent cv. Vandana (-47.1%) as most of the aerobic progenies (-43.1% for all the progenies combined) suffered extremely high reductions in fresh root weight. Among the yield-contributing traits examined, percentage filled grains per panicle was the trait most affected.
Yield was significantly reduced in about 25% of the aerobic progenies. Recently, De Waele et al. (2013) reported yield losses ranging in some upland aerobic and Asian rice genotypes evaluated under aerobic conditions in outdoors raised beds. A reduction in root fresh weight is a typical damage caused by soil-borne plant-parasitic nematodes. Especially the disruption of sedentary endoparasitic root-knot nematodes such as M. graminicola is a major cause of root damage (Trudgill, 1991). The galls and the feeding sites (giant cells) induced by these nematodes disrupt the xylem and divert assimilates (Meon et al., 1978; Wilcox-Lee & Loria, 1987). This type of damage directly reduces root growth and the uptake of water and nutrients from the soil (Evans et al., 1977). It can also cause substantial reductions in the photosynthetic rate per unit area of leaf, which in turn can make the plants non-responsive to any inputs (Loveys & Bird, 1973; Arntzen & Schans, 1988). In rice, water is most crucial during the reproductive stage starting from panicle initiation to flowering. Root damage prior and during this stage will lead to unfilled grains that eventually result in yield reduction.
Interestingly, three genotypes (IR84984-83-15-862-B, IR90019:6-86 and IR90020:22-265) were at the same time partially resistant and tolerant to M. graminicola infection. These progenies can be grown in nematode-infested field under aerobic conditions because they will limit yield losses caused by the nematodes and might suppress the build-up of high nematode soil population densities. Five other progenies with partial resistance were either less sensitive or sensitive. This observation suggests that resistance and tolerance to M. graminicola infection in Asian rice are inherited and expressed independently, confirming previous observations (De Waele et al., 2013). Progenies with partial resistance and which are less sensitive to M. graminicola (such as IR84984-21-19-685-B,
IR84984-21-19-78-B, IR90019:16-3, IR90019:17-156 and cv. Vandana) might be utilised in crop rotation sequences with susceptible and sensitive Asian rice genotypes although their efficacy in managing M. graminicola below damage threshold levels should be investigated. Progenies that are susceptible but are less sensitive might be also useful in a crop rotation sequence following resistant genotypes as means of reducing the rate of selection for virulence. Five of the tolerant progenies (IR90019:16-8, IR90020:22-81, IR90018:19-97, IR84984-83-15-862-B and IR90020:22-265) were high-yielding even when infected with M. graminicola and these can also be directly grown in nematode-infested field under aerobic conditions. Susceptible and sensitive progenies (such as IR84984-83-15-608-B and IR84984-83-15-828-B) and susceptible and highly sensitive progenies (such as IR84984-83-15-481-B) should not be cultivated in the field to avoid substantial yield losses and even yield failure.
ACKNOWLEDGEMENTS
This study was supported by a Flemish Interuniversity Council (VLIR-UOS) Ph.D. scholarship to J. Galeng-Lawilao. The authors would like to thank the Nematology and Drought/aerobic breeding group at IRRI for their technical assistance.
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Резюме. На 25 гибридах (F4 или F6), происходящих от скрещивания между засухоустойчивым индийским суходольным сортом cv. Vandana и засухоустойчивым индонезийским суходольным сортом cv. Way Rarem (Азиатские сорта), была исследована реакция на поражение нематодой Meloidogyne graminicola при аэробных условиях в полевом эксперименте на бае Международного института риса в Лос-Баньос, Филиппины. Реакцию растения-хозяина сравнивали с таковой у восприимчивых азиатских сортов ЦРЕШ-5и IR64 и устойчивым африканским сортом CG14. Ни один из гибридов не был устойчивым. По числу личинок 2-й стадии на корневую систему 22 полученных гибрида оказались частично устойчивыми в сравнении с UPLRi-5, а три - чувствительными. По числу личинок 2-й стадии на грамм корней 13 гибридом оказались устойчивыми, а 12 - восприимчивыми. В сравнении с Ж64по двум этим параметрам 13 гибридов оказались частично устойчивыми, а 12 - чувствительными. В аэробных условиях гибриды показывали значительную вариабельность в устойчивости к M. graminicola. Вес живых корней оказался наиболее восприимчивым к заражению физиологическим параметром, а процент налившихся зерен на метелку - самым восприимчивым производственным параметром. По показателю сокращения выхода зерен на растение семь гибридов рассматриваются как устойчивые (< 10% падения выхода), девять - как восприимчивые (10-20%), восемь как восприимчивые (21-30%), а один сорт - как сверхвосприимчивый (36%).
