Genetic improvement of rice in aerobic systems: progress from yield to genes

Field Crops Research 75 (2002) 171±190

Genetic improvement of rice in aerobic systems: progress from yield to genes H.R. La®ttea,*, B. Courtoisb, M. Arraudeaub a

IRRI, DAPO 7777, Metro Manila, Philippines CIRAD-Biotrop, TA40/03 Avenue, Agropolis 34398, Montpellier Cedex 5, France

b

Received 3 February 2002; accepted 7 February 2002

Abstract Genetic improvement of rice for aerobic (non-¯ooded) environments has received less attention than breeding for lowland production systems. Aerobic rice has traditionally been grown in low-input systems, but as fresh water for irrigation becomes increasingly scarce, aerobic rice cultivation is expected to expand into regions with more intensive cropping. The primary yield constraints for the low-input aerobic crop include water de®cit, acid and infertile soils, weed competition, and disease. Yield potential has been improved through traditional breeding approaches, and some improved upland rice cultivars show a similar pattern of interactions with environments as traditional cultivars. Critical environmental factors that interact with genotype are the distribution of rainfall during the season, the amount of solar radiation received in the period just prior to ¯owering, and disease pressure. In systems where adequate inputs are applied, aerobic rice tends to yield less than lowland rice, and yield reductions are dramatic when water de®cit occurs. The poor adaptation of the lowland cultivar IR72 to aerobic soils is associated with reduced height and harvest index in aerobic conditions, but IR72 had similar biomass production by anthesis as betteradapted upland cultivars. The best-yielding upland lines had very stable pre-anthesis biomass production across ®ve contrasting environments. The physiological and molecular dissection of aerobic rice yield is expected to identify opportunities to accelerate progress in the areas of aerobic adaptation, tolerance to water de®cit, and improved weed competitiveness. QTLs have been reported for a number of traits potentially related to performance under water de®cit, such as improved root morphology and osmotic adjustment. In an upland-by-lowland mapping population, alleles from the lowland cultivar contributed signi®cantly to improved yield in aerobic environments. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Rice; Drought; Water de®cit; Genotype-by-environment interaction; QTL

1. Introduction The physiological basis of genetic yield gains in irrigated lowland rice cultivars has been examined extensively (Ashraf et al., 1993; Yoshida, 1981; Peng et al., 2000). A major breakthrough came in the 1970s with the introduction of the semi-dwarf plant type, * Corresponding author. E-mail address: [email protected] (H.R. Lafitte).

which allowed greatly increased responsiveness to N fertilizer. The successful plant type had erect leaves, allowing good penetration of light into the canopy, and short, stiff stems that limited lodging. Since that time, further important gains have been achieved through the introduction of pest and disease resistances. In addition, the yield per day has increased as growth duration has been reduced without reducing grain yield. Less is understood about cultivars that have been developed for unfavorable environments. About half

0378-4290/02/$ ± see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 4 2 9 0 ( 0 2 ) 0 0 0 2 5 - 4

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of the world's rice area is grown under rainfed conditions, either in fully aerobic soils or where the soil is saturated for only part of the season in some years. Because of the much greater risk of crop failure in these areas, farmers apply minimum levels of inputs, and yield gains associated with sowing improved cultivars have been much less dramatic than in the favorable areas. The adoption of improved cultivars has been much slower in rainfed environments. Nonetheless, there are active rice breeding programs for rainfed environments. Many improved cultivars have outperformed traditional types in national testing systems and have been of®cially released (Chaudhary et al., 1998). In the rainfed lowland system, rice is generally transplanted into puddled soil, like in irrigated lowland systems, though direct seeding is used in some places (Mackill et al., 1996). In a good season, rainfall is adequate to maintain 5±20 cm of standing water in the ®eld throughout the season. In many seasons, however, rainfall is excessive and the crop suffers from submergence, or rainfall is inadequate and the soil dries out to some extent. The diversity of rainfed lowland environments and their interaction with genotypes has been documented (Wade et al., 1999). Improved cultivars that have been successful in this system were generally targeted for ®elds with shallow or intermediate water depths and are mostly of intermediate height and have reduced photoperiod sensitivity compared to traditional types. The most successful rainfed lowland improved variety, however, is characterized primarily by its productivity under low-inputs and good grain quality (`Mahsuri', Mackill et al., 1996). The tall plant type of Mahsuri and its poor response to applied fertilizer are in sharp contrast to the traits that made semi-dwarf cultivars successful in the irrigated lowlands. Efforts to understand the physiological basis of improved performance in rainfed lowland systems are reported elsewhere (e.g., Fukai et al., 1999). The non-¯ooded (aerobic) rice area comprises two major systems: the low-input, mainly subsistence systems of Asia, and a high-input, market-integrated system that is found in Brazil and that is emerging in water-limited areas of China. The low-input system includes both sedentary cultivation in South Asia and shifting cultivation in hilly Southeast Asia (Courtois and La®tte, 1999). Many improved cultivars have been

developed for these systems, but traditional cultivars still dominate the area. The high-input system in Brazil has developed as a function of the availability of improved, responsive cultivars combined with management practices that reduce the risk of production in aerobic soils, including a shift to less drought-prone areas (GuimaraÄes and Stone, 2002). In China, the high-input system is replacing lowland rice in areas where water scarcity makes lowland rice uneconomic (Wang and Tang, 2002). This paper will concentrate on rice grown in aerobic systems. We are not aware of published reports of any rice cultivars that consistently grow better in aerobic soil than in ¯ooded soil if lodging is prevented, though some upland cultivars tolerate transplanting poorly. It is generally concluded that the aerobic situation in itself implies a low level of stress for rice, particularly if the relative humidity is low (Dingkuhn et al., 1989). As soil moisture declines further below ®eld capacity, moisture stress increases. In addition to soil water availability, other factors that differ in aerobic soils are soil mechanical impedance, oxygen supply to roots, the accumulation of gases such as ethylene and CO2 in the root tissue and stem base, the nature of the N source (nitrate replacing ammonia), and activity of soil fauna (Sanchez, 1976; Voesenek and van der Veen, 1994). In ¯ooded soils, roots develop in a super®cial mat, facilitating absorption of nutrients from the ¯oodwater, while in aerobic soils root growth is more dispersed (Yoshida, 1981). In some droughttolerant cultivars, water de®cit results in root development into deeper soil layers and an increase in the root±shoot ratio (e.g., BanÄoc et al., 2000). Resources used for greater root growth and maintenance in aerobic soils are not available to support shoot growth, and this competition for photosynthate may also be responsible for lower productivity in aerobic systems. Our objectives are: 1. Describe the comparative performance of improved and traditional cultivars across a range of low-input aerobic yield trials in Southeast Asia and their interactions with environmental factors. 2. Examine the basis of cultivar differences in adaptation to higher-input aerobic environments. 3. Summarize available data on genetic regions associated with aerobic adaptation and increased stress tolerance in rice.

H.R. Lafitte et al. / Field Crops Research 75 (2002) 171±190

2. Genetic yield gains in unfavorable upland rice environments A multilocation testing system for the infertile, acid uplands of Southeast Asia has been ongoing at IRRI since 1986. Lines evaluated under this system include indica, japonica, aus, and intermediate types (for a description of rice sub-species, see Mackill et al., 1996). In order to evaluate the interactions between different lines and environments, we conducted pattern analyses for two subsets of data: (1) a group of 39 lines that had been evaluated in at least 10 of 43 trials, with any trial containing at least 12 of the entries; and (2) a subset of 22 breeding lines that had been evaluated in 18 trials for which meteorological data were

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generally available. Site and line details are indicated in Tables 1±4. We used IRRISTAT software to conduct the analyses (IRRI, 2000). Pattern analysis of standardized data was used, with both site and cultivar main effects removed (McLaren, 1996). This grouped the entries and allowed better handling of missing data than a regular genotype-by-environment analysis. The resulting data provide information on the interaction between lines and environments, rather than information on overall performance. In data set 1, 44% of the entry-by-site data matrix was ®lled. Two of the entries were traditional varieties (Dinorado and Azucena; Table 1), and the others were improved lines from upland rice breeding programs in the Philippines, Brazil, Colombia, or India. Average

Table 1 Upland cultivars and breeding lines included in 43 yield trials conducted in Southeast Asiaa Group

Genotypes

1 2 3 4 5 6 7 8 9

UPL RI-7 (1), IR57924-24 (1) IRAT 190 (6), IRAT 212 (6) IR55433-63 (1), IR60080-45 (6), CNA 4121 (6), IDSA 06 (6) IRAT 144 (6), IR60080-46A (6), IR60080-49 (6), L 081-40 (6) H.D.1.4 (6), CNA 4136 (6) DINORADO (6), UPL RI-5 (1) IR57924-08 (1), IR57924-09 (1), B 2997C-TB-4(1), CT 6510-24-1-2 (1), CT 6510-24-1-3 (1) AZUCENA (6), IRAT 216 (6), IR55411-50 (6), IR55549-01-2 (na), AUS 196 (2) IR47686-06-0 (6), IR47686-09-1 (6), IR47686-09-2 (6), IR47686-12-5 (6), IR47686-13-1 (6), IR47686-18-7 (6), IR4768631-1 (6), IR55419-04 (1), IR60080-01A (6), IR60080-42 (6), IR60080-47 (6), IR60080-48 (6), CT 6516-20-1 (6)

a The group number was identi®ed by pattern analysis and is used to identify cultivars in Fig. 1. The number in parenthesis indicates isozyme group (1: indica; 2: aus; 6: japonica).

Table 2 Details of experiments with large interaction terms out of a set of 43 experiments in Southeast Asiaa Code

Location

Year

Average yield (Mg/ha)

pH

Other

C1 C2 C4 C6 C9 I4 IRRI drt L1 L9 LA M6

Cavinti, Philippines Cavinti, Philippines Cavinti, Philippines Cavinti, Philippines Cavinti, Philippines Ilagan, Philippines IRRI, Philippines Clavaria, Philippines Clavaria, Philippines Clavaria, Philippines Matalom, Philippines

1988 1988 1989 1990 1991 1990 1989 1989 1991 1990 1990

2.00 0.74 1.32 1.79 0.94 1.03 1.65 1.55 1.40 0.90 0.32

4.0 4.0 4.0 4.0 4.0 5.3 6.0 5.0 5.0 5.0 4.5

P added No P added No fertilizer added No fertilizer added Fertilizer added (60±30±20); blast No P added Dry season drought screen P added No fertilizer added No fertilizer added; low rain month 3 No fertilizer added

a

The code is used to identify the experiments in Fig. 1.

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Table 3 Upland cultivars and breeding lines included in 16 yield trials conducted in different sites in Southeast Asia Entry

Name

Isozyme groupa

Average grain yield

Days to anthesis

Leaf drying scoreb

Average blast scorec

Leaf rolling scored

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

UPL RI-5 IRAT 216 IR47686-12-5 IR53236-342 IR55411-50 IR55419-04 IR57924-24 IR60080-01A IR60080-42 IR60080-45 IR60080-46A IR60080-47 IR60080-48 IR60081-15 IR62752-07 IR62761-20 IR63371-38 IR63372-15 IR63374-16 IR63377-08 IR63380-08 CT 6510-24-1

1 6 6 6 1 1 1 6 6 6 6 6 6 6 6 6 6 6 6 6 6 1

1.03 1.28 1.21 1.38 1.53 1.73 1.63 1.57 1.36 1.56 1.74 1.43 1.37 1.49 1.59 1.60 1.46 1.74 1.38 1.48 1.60 1.23

94 84 83 62 84 78 81 83 80 84 82 83 84 ± 82 81 80 82 82 80 79 81

2.9 2.3 1.8 3.0 3.5 3.5 4.0 ± 5.0 4.0 3.0 ± 3.0 3.0 3.0 3.0 3.0 4.0 5.0 4.0 4.0 1.3

2 2 2 4 3 2 3 6 2 2 3 5 2 1 2 3 2 1 2 1 1 2

5 1 2 2 5 5 5 ± 1 1 2 2 1 ± 1 0 0 0 0 0 0 5

a

Sozyme group 1 corresponds to indica types, group 6 corresponds to japonica types. Leaf drying score collected at soil moisture of 0.5 MPa at vegetative stage; 1: no leaf drying, 5: one-fourth to one-half of all leaves fully dried. c Average blast score for line in all experiments where it was evaluated; 1: resistant, 6: susceptible. d Data from internal IRRI report written by G. san Valentin, leaf rolling measured 69 days after sowing in Indonesia; 0: unrolled, 5: rolled. b

Table 4 Sites where yield trials were conducteda Code

Site

Year

Rain Rain Rain Rain Rain Rain month 1 month 2 month 3 month 4 month 5 total

Radiation month 3

Soil pH

Average yield

Maximum Yield yield S.D.

C1 C2 C3 C4 G1 M1 S1 L1 L2 C5 S2 S3 C6 V1 T1 U1

Cavinte, Philippines Cavinte, Philippines Cavinte, Philippines Cavinte, Philippines San Miguel Matalom, Philippines Sitiung, Indonesia Clavaria, Philippines Clavaria, Philippines Cavinte, Philippines Sitiung, Indonesia Sitiung, Indonesia Cavinte, Philippines Bac Thai, Vietnam Sto. Tomas, Philippines Ubay, Philippines

1990 1991 1991 1992 1991 1991 1990 1991 1990 1993 1993 1994 1995 1995 1990 1992

380 500 500 178 ± 319 49 97 227 287 200 287 431 389 346 69

14822 12770 12770 15188 ± 13855 ± 19762 19735 18100 ± ± 14500 ± 14015 16646

4.0 4.0 4.0 4.0 4.0 4.5 4.0 5.0 5.0 4.0 4.0 4.0 4.0 4.0 5.2 4.0

1.85 1.62 1.46 0.87 1.69 0.45 2.94 1.50 0.93 1.79 1.61 2.15 1.53 2.11 0.80 0.61

3.00 2.38 2.70 1.12 2.61 0.67 4.08 2.25 2.53 2.96 3.01 2.88 3.51 3.41 1.20 1.00

243 302 302 625 ± 273 440 249 226 430 320 123 479 526 255 218

425 503 503 393 ± 511 450 157 156 231 200 237 277 633 410 123

245 260 260 349 ± 75 340 113 258 194 25 441 871 63 206 141

655 202 202 379 ± 136 55 332 373 649 ± 310 640 40 ± 234

1293 1565 1565 1545 ± 1179 1279 616 868 1142 745 1088 2058 1611 1217 551

0.64 0.33 0.53 0.22 0.49 0.12 0.86 0.34 0.54 0.60 0.64 0.56 0.72 0.75 0.27 0.24

a Rain month x indicates millimeters of rainfall recorded in the x month of the season. Radiation month 3 is the total amount of solar radiation received in the third month after sowing, with units of MJ m 2. The symbol ` ' indicates data were not available.

H.R. Lafitte et al. / Field Crops Research 75 (2002) 171±190

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Fig. 1. AMMI biplot of ®rst two principal components axes for grain yield of upland cultivars and breeding lines grown in Southeast Asia in low-fertility experiments, mostly at sites with acid soils. Groups 1 and 7 have large PCA1 and these are indica types. Group 4 includes improved japonica types. Group 8 includes indica, aus and japonica entries. Group 8 includes the traditional cultivar Azucena, and the other traditional cultivar, Dinorado, is in Group 6. Additional details are in Tables 1 and 2.

yield across the environments was 1 Mg/ha. The environment groupings delineated different soil types (Fig. 1), particularly separating those with pH below 5 from less acid sites along the ®rst principal component axis (PCA1; negative PCA1 indicates more acid soil). Sites with greater interactions were not necessarily higher-yielding, but had greater standard deviations for yield. Individual entry averages for yield ranged from 0.7 to 1.4 Mg/ha (Table 2). The two traditional cultivars had the lowest average yields, but the traditional types did not present fundamentally different patterns of interaction with environment than the other lines. The traditional japonica cultivar Azucena interacted with environments in a similar manner to the improved indica breeding lines IR55411-50 and IR55549-01-2 and the improved japonica cultivar IRAT216. The traditional japonica cultivar Dinorado interacted with environments in a manner similar to the improved indica cultivar UPLRi-5. The patterns of

interaction did not clearly separate indica and japonica entries, but both PCA1 and PCA 2 were correlated with isozyme group at about r ˆ 0:5 (positive for PCA1, negative for PCA2), giving a predominance of indica types with interaction scores falling in the lower right quadrant in Fig. 1. There was a tendency for positive interactions between indica types and higher-yielding sites. Sister lines mostly grouped together. Crop duration varied among lines and this trait was signi®cantly correlated with PCA1 …r ˆ 0:40 †. We conclude from this analysis that traditional cultivars and improved lines had similar patterns of interaction with environment, and that indica types tended to interact positively with the less acid soil environments. In the second data set, 67% of the matrix was ®lled. The 33 entries represented primarily progenies of indica-by-indica and japonica-by-japonica crosses, and did not include traditional cultivars (Table 3).

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With two exceptions (UPL Ri-5 and IR53236-342), the lines had very similar duration. These lines were evaluated in 16 experiments (Table 4). Sites accounted for 50% of the total sum of squares, lines accounted for only 2.5%, and the remainder was due to line-bysite interaction. This decomposition of variance is fairly typical for multisite upland trials (B. Courtois, unpublished data). The ®rst two principal components axes in the ordination analysis explained 32 and 20% of the genotype-by-site sum of squares. Some characteristics of the environments were signi®cantly correlated with principal components axes (r-value required for signi®cance at P < 0:05 ˆ 0:46). Higher-yielding sites had larger values of PCA1 …r ˆ 0:63†, and this axis was correlated with rainfall received in month 2 (the month after planting;

r ˆ 0:46). The second principal component was related to amount of solar radiation received in the third month after planting …r ˆ 0:90†, and was negatively correlated with total rainfall …r ˆ 0:65†, especially rainfall received in the month of planting …r ˆ 0:77†. The AMMI2 biplot (Fig. 2) can be divided into four quadrants that can be roughly described as: (1) sites with low rainfall in months 1±3 and high radiation near ¯owering; (2) sites with high rainfall in the month of planting, low rainfall in the second month, and low radiation around ¯owering, (3) sites with high rainfall in both months 1 and 2 but low radiation near ¯owering; and (4) sites with less rain in the month of planting but adequate rainfall in the second month and high radiation near ¯owering. PCA3 accounted for 14% of the sum of squares. It was

Fig. 2. AMMI biplot of ®rst two principal components axes for grain yield of upland cultivars and breeding lines grown in the Philippines in low-fertility experiments, mostly at sites with acid soils. Site and line identi®cation is in Tables 3 and 4.

H.R. Lafitte et al. / Field Crops Research 75 (2002) 171±190

strongly negatively correlated with radiation received in month 3 …r ˆ 0:83†, independent of rainfall. Few genotype characteristics were signi®cantly correlated with principal components axes in this analysis (r-value for signi®cance at P < 0:05 ˆ 0:40). Yield differences in these experiments may re¯ect variation in disease or pest resistance rather than physiological differences. Rice blast, caused by the fungus Pyricularia grisea, is a particularly important constraint, especially in dry years, in acid soils like those of Sumatra, or in high nitrogen input environments (Zeigler et al., 1994). The average blast score (higher score indicating more severe disease symptoms) for entries across sites was positively correlated with PCA1 …r ˆ 0:43†. PCA2 was correlated with the number of productive tillers per plant …r ˆ 0:46†. PCA3 was correlated with leaf rolling score under drought measured near ¯owering in Indonesia …r ˆ 0:46†, but was not associated with the drought score collected in IRRI's standard screening system, where young plants are scored at a soil water potential of 0.5 MPa. Many rice genotypes have been screened for the ability to maintain green leaf area in a seedling screen conducted in the dry season at IRRI (De Datta et al., 1988). Scores from this standard screening system were not correlated with any principal component axis in this set of lines and environments. Standard screening system scores were signi®cantly correlated with yield measured in two drought-affected sites (M1 and U1), but the correlation was not in the expected direction. PCA3 was correlated with ¯owering date …r ˆ 0:43†. PCA4 was correlated with spikelet fertility recorded at Sitiung …r ˆ 0:60†; this PCA explained 12% of the tabular sum of squares. Genotypes that showed signi®cant interaction in Quadrant 1 might be considered tolerant of water de®cit, though vegetative drought screening scores did not indicate this. Those lines had fairly low maximum yields but were resistant to blast. Genotypes in Quadrant 2 had greater tiller number, but low maximum yields. Those in Quadrant 3 were more susceptible to blast, but responded well to high rainfall, tolerated low radiation near ¯owering and had high maximum yields. Quadrant 4 lines had the greatest maximum yields of all groups, and interacted positively with high radiation environments, but their average yields were low. It is interesting to note that many successful breeding lines, which have been advanced in the breeding program, are from Quadrant

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3. This indicates that the ability to respond to high rainfall in the vegetative period and to tolerate low radiation around ¯owering is important for low-input, acid soil systems in the humid tropics. We conclude that in the low-input, acid soil upland environment, improved yield potential with limited inputs represents the most important crop improvement goal, followed by durable disease resistance. The genetic basis of improved disease resistance has been examined through QTL analysis (e.g., Wang et al., 1994), and molecular methods to accelerate progress in disease resistance are emerging (Zeigler et al., 1994). No clear differences were found between interaction patterns for indica versus japonica lines, or for traditional versus improved cultivars. A system of multilocation yield testing, combined with improved use of host plant disease resistance, is expected to be effective for continued varietal improvement for this unfavorable environment where water availability is not the major constraint. Patterns of rainfall clearly in¯uence performance, but it is dif®cult to pinpoint a single period that is most critical in in¯uencing yield across these environments. A breeding goal should be stable performance across a range of water de®cit scenarios; thus, multilocation testing in the target region appears to be a suitable strategy for sampling realistic water de®cits. Rice is more tolerant to low soil pH than most other crops, but soil acidity still affects yield. As our understanding of the genetic basis of tolerance to acid and infertile soils improves, mechanism-based screening for tolerance to that constraint may become possible (Kirk et al., 1998). Low radiation near ¯owering may be another signi®cant abiotic factor that affects yield, and genetic improvement for shading tolerance may be worthwhile. Weed competitiveness is another desirable trait in aerobic rice, and this characteristic has been improved by breeding programs in West Africa. Genetic variation for speci®c leaf area (SLA) (cm2/g leaf) exists, and the African rice species O. glaberrima is noted for its early vigor and high SLA (Dingkuhn et al., 1999). Interspeci®c crosses have been made and high SLA progeny have been identi®ed (Dingkuhn et al., 1998). Early in the season, these hybrids have thin, lax leaves than help suppress weed growth, but as the plant develops over the season the leaves become thicker and more erect, allowing light penetration into the canopy.

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3. Yield in favorable aerobic environments In environments where soil conditions are favorable and soil fertility can be enhanced, different opportunities exist for improving aerobic rice performance. It should be possible to duplicate much of the improvement in yield potential that has taken place in lowland systems. In order to achieve this ef®ciently, we need to understand how growth changes when a

crop is moved from a lowland paddy ®eld to an aerobic ®eld. Very limited data are available to directly compare lowland and aerobic performance in improved cultivars. In order to examine the basis of superior performance in high-input aerobic environments, we evaluated eight cultivars (Table 5) across several seasons and cultivation systems (Table 6). The experiments represented a range of contrasting conditions in terms of N availability, water and solar

Table 5 Rice genotypes evaluated in a range of seasons and management systems at the IRRI experiment station, Los Banos, Philippinesa Cultivar/line

Description

Days to anthesisb

Average yield (Mg/ha)

Country of origin

(1) (2) (3) (4) (5) (6) (7) (8)

Traditional japonica upland Improved indica upland Improved japonica upland Improved japonica upland Improved japonica upland Improved indica upland Improved indica upland Improved indica lowland

89 78 78 76 82 82 77 83

1.4 2.1 2.2 2.4 1.8 3.4 3.2 2.6

Philippines Indonesia Philippines Philippines Ivory Coast Philippines Philippines Philippines

Azucena B6144 IR60080-46A IR65907-188-1-B IRAT 104 IR55423-01 IR55435-05 IR72 a b

Data for Cultivars 1 and 8 have been reported elsewhere (La®tte and Courtois, 2001). Days from sowing to anthesis recorded in 97WS, lowland ®eld.

Table 6 Details of experiments to evaluate performance of eight rice genotypes in non-acid soils with applied fertilizera Season/water

Cultivation system

Water management

N applied (kg/ha)

Average yield (Mg/ha)

Comments

WS 97/1

Lowland, dry direct seeded

105

3.7

WS 97/2

Aerobic

75

3.1

WS 97/3

Aerobic

75

1.8

WS 98/2

Aerobic

60

2.4

High percolation rate; apparent N loss requiring additional fertilizer application First season of cultivation after >5 years fallow As above, but limited midseason rainfall (total of 61 mm 63±90 DAS) Lower radiation than in 97WS

DS 99/1

Lowland, wet direct seeded

110

1.9

Severe stem borer damage or lodging in susceptible entries

DS 99/2

Aerobic

Flash flooding for establishment (28 DAS), then standing water for rest of season Rainfall ‡ sprinkler irrigation when soil moisture tension < 20 kPa Sprinkler irrigation for establishment, then rainfed (1010 mm rainfall during the season) Rainfall ‡ sprinkler irrigation when soil moisture tension < 20 kPa Flash flooding for establishment (22 DAS), then standing water for rest of season Drip irrigation 3 per week to apply 1.6 pan evaporation

110

1.9

DS 99/3

Aerobic

Drip irrigation 3 per week to apply 1.6 pan evaporation except for period 8 days to flowering

110

1.8

Severe stem borer damage in susceptible entries; second year of cultivation; possibly nematodes As above

a All experiments were conducted at the IRRI experiment station, Los Banos, Philippines. WS: wet season (June sowing date), DS: dry season (January sowing date). Water level: lowland (1); well-watered aerobic (2); aerobic with water de®cit (3).

H.R. Lafitte et al. / Field Crops Research 75 (2002) 171±190

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Fig. 3. Grain yield of eight rice cultivars versus the average grain yield in the experiment. All experiments were conducted at IRRI, Philippines, with details as given in Table 6. The order of sites plotted on the x-axis is: 97/3, 99/3, 99/2, 99/1, 98/2, 97/2, 97/1 (site codes as in Table 6). `LSDW' is the appropriate LSD at P < 0:05 to compare cultivars within an experiment, and `LSDA' is the appropriate LSD at P < 0:05 to compare cultivars across experiments.

radiation regimes, and pest pressure. We measured leaf area and aboveground biomass production at anthesis, ®nal grain and biomass production, and yield components. Two improved indica upland lines, IR55423 and IR55435, produced the greatest yields across sites (Fig. 3). The interaction between experiment and cultivar was highly signi®cant. The lowland cultivar IR72 differed from the other entries in that it was very negatively affected by water de®cit in 1997 and because it was able to yield very well in the high N lowland environment in 1999. The japonica cultivars yielded very poorly in the 1999 dry season, when severe stem borer damage occurred, and several entries had to be dropped from the analysis. We have observed that tropical japonica cultivars tend to be much more severely affected by stem borers than indica types at the IRRI experiment station, and high N levels exacerbate the problem (Zhu et al., 2002). The high-yielding lines were characterized by consistently high numbers of panicles per square meter,

though panicle number was much lower than in the lowland cultivar IR72 (Fig. 4a). While panicle number differed signi®cantly across environments, cultivars responded to environments in a similar way and the interaction between cultivar and experiment was not signi®cant. Rice cultivars are conceptually divided into two classes: panicle weight types with a large number of spikelets per panicle and heavy grains, and panicle number types, with many panicles per square meter (Mackill et al., 1996). Tropical japonica cultivars tend to be panicle weight types, and indica cultivars are generally panicle number types. Factors that vary among cultivars and in¯uence ®nal panicle number per square meter include initial number of plants established, tillers per plant, and the fraction of tillers that produce panicles. We have found that aus and indica cultivars generally establish more plants per seed sown in our conditions at IRRI. In the 1997 study, IRAT104 had unusually low numbers of plants established 1 month after sowing, and IR55423 and IR72 had greater than average numbers. In that study,

180

H.R. Lafitte et al. / Field Crops Research 75 (2002) 171±190

Fig. 4. Panicle number per square meter (a) and harvest index (b) of eight rice cultivars measured in experiments conducted at IRRI, Philippines. `LSDW' is the appropriate LSD at P < 0:05 to compare cultivars within an experiment, and `LSDA' is the appropriate LSD at P < 0:05 to compare cultivars across experiments.

differences in biomass accumulation and leaf area development were detected by 28 days after sowing, and IR65907 and IRAT104 had below-average values (data not shown). The two cultivars with superior yield in the end were not, however, different to the remaining cultivars in terms of the number of plants established, meaning that a large number of established plants is necessary but not suf®cient for good overall

performance. In aerobic ®elds with seeding rates of 60±80 kg/ha, upland tropical japonica cultivars produce an average of 2.1 tillers/plant. Upland indica cultivars generally produce more, up to 4 tillers/plant, but some improved japonica types like IR60080 can produce similar numbers (data not shown). In all wet season experiments the fraction of fertile tillers was high and similar among varieties.

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A critical feature for superior yield in favorable aerobic environments is the ability to maintain harvest index at a similar level as in lowland ®elds. Harvest index varied widely across environments, cultivars differed in harvest index, and cultivar interacted strongly with experiment for this trait (Fig. 4b). High harvest indices were achieved in the N-limited lowland experiment in 1997. Low values were recorded in both the drought-stressed rainfed experiment in 1997, where moisture stress occurred for about 14 days before ¯owering, and in the high N lowland experiment in 1999, where most cultivars produced excessive spikelet numbers and a large proportion of spikelets were sterile. Only IR72 maintained high harvest index in both lowland experiments, indicating an appropriate balance between leaf area and spikelet number. Variation in harvest index re¯ected signi®cant differences in all relevant yield components: spikelets per panicle, the fraction of sterile spikelets, and weight per grain (data not shown). The interaction between line and environment was signi®cant for each of these traits. The lines IR55423 and to a lesser extent, IR55435, produced many spikelets per panicle and a relatively large fraction of them were fertile. The high-tillering cultivar IR72 produced many small panicles in the aerobic 97WS stress experiment, with only 44 spikelets each, while the other entries produced 71±98 spikelets per panicle. The weight per grain of IR72 was similar to other indica cultivars in most environments, but was particularly low under stress in the rainfed experiment in 1997. These results indicate a range of patterns of yield component elaboration and compensation among this limited sample of rice cultivars. The ability to maintain yield in aerobic soils was not clearly related to vegetative growth. Across experiments, IR72 produced below-average leaf area by the time of anthesis and it was considerably shorter in height than other entries, but the total amount of aboveground biomass IR72 produced by anthesis in unstressed aerobic experiments was not signi®cantly different to the other entries (Fig. 5a and b). While cultivars differed in LAI at anthesis, the interaction between cultivar and experiment was not signi®cant …P < 0:11†. Both biomass and LAI were low in the aerobic ®elds in the 1999 dry season for all cultivars, despite the high levels of N and ample water provided (data not shown). This is consistent with our

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observations of rather low yield potential for aerobic cultivation systems in the IRRI dry season, but may also re¯ect a crop rotation effect. Aerobic rice yields have been found to decline sharply with successive years of cultivation (e.g., GuimaraÄes and Yokoyama, 1998). In some instances, though not all, the decline has been related to an increase in the numbers of root±knot nematodes (Meloidogyne graminicola). The numbers of this pest reached problem levels in the aerobic ®eld by the end of the 1999 dry season. That experiment had reduced plant height and leaf area, but there was less of an effect on tillering. The lowland cultivar IR72 has a very bunchy appearance in aerobic soils, which in our experiments was mainly due to reduced height in a high-tillering plant type rather than a direct increase in tillering or changes in LAI. Similar observations have been made for other lowland cultivars grown in aerobic soils. Upland cultivars have less extensive tillering in both lowland and aerobic soils, but they do not appear to differ fundamentally in the response of leaf area to ¯ooding. The superior upland cultivars IR55423 and IR55435 were distinguished, not by greater early biomass accumulation, but by greater stability across environments of the amount of biomass produced by ¯owering (Fig. 5a). These entries were not noticeably less variable in height across environments than other cultivars. Growth habit and partitioning in the highly plastic lowland rice plant are generally controlled largely by cultural practices (plant spacing, fertility regime; Yoshida, 1981) and environmental conditions (radiation, temperature; Horie, 2001). Such factors are more easily controlled in paddy ®elds, where water is not a limitation, uniform plant stands are achieved through transplanting, and spectral quality and microclimate are stabilized by the ¯oodwater. For aerobic systems, these factors are much more dynamic. Superior germplasm may be characterized by the ability to maintain the desired plant type and partitioning patterns despite ¯uctuations in the environment. Other traits that are more particularly related to water uptake or loss, such as root growth or stomatal behavior, are expected to become more important as water de®cit intensi®es. It is not yet clear what environmental signals result in reduced harvest index in aerobic soils. This reduction is seen even when the soil is maintained near ®eld capacity, suggesting that water availability alone may

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Fig. 5. Aboveground biomass measured at anthesis (a) and leaf area index at anthesis (b) for eight rice cultivars measured in experiments conducted at IRRI, Philippines. LAI was measured destructively in all experiments except 98WS, when it was measured by radiation interception. `LSDW' is the appropriate LSD at P < 0:05 to compare cultivars within an experiment, and `LSDA' is the appropriate LSD at P < 0:05 to compare cultivars across experiments.

not provide a full explanation. Even when the soil is well-watered, surface drying occurs between irrigations, and roots in that zone may experience transient water stress, possibly promoting the production of root signals that in¯uence shoot growth and dry matter distribution.

It is clear that improving the aerobic adaptation of a rice cultivar implies more than just achieving the correct plant height in a traditional upland plant type or in a lowland semi-dwarf plant type. The underlying pattern of partitioning between roots and shoots, and between leaves, stems, and reproductive structures,

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must be redesigned to maximize grain production. Partitioning must be stable across a broader range of environmental ¯uctuation than is generally found in lowland rice environments. Plant breeders in both Brazil and China have achieved signi®cant yield improvements for aerobic systems by crossing highyielding indica and japonica cultivars and then selecting for grain yield and input responsiveness (Pinheiro and de Castro, 2002; Wang and Tang, 2002). These programs have resulted in cultivars characterized by intermediate height and tillering, which produce high yields in favorable aerobic rice environments. Yields of these cultivars greatly exceed yields of traditional upland cultivars, but they generally are lower than for adapted cultivars grown under lowland conditions in the same region. In aerobic environments with less reliable rainfall or where supplemental irrigation is not available, additional drought tolerance is required. 4. Genetic regions associated with aerobic adaptation Adaptation to favorable upland environments is apparent in the effects of aerobic conditions on leaf area and the maintenance of harvest index. Differences among cultivars are large, suggesting large genetic effects. A number of mapping populations have been developed in rice between lowland and upland-adapted parents. These populations have been used to study the genetic control of disease resistance (Wang et al., 1994) and plant height and yield components in lowland environments (Courtois et al., 1995; Huang et al., 1996). Mapping populations have also been evaluated for putative drought-adaptive traits such as root morphology (Champoux et al., 1995; Yadav et al., 1997; Price and Tomos, 1997; Ali et al., 2000), root penetration through compacted layers (Ray et al., 1996; Price et al., 2000; Zheng et al., 2000), osmotic adjustment (Lilley et al., 1996), and leaf drying under vegetative stage water de®cit (Courtois et al., 2000). Several of the QTLs identi®ed for root length are consistent across mapping populations (Price and Courtois, 1999), and common genomic regions across populations and even across species have been identi®ed for root thickness, root penetration, and stomatal behavior (Zhang et al., 2001). For several of these populations, studies are underway to

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establish the relationship between individual traits and grain yield under water de®cit. Data are available on the comparative performance of lines in lowland versus aerobic environments for a population of doubled haploid lines developed by crossing Azucena and IR64, a lowland semi-dwarf cultivar (Table 7; population described by Huang et al., 1996). A subset of about 85 lines was used in these experiments in order to restrict the range of ¯owering dates and minimize the genetic sterility common in crosses between indica and japonica cultivars. Average yields were greatest in the lowland environment, followed by the sprinkler-irrigated control experiment in 1995. Grain yields in aerobic experiments tended to be low, re¯ecting the poor adaptation of IR64 to aerobic conditions and the low yield potential of the traditional cultivar Azucena. Correlations between the lowland experiment and the aerobic experiments were highly signi®cant for ¯owering date, plant height, panicle length and weight per grain (Table 8). Correlations for tiller number and spikelets per panicle were also signi®cant, but the correlations were much weaker for the percentage of sterile spikelets and for grain yield. In all aerobic experiments, the yield component most closely correlated with yield was the percentage of sterile grains (data not shown). This might be expected for the stress treatments, because stress was imposed near ¯owering when the number of tillers and spikelet number had already been established, but a signi®cant correlation was found in the well-watered plots as well. One possible explanation for this is the extreme sensitivity of rice to water de®cit imposed at ¯owering (Cruz and O'Toole, 1984; O'Toole, 1982). The aerobic control environment may have been adequate to supply water needs during the less sensitive stages of crop development, when tiller number and spikelets per panicle were determined, but not enough to avoid stress at ¯owering. Another explanation is a high level of partial sterility of some of the lines, which is a phenomenon generally observed in the progeny of indica by japonica crosses. The correlation between spikelet sterility and grain yield in the lowland experiment was also signi®cant (r ˆ 0:43, P < 0:01), indicating the possible importance of genetic sterility, even though the average level of sterility (22%) was not unusually large in the lowland experiment. The development of mapping populations within each subspecies would help

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Table 7 Performance of Azucena, IR64 and doubled haploid lines from an IR64/Azucena mapping population in a lowland experiment and in six upland experimentsa Experiment

Entry

A50b (days)

PHc (cm)

Pan/m2d

SPPe

%sterf

TGWg (g)

Yield (Mg/ha)

94 lowland

Azucena IR64 DHLs Azucena IR64 DHLs Azucena IR64 DHLs Azucena IR64 DHLs Azucena IR64 DHLs Azucena IR64 DHLs Azucena IR64 DHLs

102 74 99 102 88 99 100 91 100 94 85 91 100 96 103 90 87 94 101 93 96

142 74 103 122 67 84 ± ± ± 116 82 94 90 60 78 133 68 88 124 69 86

105 235 152 228 620 318 232 488 299 200 344 387 262 400 355 155 482 264 183 358 258

178 110 152 115 94 103 153 92 111 55 47 56 68 42 58 64 50 69 46 53 74

16 6 22 18 26 45 33 36 62 69 53 69 79 75 79 49 51 53 48 41 63

30.1 26.0 26.4 26.7 24.6 23.1 26.5 20.8 21.9 29.5 23.1 23.9 27.6 18.7 21.7 24.5 21.2 19.9 23.4 20.0 18.7

2.8 3.4 2.3 1.5 2.8 1.1 1.0 0.8 0.5 0.7 0.7 0.7 ± ± 0.3 0.8 2.2 1.3 0.8 1.7 0.8

95 control 95 stress 98 control 98 stress 99 control 99 stress

a

Details of water treatments are shown in Table 8. Days from sowing to anthesis. c Plant height. d Panicles per square meter. e Spikelets per panicle. f Percentage of spikelets that did not form grains. g Weight of 1000 grains. b

dissociate what portion of the observed spikelet sterility is due to the genetic distance between parents from what is due to stress. Data from the lowland evaluation and the aerobic experiments were subjected to QTL analysis (1994 data reported in Courtois et al., 1995 and 1998 data reported in La®tte and Courtois, 2000, 1999 data unpublished) using QTLMapper 1.0 (Wang et al., 1999). All QTLs that were identi®ed in two or more aerobic experiments were also detected in the lowland experiment (Table 9). The effect of the IR64 allele at a given location was consistent across environments. The in¯uence of IR64 alleles in the region where the recessive semi-dwarf gene sd1 has been mapped (interval RG690-RG730; Huang et al., 1996) was very clear in the aerobic experiments. The sd1 gene leads to reduced levels of gibberelic acid, which affects internode elongation along with a number of other traits

(Xia et al., 1991; Courtois et al., 1995). The effect of the IR64 allele in this region on yield in aerobic ®elds was positive. This result is unexpected given the poor performance of the semi-dwarf cultivar IR72 and most other semi-dwarf types in water-limited aerobic environments. This region on Chromosome 1 also includes QTLs for root depth and thickness (Yadav et al., 1997) and for other traits related to the ability of the line to tolerate vegetative drought stress, such as leaf drying scores and leaf relative water content (Courtois et al., 2000). The reported effect of the IR64 allele was to decrease root depth, root thickness, and leaf drying. The ability to retain green leaf area under stress was associated with the smaller size of lines with the IR64 allele at the onset of stress. In light of the low precision of QTL identi®cation in a subset of 80 lines, it is not possible to conclude that it is the presence of sd1 that improves line performance in aerobic environments,

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Table 8 Correlations between traits measured in the 1994 lowland experiment and in different aerobic environments for a set of doubled-haploid lines of IR64/Azucenaa 1995

Trait Days to anthesis Number of lines Plant height Number of lines Panicle length Number of lines Tillers/m2 Number of lines Spikelets/panicle Number of lines Sterility (%) Number of lines Weight/grain Number of lines Grain yield Number of lines

1998

1999

Control, sprinkler-irrigated 3 per week

Stress, water withheld for 10 days at anthesis, then irrigated lightly 2 per week

Control, furrow irrigated 2 per week; high sowing rate

Stress, water withheld for two 2-week periods, flowering

Control, drip irrigated 3 per week

Stress, water withheld for 14 days, flowering

0.78 68 0.88 68 0.84 68 0.48 68 0.49 68 0.49 68 0.80 68 0.28 68

0.69 68 ±

0.81 50 0.75 50 0.77 50 0.39 50 0.62 50 0.38 50 0.86 50 0.13NS 50

0.83 28 0.83 27 0.57 27 0.22NS 28 0.54 28 0.66 28 0.68 28 0.10NS 28

0.78 67 0.79 67 0.77 67 0.54 60 0.42 60 0.35 60 0.68 60 0.41 60

0.71 65 0.75 64 0.81 64 0.62 57 0.43 57 0.42 58 0.64 58 0.31 58

± 0.40 68 0.68 68 0.21NS 68 0.58 67 0.01NS 68

a All experiments were conducted at the IRRI experiment station, Los Banos, Philippines. All correlations are signi®cant at P < 0:01 unless noted as P < 0:05 () or not signi®cant (NS).

Table 9 QTLs identi®ed for plant characteristics in aerobic experiments of 80±85 doubled haploid lines of IR64/Azucena Trait

Days to flower Plant height Panicles/m2 Spikelets/panicle Sterility (%) Weight per grain Grain yield

Chromosome

3 1 3 1 2 6 4 1 5 10 1

Interval

RG348-RZ329 RZ730-RG810 CDO87-RG910 RG690-RG810 CDO686-Amy1AC CDO544-RG653 R214-RG143 RZ730-RG810 RG313-RZ556 RG257-RG241 RZ730-RG801

Number of experiments where detected/ number sites where measured

Reported for lowland experiment by Courtois et al. (1995) Interval mapping

Single marker analysis

5/6 4/5 3/6 6/6 2/6 3/6 2/6 4/6 2/6 3/6 4/6

Yes Yes No Yes No No Yes Yes No No No

Yes Yes Same chromosome arm Yes Same chromosome arm No Yes Yes Same chromosome arm Yes Yes

Direction of effect of IR64 allele

‡ ‡ ‡

‡ ‡

186 H.R. Lafitte et al. / Field Crops Research 75 (2002) 171±190 Fig. 6. Chromosome regions showing an increase in the proportion of Azucena or IR64 alleles in set of lines selected for grain yield in aerobic (A) or lowland (L) conditions. Sets of lines were selected from among 80 lines of a doubled haploid line population. Parents of the population are IR64, an improved lowland indica cultivar, and Azucena, a traditional upland japonica cultivar.

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or if other, linked genes are responsible for the effect. A set of backcrossed introgression lines that vary for markers in this region of Chromosome 1 has been developed (Shen et al., 2001) and these will be used to dissect the effects of different genes in this region. Apart from the region on Chromosome 1, no other QTL was identi®ed with a consistent effect on yield or its components across the aerobic environments. This may be because the source of aerobic adaptation in this cross is the low-yielding cultivar Azucena, or it may simply re¯ect low precision of the QTL estimates. Additional populations of introgression lines have now been developed in improved upland genetic backgrounds (e.g., Robin et al., 2002). They should allow us to assess the effect of other chromosomal segments with more precision and should provide insights into other mechanisms that improve performance in aerobic soils. To supplement the QTL analysis, allele frequencies were examined at each marker in subsets of 15 lines selected on the basis of superior yield. Some markers showed skewed segregation toward one of the parents in the original population (Fig. 6). The segregation ratios of the sub-sets of superior lines were therefore compared with those observed in the evaluated DH lines rather than to the 1:1 theoretical ratio. To separate aerobic adaptation from overall yield potential, two separate sets were identi®ed, eliminating any lines common to both sets: one set with superior yields in the 1994 lowland experiment, and one set with superior yields in the combined aerobic experiments. The 15 superior DHLs for performance in the lowland experiments (set L in Fig. 6) had a signi®cantly enriched proportion of IR64 alleles in the interval from RG173 to RG146 on Chromosome 1, from RZ318 to RG95 on Chromosome 2, and in smaller intervals on Chromosomes 5, 7 and 10. The aerobicadapted set of lines did not show changes in these regions (set A in Fig. 6). At other regions, however, the lines with superior yield in the aerobic environments had a clear majority of IR64 alleles. This was particularly apparent in the region around the sd1 gene for the aerobic lines, but not for the lowland-selected lines, and indicates that those alleles are under differential selection in the two environments. As physical mapping data become available for this region on Chromosome 1, it will be possible to untangle the basis of this apparent contradiction between traits that are expected to contribute to aerobic adaptation and

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®eld performance. It is possible that the bene®ts of improved harvest index associated with the IR64 alleles overwhelm any bene®ts associated with greater water acquisition by the deeper, Azucena-type roots. On Chromosome 8, there was a shift toward IR64 alleles in lines selected for high yield in the aerobic environment (Fig. 6). The markers affected were near QTLs that have been identi®ed for osmotic adjustment and also for root growth (Price and Courtois, 1999), with the IR64 allele conferring greater osmotic adjustment but decreased root depth. A shift to Azucena alleles in the aerobic selections was observed only for a segment of Chromosome 11. In the 1998 experiment, we mapped a QTL for stem borer damage to this marker interval, and the IR64 allele was associated with increased damage (unpublished data). In a separate mapping population derived from a cross between Azucena and the upland-adapted semidwarf indica cultivar, Bala, a shift toward Bala alleles was also detected for two markers on Chromosome 1 near the sd1 locus in subsets of lines selected for high yield in control or stress treatments (unpublished data; population described in Price et al., 2000). This change was not as clear as in the IR64/Azucena population, where several adjacent markers showed shifts in allele frequency. There was also a shift toward the Azucena allele on the long arm of Chromosome 11 in lines that yielded well under stress, as observed in the IR64/Azucena population. As additional data accumulate from other mapping populations, the in¯uence of these genetic regions can be better understood. The use of parental lines with more similar resistance to biotic stresses and without genetic sterility would avoid some of the confounded results described above. 5. Conclusions Genetic improvement for yield in the traditional low-input aerobic rice ecosystem of hilly Southeast Asia has resulted in cultivars with yields superior to farmers' traditional cultivars and with similar stability. Differences in cultivar response to environment are associated with panicle number per square meter and also with resistance to blast disease. Yields in this system appear to be limited by soil acidity and fertility, but rainfall patterns are also important. The amount of solar radiation near ¯owering appears to be an

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additional important abiotic factor, though this is confounded with rainfall. Further genetic gains may be possible in both tolerance to short-term water de®cit and in tolerance to cloudy conditions during the monsoon season. There has been clear genetic improvement for performance in the high-input aerobic rice system, where soil fertility is high and soil acidity is not a constraint. In our study, two improved indica cultivars had high yields and stable performance across environments. These cultivars are classi®ed as indica types on the basis of isozyme analysis, but there is signi®cant tropical japonica germplasm in their pedigrees. In other aerobic systems, intermediate types derived from crosses between indica and japonica cultivars have also been very successful. Superior plants have intermediate height and tillering patterns, and stable pre-anthesis biomass production and harvest index across a range of contrasting environments. Improved yields are expected to result from improved partitioning, as has occurred in lowland rice cultivars. To support this work, we need to better understand the physiological basis of altered harvest index in aerobic systems compared to lowland systems. Studies with mapping populations indicate that increased tillering and greater spikelet fertility also appear to underlie superior aerobic adaptation. Improved performance in aerobic systems is related to a complex interplay between genetic regions associated with superior harvest index and greater rooting capacity, several of which have been mapped to the long arm of Chromosome 1. Further mapping studies and advances in functional genomics should allow improved understanding of the underlying physiology of these interactions in the future. Acknowledgements Thanks to G. McLaren for assistance with the IRRISTAT analysis, and to three anonymous reviewers for helpful comments on the manuscript. References Ali, M.L., Pathan, M.S., Zhang, J., Bai, G., Sarkarung, S., Nguyen, H.T., 2000. Mapping QTLs for root traits in a recombinant

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