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A large-effect QTL for rice grain yield under upland drought stress on chromosome 1
R. Venuprasad • M. E. Bool • L. Quiatchon M. T. Sta Cruz • M. Amante • G. N. Atlin
Received: 13 April 2011 / Accepted: 17 September 2011 Ó Springer Science+Business Media B.V. 2011
Abstract Drought is a major abiotic stress factor limiting rice production in rainfed areas. In this study we identiﬁed a large-effect quantitative trait locus (QTL) associated with grain yield under stress in ﬁve different populations on chromosome 1. The effect of this QTL was further conﬁrmed and characterized in ﬁve backcross populations in a total of sixteen stress and non-stress trials during 2006 and 2008. In all the stress trials (eight in total) qDTY1.1 showed strong association with grain yield explaining on average
Electronic supplementary material The online version of this article (doi:10.1007/s11032-011-9642-2) contains supplementary material, which is available to authorized users.
R. Venuprasad (&) Á M. E. Bool Á L. Quiatchon Á M. T. Sta Cruz Á M. Amante Á G. N. Atlin International Rice Research Institute (IRRI), DAPO Box 7777, Metro Manila, Philippines e-mail: R.Venuprasad@cgiar.org Present Address: R. Venuprasad Africa Rice Centre (AfricaRice), Ibadan PMB5320, Nigeria Present Address: M. E. Bool Monsanto, General Santos, Philippines Present Address: G. N. Atlin International Maize and Wheat Improvement Centre (CIMMYT), Apdo. Postal 6-641, 06600 Mexico, DF, Mexico
58% of the genetic variation in the trait. Homozygotes for the tolerant parent allele (Apo) yielded on average 27% more than the susceptible parent allele (IR64) homozygotes. Using an Apo/3*IR64 population, the peak of this QTL (qDTY1.1) was mapped to an interval between RM486 and RM472 at 162.8 cM at a LOD score of 9.26. qDTY1.1 was strongly associated with plant height in all the environments; this was probably due to the presence of the sd1 locus in this genomic region. In a Vandana/3*IR64 population segregating for sd1, a strong relation between plant height and yield under stress was observed. The observed relation between increased height and drought tolerance is likely due to tight linkage between qDTY1.1 and sd1 and not due to pleiotrophy of sd1. Thus there is a possibility of combining reduced plant height and drought tolerance in rice. The large and consistent effect of qDTY1.1 across several genetic backgrounds and environments makes it a potential strong candidate for use in molecular breeding of rice for drought tolerance. Keywords Rice Á Drought Á QTL Á Yield
Introduction Rainfed rice occupies 50% of the total rice area in the world. Over 700 million people depend on rainfed
drought risk reduces productivity even in non-drought years. IRRI is located at 14°130 N latitude. 2009b). Deﬁnition of upland. when even moderate stress can result in drastic reduction in grain yield (Hsiao 1982. The soil type is a Maahas clay loam. 2. and rainfed trials sown under upland management in the wet season (WS). while the QTL on chromosome 12 has a large effect on yield under upland drought stress in the Vandana/Way Rarem population. because farmers avoid purchasing inputs when they fear crop loss. Rice is sensitive to drought stress during reproductive growth. stress and non-stress environments In this article. These results should hasten development and delivery of drought-tolerant varieties. 2008. These reports indicate that QTL with large effects on yield under drought stress may not be uncommon. poverty. non-puddled. and alleviating poverty in communities dependent on rain-fed production. becoming mired in a cycle of low productivity. 2007). and food insecurity (Pandey et al. non-ﬂooded and aerobic conditions in leveled upland ﬁelds. Apo/IR72. 121°150 E longitude. Venuprasad et al. The QTL on chromosomes 2 and 3 are reported to affect grain yield in lowland drought and upland environments in the Apo/2*Swarna population (Venuprasad et al. in which stress occurred naturally due to periods of low rainfall. Los ˜ Banos. Drought tolerance is considered a complex trait. Kumar et al. and at an elevation of about 21 m above mean sea level. increasing productivity. Development of rice cultivars with improved drought tolerance is thus an important element in reducing risk. Vandana/IR64. We previously evaluated ﬁve large populations (Apo/IR64. Laguna. Drought is the major abiotic stress limiting rice production in these areas. Kumar et al. Materials and methods The study was conducted at the experimental station of the International Rice Research Institute (IRRI). transplanted and anaerobic conditions. Venuprasad et al. In drought-prone areas. In spite of its importance. Compared to lowland non-stress trials. lowland refers to ﬂooded. the term upland refers to ﬁeld trials or nurseries conducted under direct-sown. The QTL on chromosome 1 was reported to have a large effect on yield under lowland drought stress in the CT9993/IR62266 mapping population (Kumar et al. 2007). progress in breeding for drought tolerance in rice has been slow. lowland. are referred to as natural stress environments. 2007 and 2008 and the wet season (WS) of 2007.Mol Breeding rice grown on 50 million ha in Asia. Therefore we need to further expand efforts to identify donors of alleles with large effects on grain yield under drought stress that may be useful in MAB on a wider scale. To date. in many cases their utility in MAB may be limited because their effects across genetic backgrounds are not consistent. puddled. Dry season (DS) trials in which drought stress was artiﬁcially imposed during the reproductive stage are referred to as stress trials. 2010. four such large-effect QTL have been reported and are located on chromosomes 1. 2007. In this study we report the identiﬁcation of such a QTL associated with yield under upland drought stress in rice. isohyperthermic mixed typic tropudalf. Vandana/IR72 and IR64*2/Azucena). in the dry seasons (DS) of 2006. The objective of this study was to identify QTL that affect yield under stress consistently in these diverse genetic backgrounds and further characterize them in multiple backcross populations. 2007). 2009b). O’Toole 1982). Another means of improving efﬁciency of breeding is to identify quantitative trait loci (QTL) with large and consistent effects on yield under drought stress that could be used for marker-assisted breeding (MAB). 2007. Though such alleles will be useful in improving understanding of the genetic and physiological basis of drought tolerance of rice varieties. Trials conducted in lowland irrigated conditions where no stress was imposed are referred to as non-stress trials. in all the upland trials mild 123 . However in recent years considerable progress has been made in the areas of identiﬁcation of suitable donors and devising of effective selection criteria for traits related to drought tolerance (Guan et al. derived from crosses between lowland and upland or upland-adapted lines to evaluate the effectiveness of direct selection under severe artiﬁcially-imposed drought stress for improving rice grain yield under natural and artiﬁcially imposed drought stress (Venuprasad et al. 3 and 12 (Bernier et al. 2007). Philippines.
The number of lines in the different populations ranged from 223 to 481. (2000) and in the Gramene database (http://www. Initial evaluation trials and identiﬁcation of QTL region IR64 and IR72 are semi-dwarf high-yielding indica lines developed for irrigated lowland conditions. (1989). approximately 5 cm of standing water was maintained in the ﬁeld until drainage before harvest. Approximately 90 mm of water was applied at each irrigation. Apo/IR72. Irrigation was withheld until soil water tension. 2000. Five large upland/lowland populations (Apo/IR64. the 30 highest-yielding lines under stress conditions. Invitrogen Corporation. they were treated as missing values. USA) following a modiﬁed CTAB protocol using a GENO grinder. 2007. polymorphic RM markers were selected so as to represent the entire genome at intervals of about every 20 cM. From 4 to 7 WAS. USA) described in Temnykh et al. the 30 highest-yielding lines under non-stress conditions and 30 random lines in each population were selected for genotyping. indicating that these two lines are not closely related. The stress cycle was then repeated. and are highly drought-susceptible (Venuprasad et al. 2008. Both the stress and non-stress trials were laid out in an alpha-lattice design and consisted of two replications with single row plots measuring 1. reached about -70 kPa at 15 cm and -40 kPa at 30 cm soil depth. 84. De Datta and Seshu 1982. Vandana/IR64 and Vandana/IR72 were 55. Venuprasad et al. progenies of the crosses were scored according to the parental banding pattern as Parent 1 homozygotes. The numbers of polymorphic markers scored in Apo/IR64. unﬂooded upland ﬁelds. Details of the 2003 phenotyping procedure were presented in detail by Venuprasad et al. The repeated cycles of stress ensured that all entries experienced stress during the sensitive stage of 15 days around ﬂowering.5 m2 in upland. 1999). (2007) and are brieﬂy reviewed below. Apo/IR72. In the stress trials. Single marker analysis was done using QTL Cartographer software (Wang et al. The electrophoresis system used for this purpose was the Triple-Wide Mini-Vertical dual-sided unit (Cat. PCR products were resolved on 8% non-denaturing polyacrylamide (PAGE) gels as described by Sambrook et al. Huntsville. Drought stress was imposed around ﬂowering by reducing the frequency of irrigation to once every 10–12 days beginning 7 WAS and continuing until harvest. (2007). 123 . Vandana/IR64. Whenever null alleles or non-parental bands were observed. From among the lines evaluated in both stress and non-stress trials during DS 2003 in each population. 70. AL. 2005). The effect of each marker on grain yield was tested in every population. Singh et al. CA.31 m2 in lowland and 0. Azucena. Apo and Vandana are upland varieties with a range of drought tolerance (Bernier et al. Trials were then basin-irrigated until soil was saturated in the root zone. basin irrigation was provided once every 4–5 days to maintain the soil near ﬁeld capacity. measured by tensiometers installed in the ﬁeld. unpuddled. seeds were sown in the nursery and 21-day-old seedlings were transplanted to the puddled lowland ﬁeld. California. Parent 2 homozygotes. PCR ampliﬁcation was performed as described in Temnykh et al. # MGV-202-33) from CBS Scientiﬁc Co. Vandana/IR72 and IR64*2/Azucena) derived from these ﬁve lines were used. (2000). gramene. IR64*2/Azucena. dry seed was direct-sown into level. The total amount of rainfall received during 2003 crop growth was 34 mm while the estimated evapotranspiration was 780 mm. (Del Mar. These ﬁve populations were previously phenotyped for grain yield under upland drought stress and in lowland irrigated environments during DS 2003 by Venuprasad et al. The position (cM) of these markers on the chromosomes was assumed from Temnykh et al. 64 and 74 respectively. In the non-stress trials. Wade et al. This irrigation regime resulted in stress levels that caused leaf rolling and tip burning at the end of each drying cycle. For the ﬁrst 4 weeks after sowing (WAS). 2007. Based on the gel banding pattern. A parental polymorphism survey was done using 600 rice-microsatellite (RM) markers (ResGen. (2001). The coefﬁcient of parentage between IR64 and IR72 is about 0. Miniprep-scale DNA extraction was done in deep-well plates (Axygen Scientiﬁc. From the parental polymorphism data. 2007).22.Mol Breeding drought stress prevailed throughout the growing season. trials were irrigated by overhead sprinklers once every 3 days for 4 h. USA).org). or heterozygous. After transplanting.
In the upland non-stress trials. IR84176. Rainfall during crop growth was about 223. The upland stress trials were managed similarly as in 2003 (Section ‘‘Initial evaluation trials and identiﬁcation of QTL region’’) except that sprinkler irrigation was followed after initial establishment. data on days to ﬂowering. four populations (IR84176. respectively. All the WS 2007 lowland trials were affected by late rains which caused lodging and 123 . dry seed was direct-sown at a rate of 8 g m-2 into unpuddled. plant height and grain yield were collected. Weeds were controlled initially by application of the preemergence herbicide and at later stages by hand weeding. N was applied in three splits at the rate of 30–40 kg ha-1 per split. The ﬁve RILs were backcrossed to IR64 (the droughtsusceptible parent) to develop ﬁve independent populations (IR83614. (2008) were selected and backcrossed to IR64 (the drought-susceptible parent) to develop ﬁve independent populations. In the natural stress trials. Approximately 40 mm of water was added each time and a total of about 800 mm of water was added throughout the crop growth. Lines from these ﬁve populations were separately evaluated in a total of 16 stress and non-stress trials between DS 2006 to WS 2008. IR78875176-B-1-1 and IR78875-207-B-2-1 respectively and consisted of 105. leveled upland ﬁelds. 2007 and 2008 The IR83614 population was evaluated in upland stress and non-stress conditions during DS 2006 and under severe upland drought conditions in DS 2007. Spacing between the rows was 0. WS 2007. DS 2008 and WS 2008. respectively. Plant height at maturity was recorded as length of the plant from the ground to the tip of main panicle. when two seedlings per hill were transplanted. A summary of the ﬁeld experiments conducted for conﬁrmation of the chromosome 1 QTL is given in Electronic Supplementary Material Table 1. In DS 2008 two populations (IR84177 and IR90755) were evaluated under upland non-stress conditions in adjacent trials. The IR84176 population was derived by crossing IR78875-176-B-2 to IR64 and again backcrossing the resulting BC1F1 s to IR64. a marker with consistent effects across populations on yield under upland stress was detected on chromosome 1.0 m2 in lowland.20 in lowland. generating 314 BC2F2:3 lines. In all the lowland nonstress trials.25 m in upland and 0. After transplanting. 130. DS 2007. Experiments to conﬁrm the effect of this region and to localize the QTL were conducted in several BC1 and BC2 populations. In WS 2007. irrigation was to ﬁeld capacity throughout the experiment. 60 and 115 BC2F2:3 lines. One seedling was transplanted per hill at a spacing of 10 cm between hills in a row. 600 and 498 mm. seeds were sown in the nursery and 21-day-old seedlings were transplanted to the main ﬁeld. 940. approximately 5 cm of standing water was maintained in the ﬁeld until drainage before harvest. and ZnSO4 fertilizers were each applied at the rate of 40 kg ha-1 as a basal dose. IR78875-176-B-1-1. 512. upland non-stress and lowland non-stress conditions. IR90754 and IR90755 populations were similarly generated using RILs IR78875-85-B-4-2. Inorganic P. while evaporation was 633. The number of days taken for 50% of the plants in a plot to ﬂower was recorded as days to ﬂowering. Screening in stress and non-stress environments during 2006. All the trials were laid out as two-replicate alphalattices. IR84177.5 m2 in upland and 1. K. except in DS 2007. unﬂooded. after the initial establishment the crop was solely dependent on rainfall for water. 880. IR84177. IR78875-131-B-1-2. Sucking insect pests were controlled by insecticides when necessary. Inorganic NPK fertilizer was applied at the rate of 90–30–30 kg ha-1. ﬁve recombinant inbred lines (RILs. All the trials consisted of single-row plots measuring 0. respectively. IR78875176-B-2 and IR78875-207-B-2-1) with high yield in earlier drought stress trials conducted by Venuprasad et al. IR78875-85-B-4-2. Data collection In all the trials. IR90754 and IR90755). In the upland trials. The IR83614 population was derived by crossing IR78875-131-B-1-2 to IR64 and 400 BC1F2:3 lines were generated. IR90754 and IR90755) were evaluated under upland stress. All of the IR78875 lines were homozygous for the Apo-derived allele of RM472. From the Apo/IR64 population.Mol Breeding Conﬁrming the effect of the QTL in backcross populations Genetic material In the experiments described above. 355 and 860 mm during DS 2006. IR84177.
The IR84176 population was genotyped for RM486 (34.89 Mb) markers that were adjacent to RM472 (37.573 -1.499 2.5-LOD support interval was used to obtain the plausible location of QTL (Manichaikul et al.739 43.492 43. 1.596 19. which was in the middle of this region. 2006).01 was maintained for QTL detection and the genome scan interval was kept at 2 cM. RM6703 (34.347 6.307 22. the lower half of chromosome 1 (146–191 cM.301 43. To map the QTL linked to RM472 (qDTY1. covering *24 cM and containing 4 RM marker loci. 0.957 33. location on chromosome 1 as per IRGSP (2005)).1) on chromosome 1. ****: Signiﬁcant at P = 0. was used in genotyping all the ﬁve populations. Genotyping and QTL mapping Genotyping of the ﬁve backcross populations was done as described earlier (Section ‘‘Initial evaluation trials and identiﬁcation of QTL region’’).242 38.942 -4.88 Mb). the region between RM486 and RM431. ns non-signiﬁcant 123 .0001.563 7.369 9.389 10. was explored.906 7. An experiment-wise signiﬁcance level of P \ 0.998 9.997 1.05. A polymorphic simple sequence repeat (SSR) marker RM472.781 38.759 11.114 41. Mapping of QTL linked to RM472 was done using phenotypic data on WS 2007 grain yield data of the IR84176 population.Mol Breeding grain shattering and hence grain yield data from these trials were rejected.1.607 31.739 24. ***.865 -9.000 permutation tests were used to calculate the critical LOD value to control the genome-wise type I error.677 7. For the estimation of means for lines.661 32. respectively.925 26.743 -6.471 2.349 b1b 3. data were analyzed using the REML option of the SAS MIXED procedure Table 1 Single marker analysis of effect on grain yield under severe upland drought stress of markers on chromosome 1 in several rice populations: IRRI DS 2003 Population Apo/IR64 Marker RM237 RM543 RM315 Apo/IR72 RM237 RM543 RM315 RM568 IR64*2/Azucena RM473A RM102 RM472 RM414 Vandana/IR64 RM488 RM473A RM543 RM431 Vandana/IR72 RM237 RM297 RM486 RM431 RM568 a b c Position (cM) 115 146 165 115 146 165 197 120 152 172 191 101 120 146 178 115 134 154 178 197 b0a 24.001. RM543-RM414 interval) was found to contain a large-effect QTL for yield under stress (Table 1).01.026 13.872 Pc * **** **** ns *** *** *** ns ** *** ns ns ns ns **** ** **** **** **** **** b0 indicates population mean (g m-2) b1 indicates additive effect *.600 38. 0.51 Mb) and RM431 (38. A 1. Statistical analysis Statistical analysis was performed on individual trials using SAS v9.349 31.089 23.678 39.95 Mb.237 12. **. \0. Composite interval mapping of QTL was performed using QTL Cartographer.600 25.345 32. Based on the analysis of initial populations.054 24.324 26. 2004).3 (SAS Institute Inc.
0 cM) and RM25 (52. From the Vandana/IR64 population which was evaluated earlier (Venuprasad et al.7 cM) and RM245 (112. clearcut segregation was visually observed for plant height and the population was divided into tall and short plants based on height. of the total of 372 plants.0 cM) and RM206 (102.8 cM) and RM245 (112. The averages of ten random tall plants and ten random short plants at maturity were 124.1 cM).2 cM) on chromosome 8. data were analyzed using a model in which marker classes were considered ﬁxed and lines within marker classes. The resulting BC1F1s were again backcrossed to IR64 to produce BC2F1 and by repeated selﬁng BC2F3 s were subsequently obtained. Similarly. In the Vandana/IR72 population ﬁve regions.Mol Breeding where lines were treated as a ﬁxed effect.0 cM) and RM281 (128.90 (±3. Days to ﬂowering and grain yield were also recorded as explained above. RM172 (115. RM136 (51. whereas in the Vandana/IR64 population 12 regions located on eight different chromosomes showed strong associations with grain yield under stress. In the IR64*2/Azucena population one region.50 (±1.8 cM) on chromosome 6. RM183 (110 cM) on chromosome 2.4 cM) on chromosome 10 and RM511 (59. in the Apo/IR72 and Apo/IR64 123 .3 cM) on chromosome 9. 2.4 cM). RM285 (1. RM219 (11. Similarly. at ﬂowering. RM485 (0.8 cM) on chromosome 12. Using an SSR marker linked to the sd1 locus we conﬁrmed that the region near sd1 was segregating in concordance with height segregation (data not shown).2 cM) on chromosomes 1. They were RM315 (165. replicates and blocks within replicates as random. 2 months after seeding. RM231 (15. RM472 (171. 5. and replications and blocks within replications as random. RM431 (178. RM25 (52. and RM431 (178. RM506 (0. Heterogeneous lines derived from plants that were heterozygous at the locus in question were omitted from the single-marker analysis.6 cM) on chromosome 1.2 cM). RM163 (80. RM571 (205.1 cM). markers on the lower half of long arm of chromosome 1 showed substantial consistency (Table 1).6 cM) on chromosome 8.45 cM). and RM17 on chromosome 12 (109.3 cM). and at maturity. Both the trials were laid out as alpha-lattices with two replications consisting of single-row plots.9 cM) on chromosome 11. RM510 (20. On comparing effects of markers on grain yield under stress across populations. These were RM462 (2. RM333 (110. They were RM315 (165. For the estimation of the means for different marker classes in a trial. The proportion of the genetic variance explained by the QTL (R2 ) was estimated as the ratio G of variance explained by RM472 marker to the total genetic variance for the trait. RM523 (12 cM) on chromosome 3.3 cM) on chromosome 1. showed a highly signiﬁcant effect on grain yield under stress. showed strong association with yield under stress. 6.3 cM) on chromosome 7.5 cM) on chromosome 6. Variance components for a completely random model were estimated using the REML option of SAS PROC VARCOMP.8 cM).3 cM) on chromosome 1. In the Vandana/IR72 population all four markers between 134 and 197 cM showed highly signiﬁcant effects (P \ 0. RM327 (67. RM346 (56. In the two upland trials. Results Initial evaluation trials and identiﬁcation of a common QTL region affecting yield under upland drought stress across populations In the Apo/IR64 population seven marker regions distributed on six chromosomes showed highly significant effects on grain yield under stress and thus were identiﬁed as putatively linked to QTL for grain yield under drought stress. 185 were tall and 187 were short. a semi-tall RIL (IR78908-63-B-1) which was high-yielding under upland stress was backcrossed to IR64. 3. Evaluating the effect of height (sd1) on yield under stress and non-stress Vandana is a moderately tall line while IR64 is a semidwarf. The tall and short plants were evaluated during WS 2007 in upland non-stress and stress conditions. Management of the trials was as explained earlier for the WS 2007 experiments. In this population (IR84184). Data analysis to obtain means for different traits was done as explained above. seven marker regions on seven different chromosomes were found to be linked to grain yield under stress.3 cM) on chromosome 9.5 cM) on chromosome 1. plant height was measured at four times: 1 month after seeding.0 cM) on chromosome 2. 2007). and RM286 (0. RM493 (79. using the REML option of the SAS MIXED procedure.7 cM).20) cm respectively. 7 and 8 respectively). in the Apo/ IR72 population.82) and 86. A segregation ratio of 1:1 was observed.001) on grain yield under stress.7 cM) on chromosome 3. RM340 (133.
respectively. RM472 had a signiﬁcant effect.Mol Breeding populations.780 in different populations) and in the DS 2008 mild stress trial the average H of the two populations was 0. IR90754 and IR90755 populations under stress were reduced by 53. The means of the three BC2 populations were between 277 and 337 g m-2 under non-stress conditions and between 136 and 168 g m-2 under stress. all the markers from 146 cM and beyond showed highly signiﬁcant effects (P \ 0.84. in upland. Thus it seems likely that a large effect QTL for grain yield under stress lies in the 146–191 cM interval on chromosome 1. under lowland non-stress conditions IR64 ﬂowered about 4 days earlier than Apo (Supplementary Table 2). the recurrent parent. Apo yielded 345 g m-2. In the IR83614 population under moderate and severe stress conditions. Apo was taller than IR64 by about 17 cm (the difference was greater in WS 2007 than DS 2007) while in upland trials the difference was between 17 and 37 cm. which was only 10% of the DS 2006 moderate stress trial yield. in the mild stress environment. respectively (Supplementary Table 3). hence the yield data were not used for further analysis. under upland non-stress conditions and under stress they showed 27 and 74% yield reduction.70 (ranging from 0. while the two BC2 populations yielded 184 and 210 g m-2 (Supplementary Table 3). RM472 explained 37 and 15% of the genetic variance in the trait in these two environments. respectively. than to Apo. under severe stress IR64 ﬂowered approximately 14 days later than Apo. Screening of the backcross populations of Apo and IR64 under stress and non-stress conditions Four backcross populations involving Apo as the donor parent and IR64 as the susceptible recurrent parent were evaluated in several stress and non-stress environments during DS 2006–WS 2007. IR90754 and IR90755). The yield of the populations in lowland non-stress was low (between 156 and 206 g m-2) probably due to heavy late-season rains. H of grain yield in DS 2008 non-stress trial was 0. Under lowland non-stress conditions.54 to 0. Similarly. 0. During WS 2007 Apo and IR64 yielded about 466 and 332 g m-2. IR84177.51 g m-2 while under stress it was 133. and severe stress during DS 2007 was 0. Stress in the DS 2007 season was very severe and the population mean was just 10. a highly signiﬁcant effect of RM472 on 123 . Conﬁrming the effect of the QTL in backcross populations No effect of RM472 on grain yield in upland nonstress was observed in any of the ﬁve studied populations. In Vandana/IR64 only one marker was available beyond 146 cM and it had a highly signiﬁcant effect on yield under stress.45. In most cases BC2 progeny means were closer to IR64. During DS 2006. though Apo and IR64 possess similar days to ﬂowering under non-stress and mild stress conditions. moderate stress during DS 2006. In all cases progeny means were intermediate to those of the two parents. with Apo allele homozygotes giving larger yields than IR64 homozygotes by 12 and 38%. Under lowland non-stress conditions. The difference was wider under severe stress. During DS 2008. Apo consistently gave greater yields than IR64 in all the upland environments. IR64 is a semi-dwarf line and thus it was consistently shorter than Apo in all trials. Apo and IR64 yields were on par (494 vs. 503 g m-2) and the population yielded 472 g m-2 on average. but a large and signiﬁcant effect was seen under stress conditions in all the studied populations (Table 2). where the height of IR64 was only *55% that of Apo (Supplementary Tables 2 and 3).5 times higher than IR64.35 (range 0. Relative to their yields under upland non-stress conditions. respectively.001).62 g m-2. Broad sense heritability (H) of grain yield under upland non-stress. respectively. Under upland non-stress conditions in DS 2006 the population mean was 178.12–0. IR64 ﬂowered earlier than Apo but in DS 2008 mild stress trial it ﬂowered later than Apo (Supplementary Table 3). on average. data not shown).32 and 0.44 while under stress the average H was 0. in WS 2007. The IR83614 population was evaluated during the DS of 2006 and 2007.55 (data not shown). respectively. about 2. in the four BC2 populations (IR84176.58. In all the wet season trials of 2007. with more delay under severe stress. In the IR64*2/Azucena population two markers at 152 and 172 cM showed highly signiﬁcant effects while the marker at 191 cM did not have a signiﬁcant effect. a 25% reduction (Supplementary Table 2).42. the average yields of the IR84177. IR83614 (BC1) progeny as a whole showed delayed ﬂowering due to stress. while in lowland non-stress it was 0. 52 and 29%.
DTY.26 18.\0.48 0.22 and 16.20 207. upland stress and lowland non-stress environments. The Apo allele was always associated with greater plant height irrespective of the environment. Even in the DS 2008 mild stress trials.72 ± 7. the Apo allele homozygotes were taller than IR64 allele homozygotes by 13. *. In the IR84176 population it showed a signiﬁcant effect in all the environments while in the IR90754 population an effect was observed only in the lowland non-stress environment. **** signiﬁcant at P = 0.54 ± 5.00 1. 1).37 ± 8.0001.Mol Breeding grain yield was seen in upland stress conditions. explaining 67–84% of the genetic variance for this trait.00 293.68 ± 5. a large-effect QTL was located Table 2 Effect of the RM472 locus on grain yield (g m-2) under upland drought stress and non-stress conditions.76 13. explaining on average 63% of the genetic variance across populations (range 51–100%) for the trait.35 ± 5. Homozygotes for the Apo allele gave larger yields than those for the IR64 allele by an average of 32% (range 27–41%). Mapping of the QTL A QTL related to grain yield under stress and linked to RM472 (henceforth referred to as qDTY1.94 15.66 ± 13.39 138. while in the IR84177 and IR90755 populations it showed signiﬁcant effects in the non-stress environments but not in the stress environments (Table 4). The effect of RM472 on days to ﬂowering was inconsistent. with Apo allele homozygote yielding an average of about 20% more than the IR64 allele homozygotes. In the IR83614 population.59 275.10 ± 20. in Apo/IR64 backcross populations: IRRI 2006–2008 Environment Populationa Season Number of lines Homozygotes for allele type Apo 177.26 ± 18.32 ± 5.62 207.**.99 Upland non-stress IR83614 IR84177 IR90754 IR90755 06DS 07WS 07WS 07WS 06DS 07DS 07WS 07WS 08DS 07WS 07WS 08DS 400 105 60 115 400 400 314 105 105 60 115 115 Upland stress IR83614 IR83614 IR84176 IR84177 IR84177 IR90754 IR90755 IR90755 a IR83614 = IR78875-131-B-1-2/2*IR64. 14. 0.02 ± 17.68 1.30 IR64 175. and the proportion of genetic variability for the trait explained by the locus. The region between RM6703 and RM431 on chromosome 1 was explored.41 cm in upland non-stress.71. it showed a signiﬁcant effect in the stress environments but not in the non-stress environments.47 ± 9.17 10.03 207.19 252.48 172.89 382.15 0.68 129. with the Apo allele homozygotes yielding more than the IR64 allele homozygotes.76 10. 0.1.96 ± 9. the Apo allele was always associated with fewer days to ﬂowering than the IR64 allele.90 345.97 ± 6.31 9.62 Pb R2c Average magnitude of difference as % population mean 0.52 2. respectively.06 145.00 0.01.11 163. IR84177 = IR78875-85-B-4-2/2*IR64. Under stress.13 ± 1. respectively Genetic variance explained by the marker b c 123 .23 ± 6.55 5.52 0.50 160.65 12.05.***.49 177.81 ± 7.19 ± 14.79 16. grain yield under drought) was mapped using data from the IR84176 population phenotyped in stress and non-stress trials during WS 2007 (Fig.56 ± 21.22 147.96 284.37 0. In the IR83614 population RM472 had a small effect on yield in lowland nonstress conditions. a signiﬁcant effect of RM472 on grain yield was observed in both populations (IR84177 and IR90755) and explained 81% of the genetic variance among BC2-derived lines on average. IR84176 = IR78875-176-B-2/2*IR64 Probability of difference between the two homozygotes. consistent and large effect of RM472 on yield under drought stress.66 ± 8. IR90754 = IR78875-176-B-1-1/2*IR64. Thus there is a signiﬁcant.14 8.48 ± 35.04 206. Averaged over all the populations.69 ± 1.18 ± 7.001.01 ± 9. There is a consistent and highly signiﬁcant effect of RM472 on plant height in all the populations and in all the environments (Table 3).71 119. IR90755 = IR78875-207-B-2-1/2*IR64.07 ns ns ns ns * * **** **** * *** ** ** 0 0 0 0 0.15 289. but not under non-stress conditions.51 1.47 5. Whenever the effect was signiﬁcant.97 ± 22.
09 ± 1.38 ± 0.95 ± 5.44 ± 1.02 ± 1.54 0.93 78. One region.77 ± 1.33 ± 1.20 47. respectively Genetic variance explained by the marker b c between RM486 and RM472 with its peak at a distance of 3. Initially this was identiﬁed in DS 2003 wherein ﬁve large RIL populations derived from tolerant 9 susceptible crosses were phenotyped for grain yield under severe upland drought stress at the reproductive stage.30 ± 0.11 ± 1.88 ± 3. IR84177 = IR78875-85-B-4-2/2*IR64.02 105.34 ± 3.48 ± 1.5-LOD support interval.09 90.28 108. Using the 1. at maturity. In fact.14 90.28 81.76 0. There was a clear and signiﬁcant difference in height between the tall and short lines at all the four stages.08 ± 2.29 0.26 while the threshold LOD was 2. Discussion In this study we detected a large-effect QTL (qDTY1.78 06DS 07WS 07WS 07WS 06DS 07DS 07WS 07WS 08DS 07WS 07WS 08DS 07WS 07WS 07WS 07WS 400 105 60 115 400 400 314 105 105 60 115 115 314 105 60 115 88.31 ± 2.***.89 91.31 81.93 0. (2001) is RM568 at 196.01.91 0.05 89.11 92.11 ± 0. 0.73 ± 1.85 87.21 91.41 91.33 ± 2.1 was inferred to be located in a 6-cM interval.74 76.08 88.25 91. IR84176 = IR78875-176-B-2/2*IR64 Probability of difference between the two homozygotes.0001.5. Testing the effect of height on grain yield in Vandana/3*IR64 population In the WS 2007 the effect of plant height on grain yield was analysed in upland non-stress and stress environments.88 111.51 0.27 59.43 90.13 ± 2.11 ± 7.26 107.18 ± 1.66 IR83614 = IR78875-131-B-1-2/2*IR64. in IR64*2/Azucena the last marker on chromosome 1 (RM414. With respect to grain yield.26 108.23 ± 2. However. \0. the tall set was about 41 cm taller than the short set in non-stress and about 31 cm taller in stress (Table 5).38 ± 1.77 0.27 94. qDTY1.83 0.49 106. On average.79 ± 1.59 0.45 ± 1. **. and association between genotype and phenotype established by single-marker analysis.70 0.02 ± 5.35 103.80 0.001.23 ** **** **** **** **** **** **** **** **** *** **** **** **** **** **** **** 0.19 ± 0.48 ± 1.32 ± 1.68 ± 1. the tall set yielded signiﬁcantly more than the short set under both non-stress (by 67%) and stress (by 42%).72 0.60 98.35 97. There was a signiﬁcant effect of height on ﬂowering with the taller set ﬂowering about 2 days earlier than the shorter set under non-stress and one and half days earlier under stress. all genotyped markers beyond 146 cM to end of the chromosome in four of the ﬁve populations (Apo/IR64.Mol Breeding Table 3 Effect of the RM472 locus on plant height (cm) in Apo/IR64 backcross populations under drought stress and non-stress conditions: IRRI 2006–2008 Environment Populationa Season Number of lines Homozygotes for allele type Apo Upland non-stress IR83614 IR84177 IR90754 IR90755 Upland stress IR83614 IR83614 IR84176 IR84177 IR84177 IR90754 IR90755 IR90755 Lowland non-stress IR84176 IR84177 IR90754 IR90755 a Pb R2c IR64 82. was found to affect grain yield under drought consistently across populations (Table 1). 191 cM) did not show any association with yield.2 cM from RM472. **** signiﬁcant at P = 0. the lower part of the long arm of chromosome 1. The peak LOD score of this QTL was 9.71 0. IR90755 = IR78875-207-B-2-1/2*IR64.62 98. This delimitation of the QTL into a smaller region in one population could be because 123 .13 ± 7.71 0.1) associated with grain yield under drought stress in rice.34 ± 0.21 109.93 0. Apo/IR72.85 71.5 cM). Vandana/IR64 and Vandana/IR72) showed strong associations with grain yield (the last marker on chromosome 1 as per Temnykh et al. IR90754 = IR78875-176-B-1-1/2*IR64.98 ± 2.
73 0. qDTY1. IR90754 = IR78875-176-B-1-1/2*IR64.74 81.51 ± 0. while the rest of the populations consisted of F2:3 RILs with more limited recombination opportunities in the region of interest during their development.87 ± 0.28 ± 0. IR84176 = IR78875-176-B-2/2*IR64 b Probability of difference between the two homozygotes.19 86.90 89.80 78. 2007).51 ± 0.**.98 ± 0.1 showed strong association with grain yield under stress.and four BC2derived populations) involving Apo as the donor and IR64 as the recurrent parent were tested in a total of sixteen stress and non-stress trials during DS 2006 and DS 2008.90 ± 0.03 ± 0. Consistent effects were seen in all the 4 years 2003.75 80. the effect was seen both in the dry seasons as well as the wet season and in a range of stress levels. this QTL (qDTY1.**** signiﬁcant at P = 0.73 0.37 ± 1.05.01. 2007 and 2008.41 84.62 ± 2.22 84.82 79. characterize and map the QTL. a marker linked to RM472.1) for drought tolerance in rice has an effect only under severe upland stress (Bernier et al.03 ± 1.18 85.49 ± 0.97 ± 0. Interestingly.28 ± 0.42 0. 2006.81 ± 1.46 ± 0. 0.71 77. IR84177 = IR78875-85-B-4-2/2*IR64.90 ± 0.12 89. respectively.0001. Thus comparing across populations it seems likely that the QTL lies in the 146–191 cM interval on chromosome 1. The other previously identiﬁed large-effect QTL (qtl12.Mol Breeding Table 4 Effect of the RM472 locus on days to ﬂowering in Apo/IR64 backcross populations under drought stress and non-stress conditions: IRRI 2006–2008 Environment Populationa Season Number of lines Homozygotes for allele type Apo Upland non-stress IR83614 IR84177 IR90754 IR90755 Upland stress IR83614 IR83614 IR84176 IR84177 IR84177 IR90754 IR90755 IR90755 Lowland non-stress IR84176 IR84177 IR90754 IR90755 a Pb R2c IR64 87. explaining on average 58% of the genetic variation for the trait (Table 2).66 ± 0.99 85. producing on average 27% more than the susceptible parent allele (IR64).and BC2derived populations (Tables 1 and 2).46 ± 0. \0.14 ns * ns * **** **** ** ns ns ns ns ns **** * ** * 0 0. 2009).39 ± 0.96 80.21 ± 0. During DS 2007 a signiﬁcant effect of RM6703.1) had an effect in ﬁve parental populations involving three different donors and two different susceptible parents.09 06DS 07WS 07WS 07WS 06DS 07DS 07WS 07WS 08DS 07WS 07WS 08DS 07WS 07WS 07WS 07WS 400 105 60 115 400 400 314 105 105 60 115 115 314 105 60 115 86.47 ± 0. *.49 ± 0.04 ± 0.18 0.20 85.54 0.71 79. To further conﬁrm.11 ± 1.21 0 0. a large-effect QTL in this region for yield under lowland drought stress has already been reported in CT9993/IR62266 doubled-haploid population (Kumar et al.53 80. Furthermore.09 ± 0.14 0 0 0 0 0 0.15 88.77 ± 2.08 0. In all the stress trials (eight in total). Subsequently its effect was conﬁrmed in ﬁve different backcross populations.69 81.33 ± 1.83 91. was observed on yield under severe stress in the Vandana/2*IR72 123 .10 81.45 ± 1.29 98.33 ± 0.22 IR83614 = IR78875-131-B-1-2/2*IR64.48 85.15 84.54 85. and in both DS as well as WS. IR90755 = IR78875-207-B-2-1/2*IR64.37 ± 0. the tolerant parent allele (Apo) was always associated with higher yield. ﬁve backcross populations (one BC1. As seen in this study.85 ± 0.93 81. ns not signiﬁcant Genetic variance explained by the marker c the IR64*2/Azucena population consisted of BC1F2:4 derived lines and thus had more chance for recombination.30 93.19 ± 0.49 81. moderate (with mean reduction of about 25% relative to non-stress) to very severe (with mean reduction of about 94% relative to non-stress) (Supplementary Table 2 and Table 2).43 82. The direction and magnitude of the effect was consistent in the RIL.34 88.82 86. BC1.
Thus available evidence indicates that the observed relationship between plant height and drought tolerance is probably largely due to linkage of sd1 with other loci affecting drought tolerance. 2002). root characters including rooting depth. Firstly. QTL for cell membrane stability. Venuprasad et al.1 under upland stress (solid line) and nonstress (dotted line) conditions. (2008) considered this region as one of the four key regions for drought resistance in rice. For the QTL under stress conditions the threshold LOD is 2. If the observed relation between height and drought tolerance is due to linkage then our study suggests tight linkage (Tables 3 and 5). The results of the Vandana/3*IR64 population indicate that lines differing substantially in height and therefore probably in sd1 genotype did differ signiﬁcantly in drought tolerance (Table 5).5-LOD support interval for QTL under stress population (Bool. The strong effect on height is probably due to the presence of the sd1 gene in this region (Spielmeyer et al. Khowaja et al.Mol Breeding Fig. Khowaja et al.5 while the peak LOD is 9. In their review. (2010) have all considered it to be an important locus for drought resistance. root thickness. The above results have implications for breeding rice for drought-prone environments. in many rice breeding populations. leaf water potential and several yield related traits have all been reported in this region. In divergent selection response studies involving the Apo/IR64 population. which is likely to be segregating in all the populations in this study. the relationship between increased plant height and drought tolerance has been empirically observed (IRRI. unpublished data). Kamoshita et al. (2009) and Kanagaraj et al. In addition. this region had a strong effect on grain yield under stress but not on height. (2009). in which sd1 was not segregating. few reports (Jiang et al. rather than being mainly a pleiotropic effect of sd1. Arrow on the x-axis indicates 1. (2007) report that under drought stress this region is associated with height and ﬂowering but not with grain yield. 2009). relative water content. 123 . leaf rolling and drying. Bernier et al. (2007) reported that in the CT9993/ IR62266 population. but the effect on ﬂowering was inconsistent (Tables 3 and 4). 2009) suggest that the relation between sd1 and drought tolerance is due to linkage. Courtois et al. A strong effect of RM472 on plant height was seen irrespective of the environment.26 at 162. The simultaneous effect of this locus on height and yield under stress could be either due to pleiotropy of the sd1 gene or to its linkage with other drought-tolerance QTL. On the other hand. root weight and root:shoot ratio.9 cM. 1 LOD score curve of QTL qDTY1. Kumar et al. 2004. (2009a) have shown a strong effect of RM6703 on grain yield under drought stress in both upland and lowland.
Tuong TP.36 ± 2.15 ± 40.03 ± 2. limiting fertilizer application and therefore yield potential.87 ± 2.89 115.87 74.72 ± 1.04 ± 3.86 104. Some researchers have concluded that sd1 may limit drought tolerance (Atlin and Laﬁtte 2002. Ahmadi N.04 \0.00 ± 3.23 ± 1. 2007.Mol Breeding Table 5 Effect of height on yield in different conditions in the IR78908-63-B-1/2*IR64 population: IRRI WS 2007 Line/group Plant height (cm) at: One month after seeding Nonstress IR64 IR78908-63-B1 Vandana Short progeny (n = 103) Tall progeny (n = 142) P$ Stress IR64 IR78908-63-B1 Vandana Short progeny (n = 103) Tall progeny (n = 142) P$ $ Two month after seeding 59. Spaner D.63 79.77 ± 1. Acknowledgments This work was funded by grants from the Rockefeller Foundation.55 ± 2. is urgently required.73 95.42 \0.07 ± 2.19 88.55 ± 1.73 ± 2.84 \0.85 89.29 \0. Mahto RN.32 \0.71 ± 1.25 ± 2. IRRI.0001 79.0001 Flowering Maturity Days to ﬂowering Grain yield (g m-2) 28. Hamelin C. Frouin J. Wade et al. We wish to thank Dr.79 ± 1.15 ± 3.51 ± 1.50 ± 1.94 ± 3.78 40. Rice 2:115–128 De Datta SK.35 ± 3.12 ± 22.) through bulk segregant analysis. the semi-dwarf trait has been correlated with drought susceptibility. Venuprasad R. USA and Generation Challenge Program. Though evidence indicates this could be achieved.82 123.63 73.99 ± 2.13 ± 1.08 ± 2. taller rice plants generally lodge under nonstress conditions in highly fertile soils.004 179.46 180.41 72.99 ± 1.44 ± 3. Dongre PR. However. LosBanos. Los Banos. A deﬁnitive test of the hypothesis that sd1 and qDTY1. Venuprasad R.20 ± 3. Price A.78 29. Rami J-F.69 49. Hengsdijk H. IRRI. M.31 ± 2.82 84. Laﬁtte et al.0001 62. Hardy B.74 \0.29 37.99 ± 0.79 ± 3.31 ± 22.19 60. Sinha PK. In: Bouman BAM.55 ± 2.1 are linked loci.24 ± 1. Ruiz M (2009) Rice root genetic architecture: meta-analysis from a QTL database improves resolution to a few candidate genes. pp 245–263 123 .90 73. Verlukar S.90 104. Philippines.1 over a range of environments in the Philippines and eastern India. Thus there is a need to breed drought tolerant rice lines with medium or semi-dwarf height.19 85. Esperitu.43 83.43 ± 1.85 \0. Philippines Courtois B.98 \0. Philippines.09 ± 3.0001 Probability of difference between the short and tall progeny groups Conversely.07 \0.55 300. Crop Sci 47: 507–516 Bernier J.99 78.43 ± 1. Peeraju P. tight linkage between sd1 and drought-tolerance genes would slow the development of such cultivars.0001 73.0001 80. Del Valle for the help provided.63 63. Proceedings of the international workshop on waterwise rice production. p 356 Bernier J.75 ± 3.12 ± 40.10 118.82 108.59 ± 46. 1999).0001 66. Seshu DV (1982) Evaluating rices for drought tolerance using ﬁeld screening and multilocation testing. Secondly.46 289.19 ± 22.68 93.64 ± 1.22 133.87 69.46 ± 0.00 125.23 102. Kumar A. ˜ ˜ 8–11 April 2002. There is a need to ﬁne-map this region.32 ± 1.50 \0.46 ± 3. Bindraban PS.10 145. MAB for drought tolerance should be possible in rice with candidates such as qDTY1. MS Thesis submitted to UPLB. Atlin GN (2009) Characterization of the effect of rice drought resistance qtl12. In: Drought resistance in crops with emphasis on rice.68 94.69 36.69 ± 3.87 64. C.74 98.00 ± 46.98 0. Dalid and M.83 ± 2. References Atlin GN.0001 38.68 63.90 100.1 given its large and consistent effect in several genetic backgrounds and environments. Kumar.0001 71.70 ± 1.0001 61. Laﬁtte HR (2002) Developing and testing rice varieties for water-saving systems in the tropics.46 301.67 ± 2.32 46.22 177. Ladha JK (eds) Water-wise rice production.0002 83.74 ± 1. Atlin GN (2007) A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice.73 99.25 ± 3. Mandal NP.15 ± 2.69 50.53 ± 1.89 77.83 ± 1. Los Banos Philippines.89 101.78 34.32 ± 16. Kumar A.40 0.54 ± 3. Khowaja F.73 68.06 ± 16. or due to late season rains and wind. Euphytica 166:207–217 Bool E (2009) Detection of putative QTL for drought tolerance in rice (Oryza sativa L. rather than pleiotropic expressions of the same locus. Spaner D.45 ± 46.41 ± 1.
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