Published in Crop Sci. 44:248-253 (2004).
© 2004 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
GENOMICS, MOLECULAR GENETICS & BIOTECHNOLOGY
A Microsatellite Marker and a Codominant PCR-Based Marker for Marker-Assisted Selection of Submergence Tolerance in Rice
Kenong Xua,
Rashmi Deba and
David J. Mackill*,b
a Dep. of Agronomy & Range Science, University of California, Davis, CA95616-8515 USA
b International Rice Research Institute (IRRI), DAPO Box 7777, Metro Manila, Philippines
* Corresponding author (d.mackill{at}cgiar.org).
 |
ABSTRACT
|
|---|
Submergence tolerance is an important trait for rice (Oryza sativa L.) in rainfed lowland conditions and is being evaluated as a weed control strategy for rice seeded directly into standing water. The trait is largely controlled by a major gene designated Sub1. The present study was conducted to assess the use of the microsatellite marker RM219 and the codominant PCR-based marker RM464A (derived from a microsatellite marker, RM464) to select for submergence tolerance. The two markers RM219 and RM464A were found to be linked to Sub1 by 3.4 and 0.7 cM, respectively. These two markers were further tested in 55 diverse indica and japonica rice cultivars and breeding lines. RM219 was highly polymorphic in this set of cultivars, showing 14 different alleles, and none of the 55 cultivars had the same allele as the submergence tolerance source IR40931-26. RM464A showed three different alleles in the 55 cultivars. The allele of RM464A of most japonica genotypes was 231 bp in size, 5 bp larger than that of IR40931-26, whereas the allele of most indica rice samples was the same as that of IR40931-26. This indicated that the marker RM219 could be used in breeding programs to select for the Sub1 gene in a wide range of backgrounds, whereas RM464A was more useful in selection for the Sub1 gene in japonica rice background. The two markers were used to identify lines from backcrossing a submergence tolerance donor to the temperate japonica cultivar M-202. Several lines were identified that were homozygous for RM219, RM464A, and Sub1, and were otherwise genetically similar to M-202. Near isogenic lines (NILs) developed from these sources will be a valuable tool for genetic and physiological studies of submergence tolerance and will also be valuable for evaluating submergence tolerance as a useful trait in water-seeded temperate rice production.
Abbreviations: AFLP, amplified fragment length polymorphism • bp, base pair • cM, centimorgan • MAS, marker assisted selection • PCR, polymerase chain reaction • NIL, near isogenic line • RAPD, random amplified polymorphic DNA • RFLP, restriction fragment length polymorphism
|
INTRODUCTION
|
|---|
IN ADDITION to being the major food crop grown in tropical climates, rice is also widely grown in temperate regions, where the japonica subspecies is predominant. Most highly productive rice systems rely on maintaining the fields flooded to a depth of 5 to 10 cm. However, it is often not possible to control the water depth, and submergence of the plants may occur. Submergence tolerant rice cultivars have been identified that can survive up to 2 wk of inundation (Vergara and Mazaredo, 1975). In areas where water control is poor, submergence tolerance is an important breeding objective. It is also of interest in areas where rice is seeded directly into standing water as a means of weed control. In such areas as California, deeper water depths have been shown to increase weed suppression; however, rice emergence is inhibited (Williams et al., 1990).
The physiological mechanism of submergence tolerance is not well understood. Submergence tolerant cultivars tend to have reduced elongation of shoots under submergence compared with intolerant cultivars. This is thought to conserve carbohydrate reserves to allow survival and recovery on desubmergence (Setter and Laureles, 1996). The most widely used source of submergence tolerance has been the Indian cultivar FR13A. This is a tall, photoperiod sensitive and low-yielding cultivar with poor grain quality. The submergence tolerance trait was transferred into more productive semidwarf plant types (Mackill et al., 1996). While highly tolerant lines show some yield reduction, lines with good submergence tolerance and high yield potential have been identified.
Submergence tolerance was shown to be controlled mainly by a single locus, designated Sub1, and mapped on rice chromosome 9 (Xu and Mackill, 1996). Additional QTLs conferring tolerance have also been identified (Nandi et al., 1997) and are thought to contribute to higher levels of tolerance. In the mapping of the Sub1 gene, RFLP, AFLP, and RAPD markers were used; however, these markers are generally not suitable for application in marker assisted selection (MAS) programs, because they are laborious to measure and require a large amount or high quality of DNA. Codominant PCR-based markers, such as microsatellite markers, would be ideal for selection for submergence tolerance in breeding programs.
The objectives of this study were to evaluate the potential of a codominant PCR-based marker RM464A identified in this study and a microsatellite marker RM219 for selection of submergence tolerance in a breeding program, and to apply the two markers to develop NILs similar to the japonica cultivar M-202 that possess the Sub1 gene.
|
MATERIALS AND METHODS
|
|---|
Plant Materials
The F2 population designated DX236 was developed from a cross between the submergence tolerant line DX202-9 and M-202. M-202 is a temperate japonica cultivar that is widely grown in California. DX202-9 is a submergence tolerant F3 line from the cross DX18-121/M202; DX18-121 is a tolerant F3 line from the cross PI543851/IR 40931-26, which was used by Xu and Mackill (1996) to map the submergence tolerance locus Sub1 to chromosome 9. IR40931-26 is an indica line inheriting submergence tolerance from the Indian land race FR13A (Mackill et al., 1993), and PI543851 is a partially sterile mutant from California japonica cultivar Calrose 76 (Rutger and Schaeffer, 1989). This population (DX236) thus represents two crosses from the original indica/japonica cross to the temperate japonica cultivar M-202. This F2 is similar to a backcross population (BC2F2) because the line PI 543851 is genetically similar to M-202 (Mackill, 1995; Mackill et al., 1996). The F2 of 150 plants and the resulting F3 lines were used in the study to determine the linkage between Sub1 and markers, RM464A and RM219. A diverse set of 55 rice genotypes from different origins were used to study the variability at the marker loci of RM464A and RM219 (Table 1). These rice genotypes, except for the tolerant parent IR40931-26, were susceptible to submergence stress. Rice cultivars with strong submergence tolerance are rare among the tens of thousands of accessions screened at the International Rice Research Institute (IRRI), Philippines (Vergara and Mazaredo, 1975).
Submergence Screening Procedure
Submergence treatment was conducted in the greenhouse at the University of California, Davis, following the procedures of Xu and Mackill (1996) with minor modifications. Seeds of the F3 families and the cultivars IR 40931-26 and M-202 were pregerminated for 48 h at 37°C and approximately 10 seedlings were planted in each 10- by 10- by 10-cm pot in two replications. The pots contained approximately 400 g of soil. On the eighth day after planting, the plants were submerged in tanks filled with water up to 75 cm for 12 d. The water temperature was 25°C ± 1 throughout the screening process. The tanks were covered with shade cloth to increase the level of stress (Xu and Mackill, 1996).
Chlorosis, significant elongation, and other visible damage to the plants, as evidence for the classification of submergence susceptible plants, were first evaluated when 70% of the water was drained. The 30% remaining water was crucial for clearly observing the above symptoms for all plants in a pot when scoring, because it prevented the elongated plants from becoming tangled with each other. The second score was taken after 7-d recovery on the basis of individual plants that survived or died within a pot. For each of the F3 family, plants in two different pots were first evaluated independently, then only one integrated score, i.e., tolerant (T), susceptible (S) or segregating (H), was given. This three-category scoring system was adopted from Xu et al. (2000).
Analysis of Microsatellite Markers
DNA was extracted from fresh leaves following Redoña and Mackill (1996). On the basis of their map locations relative to the Sub1 locus, 123 microsatellite markers (Chen et al., 1997; Temnykh et al., 2001; Temnykh et al., 2000) were chosen and divided into two groups for analysis: Sub1-linked (5) or Sub1-unlinked (118). Sub1-linked microsatellite markers polymorphic between the two parents (M202 and DX202-9) of the F2 population (DX236) were assessed on the F2 plants to determine the tightness of linkage and on the 55 diverse rice accessions to study the potential of these markers for MAS in breeding programs. Sub1-unlinked microsatellite markers were used to screen the F2 population to determine the genetic contribution of the japonica recurrent parent M-202 to the plants. Those Sub1-unlinked microsatellite markers that were polymorphic between the two parents were further used to assay the F2 population to identify plants for the development of NILs.
The PCR was performed in a mixture of 10 µL containing 25 ng genomic DNA, 330 nM primer (Research Genetics, Inc, Carlsbad, Ca) each, 200 µM of each dNTP, 0.2 U of Tag DNA polymerase (Life Technologies, Carlsbad, CA), 0.4 µM fluorescent labeled dCTP (PE applied Biosystems, Foster City, CA), and 1x PCR buffer (20 mM Tris-HCL (pH 8.4), 50mM KCL and 2mM MgCL2). The PCR was conducted with a profile of 35 cycles at 94°C for 1 min, 55°C for 2 min, 72°C for 1.5 min with a final extension at 72°C for 5 min with a GeneAmp 9700 thermocycler (PE applied Biosystems). The PCR products were fractionated through a 5% (w/v) polyacrylamide gel (Long Ranger, in 1x TBE buffer with 6 M urea) for 2 h at 2000 V with an ABI 377 sequencer (PE Applied Biosystems) using GS-500-Rox internal size standards. The gels were analyzed by the computer program Genescan 3.0 (PE Applied Biosystems) and genotyped by Genotyper 2.1 (PE Applied Biosystems).
Linkage Analysis
The observed segregation ratios were compared to the expected ratio of 1:2:1 by chi-square goodness-of-fit test. A linkage map was then constructed (not shown) with the Macintosh computer program MAPMAKER 2.0 (Lander et al., 1987) using the Kosambi mapping function.
|
RESULTS
|
|---|
Evaluation of Submergence Tolerance
A total of 2933 seedlings of the 150 F3 families derived from the corresponding F2 (DX236) individuals, averaging 19.6 ± 6.1 seedlings per family in two pots, were evaluated for submergence tolerance. Submergence tolerance scores on the two parental controls were distinct and consistent, either tolerant (IR40931-26) or susceptible (M202). The 150 F3 families were scored as 35 (tolerant): 86 (segregating): 29(susceptible) showing a good fit to a ratio of 1:2:1 (0.20 > P > 0.10). This result confirmed Mendelian segregation of a single gene controlling submergence tolerance in the F2 population.
Identification of the Codominant PCR-Based Marker RM464A and the Microsatellite Marker RM219 Linked to Sub1
Amplification products of five microsatellite markers, RM285, RM316, RM444, RM464, and RM219 (Chen et al., 1997; Temnykh et al., 2001) linked to Sub1, were compared between the two parents (DX202-9 and M202). Polymorphic peaks were observed for RM316, RM464, and RM219, but not for RM285 and RM444. When RM316, RM464, and RM219 were tested in the DX236 F2 population, RM464 and RM219 could be clearly scored (Fig. 1), but it was difficult to score RM316. The reason was that the size difference of the primary RM316 peaks between the two parents was only two bases and there were secondary peaks, making the primary peaks of RM316 difficult to score.
View larger version (26K):
[in this window]
[in a new window]
|
Fig. 1. Plot view (adopted from the output of Genotyper V2.5) of segregation of RM464A (panel A) and RM219 (panel B) in BC2F2 (DX236) plants. Plants 16 and 19 represent parental homozygous alleles for DX202-9 and M-202, respectively, while the other plants are heterozygous.
|
|
The RM219 amplicons from DX202-9 and M-202 were 204 and 194 bp (Fig. 1), respectively. These amplicons are within the 192- to 222-bp range of RM219 amplified from various rice cultivars (Chen et al., 1997). Hence, the fragments amplified with the RM219 primers in this experiment were concluded to be the same referred to in Chen et al. (1997). However, RM464 displayed two primary peaks (Fig. 1). One monomorphic peak at 263 bp was within the expected range of 259 to 265-bp for RM464 (Temnykh et al., 2001). Presumably this 263-bp amplicon was the target peak for RM464. The second peak was polymorphic and segregating codominantly in the population. This second peak was measured at 226 and 231 bp for DX202-9 and M-202, respectively, much smaller than the expected sizes (259–265 bp) of RM464. Moreover, the 226-bp RM464 amplicon from DX202-9 displayed no sequence homology to AQ328629, a GenBank accession carrying a motif of (AT)21 from which RM464 was originally developed (Temnykh et al., 2001). The sequence of this smaller fragment derived from DX202-9 matched perfectly a portion of the sequence of AAAA01003627 (an accession in GenBank) sequenced from 93-11, an indica rice line (Yu et al., 2002), except for one base in each of the two primer regions (Fig. 2). Such a difference in primer regions could be directly introduced from the RM464 primers used in the PCR reaction amplifying the second peak (the smaller fragment) (Fig. 1). We designated this smaller fragment amplified by the same primers of RM464 as RM464A. On the basis of the sequence of RM464A derived from DX202-9 (Fig. 2), the longest array of simple sequence repeat was (AT)4 beginning at base 59. This showed that RM464A is probably not a microsatellite marker, but rather a codominant PCR-based marker.
View larger version (33K):
[in this window]
[in a new window]
|
Fig. 2. DNA sequence of the marker RM464A fragment. The alignment shows the positions of the two RM464 primers and the sequence identity in the RM464A region between DX202-9 and 93-11 (from accession AAAA01003627 in GenBank), an indica line sequenced by Yu et al. (2002).
|
|
Applying the RM219 marker to the F2 (DX236) population resulted in a segregation of 36 (DX202-9 allele): 88 (heterozygous): 26 (M-202 allele), a good fit to the 1:2:1 ratio at 0.10 > P > 0.05. The RM464A marker revealed a ratio of 36 (DX202-9 allele): 86 (heterozygous): 28 (M-202 allele), a good fit to the 1:2:1 ratio at 0.20 > P > 0.10. Linkage analysis showed that RM219 was linked to Sub1 at 3.4 cM at a LOD score of 46.6, and that RM464A were linked to Sub1 at 0.7 cM at a LOD score of 59.5. These two markers were both located on the same side as that of RZ698, a RFLP marker flanking Sub1 (Xu et al., 2000). On the basis of such a tight linkage between Sub1 and the two markers, it was anticipated that both RM219 and RM464A could be used for MAS of submergence tolerance in rice breeding programs.
Allelic Variability of RM219 and RM464A in Rice Germplasm
To determine the usefulness of RM219 and RM464A for MAS on a wider scale, 55 diverse rice accessions were assayed with the two markers. In the samples tested, 14 different alleles were detected with a size range of 180 to 224 bp for RM219 (Table 1). All japonica cultivars with the exception of Katy from the southern USA showed fragments from 2 to 14 bp smaller than DX202-9 (194 bp). Three indica cultivars, IR50, GZ 5121-5-2-1, and N22, had an allele of 2 to 10 bp smaller than DX202-9. Most indica cultivars had an allele 8 to 30 bp larger than DX202-9. Surprisingly, none of the rice cultivars except IR40931-26 had an allele in size equal to DX202-9. This would strongly indicate that this marker is highly polymorphic within this population and would be useful in a wide range of germplasm.
RM464A displayed three different alleles, with sizes of 224, 226, and 231 bp among these 55 rice accessions (Table 1), much less than the allelic variability for RM219. All 47 rice cultivars with a smaller size than DX202-9 at the RM219 locus had an RM464A allele of 231 bp with the exception of Labele (226 bp) and TESA-2 (226 bp). Seven rice cultivars possessing alleles with larger size than DX202-9 at the RM219 locus showed larger allelic variability at the RM464A locus with four having the 226-bp allele, two having the 231-bp allele, and one having the 224-bp allele. The RM464A DX202-9 amplicon was 226 bp, the same allele for six other samples in these 55 genotypes. The 231-bp allele of RM464A was present in 42 of 47 japonica genotypes, and the 224- and 226-bp alleles were mainly in indica rice (6 out of 8 genotypes). Therefore, the RM464A seemed more useful in selection for introgression of Sub1 into the japonica background than into the indica background.
MAS in the Development of the Sub1-NILs
An important objective in this study was to develop the Sub1-NILs in the M-202 background. To measure the similarity of the F2 (DX236) plants to the parent M-202, 118 microsatellite markers covering all 12 chromosomes in the rice genome (Chen et al., 1997; Temnykh et al., 2001) were used to screen the immediate parents (DX 202-9 and M202) of the F2 population. Of these 118 markers, only three (RM106, RM167, and RM189), produced fragments polymorphic between the two parents. This would indicate that these F2 plants were very similar genetically to M-202 aside from the region of Sub1 and the regions covered by the three markers (RM106, RM167, and RM189) and therefore they were valuable plant resources for the development of Sub1 NILs.
On the basis of the genotypes at the loci RM219, RM464A, RM106, RM167, RM189, and Sub1, six plants were selected from the F2 population that could be used to recover Sub1-NILs in the F3 families rapidly (data not shown). In two of these plants, two of the three loci unlinked to Sub1 and segregating in the population were homozygous for M-202 alleles and the third locus was heterozygous. Sub1 NILs could be isolated from these two plants.
|
DISCUSSION
|
|---|
This study shows that RM219 is a useful microsatellite marker for MAS for submergence tolerance in rice. Siangliw et al. (2003) also found RM219 linked to the submergence tolerance locus on chromosome 9, but they did not show its position relative to Sub1. Although the linkage between RM219 and Sub1 is quite close (3.4 cM), there will be some crossovers between the two. This marker could be used for initial screening in segregating populations. Lines with the homozygous alleles from the tolerant parent for RM219 could be screened for submergence tolerance at a later generation. As shown from this study, there were 14 alleles at the RM219 locus identified in the 55 indica and japonica rice cultivars, and none of these had the same RM219 allele as IR40931-26. This would suggest that the marker would be widely applicable in rice germplasm including indica rice. Such applicability of this marker to indica germplasm would be of great importance because flash flooding occurs more commonly in South and South East Asia, and many breeding programs in these regions seek to improve submergence tolerance of their indica rice cultivars.
On the basis of the sequence analysis, RM464A was a new codominant marker identified in this study, but it shares the same primers for RM464, a microsatellite marker (Temnykh et al., 2001). Selection for Sub1 based on RM464A should be highly reliable because of the extreme tightness of linkage (only 0.7 cM apart) between them. In practice, RM464A seems a better marker for introgression of Sub1 into japonica background than into indica background, because of similar or identical size of the RM464A fragment amplified from DX202-9 and those from most indica rice cultivars. Since rice cultivars grown in California were mostly classified as temperate japonica rice, this marker would have potential for the development of submergence tolerant lines. As shown in Fig. 2, there is a base mismatch in each of the priming regions of RM464A primers compared with the sequence of 93-11. To improve the yield and reliability of PCR reaction specific to the RM464A fragments, the two primers of RM464A should be adjusted to
 |
to eliminate the two priming mismatches, assuming that the two mismatches were introduced by the RM464 primers in PCR (Fig. 2). The base substitution from C to G at the 14th base for RM464A-R may have an important role in increasing the specificity of RM464A since the base is considerably close to the 3' end of the primer. Because both RM219 and RM464 were linked to Sub1 on one side rather than flanking Sub1 with one on each side, MAS using these two markers would be in fact based on only one of them.
The population developed in this study, which is similar to a BC2F2, is valuable in terms of providing the basis for the development of the Sub1-NILs in the background of the temperate japonica type represented by M-202. The six plants selected in the population could be considered as lines very close to Sub1-NILs. We are currently advancing these plants to later generations. The NILs to be produced should be excellent materials for the study of the physiological mechanism of submergence tolerance in rice. Whether or not these Sub1-NILs of M-202 background could be used to improve the weed control by raising water level during crop establishment remains to be tested.
|
NOTES
|
|---|
This work was supported in part by a grant from the USDA Plant Genome Program.
Received for publication November 27, 2002.
|
REFERENCES
|
|---|
- Chen, X., S. Temnykh, Y. Xu, Y.G. Cho, and S.R. McCouch. 1997. Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.). Theor. Appl. Genet. 95:553–567.[ISI]
- Lander, E.S., P. Green, J. Abrahamson, A. Barlow, M. Daly, S.E. Lincoln, and L. Newburg. 1987. Mapmaker: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181.[Medline]
- Mackill, D.J. 1995. Classifying japonica rice cultivars with RAPD markers. Crop Sci. 35:889–894.
- Mackill, D.J., M.M. Amante, B.S. Vergara, and S. Sarkarung. 1993. Improved semidwarf rice lines with tolerance to submergence of seedlings. Crop Sci. 33:749–753.[Abstract/Free Full Text]
- Mackill, D.J., W.R. Coffman, and D.P. Garrity. 1996. Rainfed lowland rice improvement Int. Rice Res. Inst., Manila.
- Mackill, D.J., Z. Zhang, E.D. Redona, and P.M. Colowit. 1996. Level of polymorphism and genetic mapping of AFLP markers in rice. Genome 39:969–977.[Medline]
- Nandi, S., P.K. Subudhi, D. Senadhira, N.L. Manigbas, S. Sen-Mandi, and N. Huang. 1997. Mapping QTLs for submergence tolerance in rice by AFLP analysis and selective genotyping. Mol. Gen. Genet. 255:1–8.[ISI][Medline]
- Redoña, E.D., and D.J. Mackill. 1996. Mapping quantitative trait loci for seedling vigor in rice using RFLPs. Theor. Appl. Genet. 92:395–402.
- Rutger, J.N., and G.W. Schaeffer. 1989. An environmentally-sensitive genetic male sterile mutant in rice. p. 98. In Agronomy Abstracts. ASA, Madison, WI.
- Setter, T.L., and E.V. Laureles. 1996. The beneficial effect of reduced elongation growth on submergence tolerance of rice. J. Exp. Bot. 47:1551–1559.
- Siangliw, M., T. Toojinda, S. Tragoonrung, and A. Vanavichit. 2003. Thai jasmine rice carrying QTLch9 (SubQTL) is submergence tolerant. Ann. Bot. 91:255–261.[Abstract/Free Full Text]
- Temnykh, S., G. DeClerck, A. Lukashova, L. Lipovich, S. Cartinhour, and S. McCouch. 2001. Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): Frequency, length variation, transposon associations, and genetic marker potential. Genome Res. 11:1441–1452.[Abstract/Free Full Text]
- Temnykh, S., W.D. Park, N. Ayres, S. Cartinhour, N. Hauck, L. Lipovich, Y.G. Cho, T. Ishii, and S.R. McCouch. 2000. Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theor. Appl. Genet. 100:697–712.[ISI]
- Vergara, B.S., and A. Mazaredo. 1975. Screening for resistance to submergence under greenhouse conditions. p. 67–70. In Proceedings of the International Seminar on Deepwater Rice. August 1974. Bangladesh Rice Res. Inst., Dhaka.
- Williams, J.F., S.R. Roberts, J.E. Hill, S.C. Scardaci, and G. Tibbits. 1990. Managing water for weed control in rice. Calif. Agric. 44(5):6–10.
- Xu, K., and D.J. Mackill. 1996. A major locus for submergence tolerance mapped on rice chromosome 9. Mol. Breed. 2:219–224.
- Xu, K., X. Xu, P.C. Ronald, and D.J. Mackill. 2000. A high-resolution linkage map in the vicinity of the rice submergence tolerance locus Sub1. Mol. Gen. Genet. 263:681–689.[ISI][Medline]
- Yu, J., S.N. Hu, J. Wang, G.K.S. Wong, S.G. Li, B. Liu, Y.J. Deng, L. Dai, Y. Zhou, X.Q. Zhang, M.L. Cao, J. Liu, J.D. Sun, J.B. Tang, Y.J. Chen, X.B. Huang, W. Lin, C. Ye, W. Tong, L.J. Cong, J.N. Geng, Y.J. Han, L. Li, W. Li, G.Q. Hu, X.G. Huang, W.J. Li, J. Li, Z.W. Liu, J.P. Liu, Q.H. Qi, J.S. Liu, T. Li, X.G. Wang, H. Lu, T.T. Wu, M. Zhu, P.X. Ni, H. Han, W. Dong, X.Y. Ren, X.L. Feng, P. Cui, X.R. Li, H. Wang, X. Xu, W.X. Zhai, Z. Xu, J.S. Zhang, S.J. He, J.G. Zhang, J.C. Xu, K.L. Zhang, X.W. Zheng, J.H. Dong, W.Y. Zeng, L. Tao, J. Ye, J. Tan, X.D. Ren, X.W. Chen, J. He, D.F. Liu, W. Tian, C.G. Tian, H.G. Xia, Q.Y. Bao, G. Li, H. Gao, T. Cao, W.M. Zhao, P. Li, W. Chen, X.D. Wang, Y. Zhang, J.F. Hu, S. Liu, J. Yang, G.Y. Zhang, Y.Q. Xiong, Z.J. Li, L. Mao, C.S. Zhou, Z. Zhu, R.S. Chen, B.L. Hao, W.M. Zheng, S.Y. Chen, W. Guo, G.J. Li, S.Q. Liu, M. Tao, L.H. Zhu, L.P. Yuan, and H.M. Yang. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp indica). Science 296:79–92.[Abstract/Free Full Text]
This article has been cited by other articles:
|
|
|
|
 
T. Fukao, K. Xu, P. C. Ronald, and J. Bailey-Serres
A Variable Cluster of Ethylene Response Factor-Like Genes Regulates Metabolic and Developmental Acclimation Responses to Submergence in Rice
PLANT CELL,
August 1, 2006;
18(8):
2021 - 2034.
[Abstract]
[Full Text]
[PDF]
|
|
|
TOP
ABSTRACT
INTRODUCTION
