RFLP facilitated analysis of tiller and leaf angles in rice (Oryza sativa L.)
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1 Euphytica 109: 79 84, Kluwer Academic Publishers. Printed in the Netherlands. 79 RFLP facilitated analysis of tiller and leaf angles in rice (Oryza sativa L.) Zhikang Li 1,2,3, Andrew H. Paterson 1, Shannon R.M. Pinson 4 & James W. Stansel 2 1 Department of Soil and Crop Sciences, Texas A&M University, College Station 77843, U.S.A.; 2 Texas A&M University System Agricultural Research and Extension Center, Route 7, Box 999, Imes Rd., Beaumont, TX 77713, U.S.A.; 3 present address: The International Rice Research Institute, P.O. Box 933, 1099 Manila, The Philippines; 4 USDA-ARS, Route 7, Box 999, Imes Rd., Beaumont, TX 77713, U.S.A. Received 30 March 1998; accepted 27 September 1998 Key words: ideotype, pleiotropy, QTLs, yield potential Summary Plant type is an important composite trait associated with the yield potential in rice and other cereal crops. Several characters associated with the plant type of modern rice cultivars including tiller angle, leaf and flag leaf angle, were investigated using a complete linkage map with 115 well distributed RFLP markers and progeny testing of 2418 F 2 derived F 4 lines from a cross between O. sativa ssp. japonica cv. Lemont and spp. indica cv. Teqing. One major gene (Ta) and 11 QTLs were largely responsible for the tremendous variation of the three plant type characters in the Lemont/Teqing F 2 population. The major gene, Ta, located between RZ228 and RG667 on chromosome 9, accounted for 47.5% of the phenotypic variation in tiller angle and had large pleiotropic effects on both leaf and flag leaf angles. This gene plus four QTLs accounted for 69.1% of the genotypic variation in tiller angle. Eight additional QTLs for leaf and flag leaf angles were also identified, which collectively explained 52.0 and 66.4% of the genotypic variation of these traits. Ta and three QTLs (QFla2,QFla5 andqfla7)apparently affected the related plant type characters differently, suggesting their possible differential expression in different developmental stages of rice plants or possibly clustering of different genes affecting these traits. Plant type, and consequently grain yield of rice, may be improved by deliberately manipulating these QTLs in a marker-assisted selection program. Introduction Ideotype is a complicated concept which includes combinations of many morphological and physiological traits into a multi-dimensional plant structure that maximizes the biomass and its partition (Donald, 1968; Donald & Hamblin, 1976; Rasmussen & Connell, 1972). This concept was associated with the development of semidwarf rice and wheat varieties in early 1960 s, which had dramatically improved the productivity of these two important crops. In addition to reduced height, the morphology of semidwarf wheat and rice cultivars is characterized by more compact plant type, associated with reduced tiller and leaf angles. This compact plant type has been considered as a major component of the ideotype in many cereal crops (Donald & Hamblin, 1976). Traditional landraces of cultivated cereals have a relatively open plant architecture, i.e. relatively larger tiller and leaf angles, which may offer advantages such as competitiveness over weeds. However, under the conditions of modern agriculture with increased application of N fertilizer, larger tiller and leaf angles may cause many problems such as shading, increased humidity favoring diseases and insects, lodging, and others. At the other extreme, a highly compact plant type with completely vertical tillers and erect leaves tends to be inefficient at utilizing solar energy at early growing stages, and is vulnerable to those insects and diseases which are transmitted by tissue contact. The ideotype that most cereal breeders have selected for tends to be intermediate between these extremes with erect leaves and relatively small tiller angle, allowing a high leaf area index (coverage of soil by leaves) without causing mutual shading. Together with reduced height and a thicker stem, this plant type has conferred modern GSB: 33 - ARTICLE: euph4862/typeset - PIPS Nr.: (euphkap:bio2fam) v.1.1 euph4862.tex; 3/08/1999; 11:05; p.1
2 80 cereal cultivars with increased response to N fertilizer and increased productivity per unit area. While application of the ideotype concept to cereal breeding has been successful, little information exists regarding the genetic basis of improved plant type in elite germplasm. Several mutants with extreme phenotypes have been mapped (Jones & Adair, 1938; Takahashi et al., 1968; Xu et al., 1998). However, these mutants are difficult to utilize in achieving the intermediate phenotype that appears to maximize the yield potential. A recent biometric study on tiller angle of improved plant type in crosses between four semidwarf indica cultivars suggested that there were at least four genetic factors or QTLs largely responsible for the transgressive segregation of tiller angle, and these inferred QTLs were non-allelic to the major mutant la (Xu et al., 1998). Unfortunately, without molecular markers, this study provided very limited information about the genes/qtls affecting tiller angle in rice. This paper describes a QTL analysis on an F 2 -derived F 4 progeny from a cross between two divergent semidwarf commercial rice cultivars which differ in both plant type and yield potential. Transgressive segregation for several plant type characters in this population, and a nearly complete RFLP linkage map allowed us to gain insights into individual genetic determinants of improved plant type in elite rice genotypes. Materials and methods Plant materials Oryza sativa L. cultivars, Lemont (the female parent, ssp. japonica) and Teqing (the male parent, ssp. indica) were used as the parents in the study. Two hundred fifty five F 2 plants from the Lemont/Teqing cross were used as the mapping population. Fifteen to thirty F 3 plants derived from each of the 255 F 2 plants were used for DNA extraction to reconstruct the marker genotypes of individual F 2 plants. A total of 2418 F 2 -derived F 4 lines from the 255 F 3 lines ( 10 F 4 lines from each of the F 3 progenys) were used for the phenotyping experiment, as described previously (Li et al., 1995). RFLP marker genotyping and the field experiment Construction of a linkage map with 115 RFLP markers for the F 2 population has been described previously (Li et al., 1995). The resulting 115 loci were spaced at an average 19.1 cm across the 12 rice chromosomes. Phenotyping of the 2418 F 4 lines was conducted in 1990 at the Texas A&M University System Agricultural Research & Extension Center in Beaumont. The F 4 lines were drill planted in family groups separated by two parental plots with each F 4 line in a single row plot 2.4 m long and a spacing of 28 cm between rows. Three characters associated with plant type were measured, including tiller angle (TA) which was scored visually at peak tillering (approximately 90 days after seeding), and flag leaf angle (FLA) and leaf angle under the flag leaf (LA) which were scored 3-5 days after panicles emerged from the flag leaf sheath. The scoring was taken on each of the F 4 line rows based on the standard scale of 1 7 scores in which 1 indicated an angle of zero degree with the stem (completely erect), and 7 indicating an angle larger than 90 degrees with the stem (IRRI, 1985). Breeding values of the 255 F 2 plants, calculated from the mean of their 10 derived F 4 lines, were used in analyses of each trait. Data analysis Quantitative trait loci (QTLs) were identified in two steps. First, putative QTLs were identified using interval mapping with a threshold of LOD 2.4 using both MapMaker/QTL and ANOVA (p 0.002) (Li et al., 1997a). Then, all putative QTLs identified in the first step were re-evaluated using multiple-qtl interval models (MapMaker/QTL) and multiple regression models (Li et al., 1997a), in which all intervals (QTLs) were sequentially fitted starting with the interval (QTL) having the largest LOD. Intervals (QTLs) with the next largest LOD (F value) were added to the model and kept if the interval (QTL) increased the overall LOD of the model by 2.0 or greater. Gene actions for individual QTLs were estimated in the multiple-qtl models. Results Trait variation Lemont had a mean score of 1.4 (approximately 8 degrees) for TA, 2.2 (18 degrees) for LA, and 2.6 (25 degrees) for FLA. Teqing had a larger TA (3.0 or 30 degrees), but virtually erect leaves and flag leaves with a mean score of 1.2 and 1.3 (< 5 degrees) for LA and FLA, respectively. The differences between the parents for the three characters were relatively small but statistically significant (p < in ANOVA). euph4862.tex; 3/08/1999; 11:05; p.2
3 81 Figure 1. Histograms of the frequency distribution of the breeding values in the Lemont/Teqing F 2 population for three plant type characters tiller angle (TA), leaf angle (LA), and flag leaf angle (FLA), respectively. euph4862.tex; 3/08/1999; 11:05; p.3
4 82 Figure 2. Chromosomal locations of the major gene Ta, and 11 QTLs affecting three plant type characters in the Lemont Teqing cross. Mean scores of the F 2 plants for the three characters showed considerable transgressive segregation (particularly for TA and FLA), as indicated by the observation that a significant proportion (> 25%) of the F 2 plants had significantly greater or smaller mean scores than the parental scores (Figure 1). LA showed a normal distribution but TA and FLA exhibited a slightly skewed distribution. Data transformation did not improve normality. Broad sense heritability estimates were 0.95, 0.84 and 0.92 for TA, LA and FLA, respectively. The genotypic correlation was 0.49 (p < ) between TA and LA, 0.48 (p < ) between TA and FLA, and 0.65 (p < ) between LA and FLA, respectively, suggesting overlapping genetic control of the 3 characters. Interval mapping of QTLs One major gene and 11 QTLs influencing the three plant type characters were identified using both interval mapping and multiple regression models. These QTLs mapped to 8 of the 12 rice chromosomes (Figure 2) and collectively explained 69.1%, 52.0% and 66.4% of the genotypic variation for TA, LA and FLA, respectively. Tiller angle A major gene and four QTLs affecting TA were mapped to 5 (1, 2, 5, 8 and 9) different rice chromosomes (Table 1). The major gene, designated Ta,fell in the interval of 11 cm between RZ228 and RG667 on chromosome 9 with a LOD score of 32.3, explaining 47.5% of phenotypic variation of TA. The Teqing allele at this locus had an additive effect of 0.82 (approximately 12 degrees) for increased TA, and large euph4862.tex; 3/08/1999; 11:05; p.4
5 83 Table 1. Biometric parameters for Teqing alleles at one major gene and eleven QTLs affecting tillering (TA), leaf angle (LA) and flag leaf angle (FLA) in the Lemont/Teqing cross QTLs Trait Marker interval a Chrom. a b R 2 (%) LOD Ta TA RZ228/RG LA FLA QTa2 TA RG171/RG QTa8 TA RG20/RG QTa5 TA gl-1/rg QTa1 TA RG173/RG QLa3 LA RG104/RG QLa1 LA RG381/CDO388a QFla2 FLA RZ260/RG598b LA QFla5 FLA RG470/RG TA LA QFla6 FLA C/RG QFla7 FLA RG711/RZ LA QFla9 FLA RG757/RG a The underlined markers are those closer to LOD peaks of the detected QTLs. a and d are additive and dominance effects of the identified QTLs. All genetic parameters and LOD scores associated with the identified QTLs are estimates obtained from the multiple-qtl models using Mapmaker/QTL. pleiotropic effects (0.36) on both LA and FLA. The other four QTLs had relatively small additive effects ranging from 0.18 to 0.28 units. One of these QTLs (QTa2) showed heterosis for increased tillering angle, as reflected by a large dominance effect but a small additive effect. The Lemont allele at Ta and QTa1 resulted in reduced TA, while the Teqing allele at the remaining three QTLs reduced TA. Leaf and flag leaf angle Five QTLs influencing FLA mapped to 5 rice chromosomes (Chromosomes 2, 5, 6, 7, and 9) (Table 1 andfigure1).oneqtl,qfla5 detected with a LOD score of 7.8 also had a significant effect on both TA and LA. Two other QTLs, QFla2 andqfla7 influenced both FLA and LA. Two QTLs (QLa1, and QLa3) affected LA only. The Teqing alleles at most QTLs(5forLAand4forFLA)resultedinreduced leaf angle, with the exception of QFla9(Table1). Discussion The male parent, Teqing, which is among the highest yielding commercial rice cultivars in China, represents a new generation of ideotype called fast tillering and growing type (Huang et al., 1983; Xiong et al., 1988). The plant type of Teqing is characterized by a relatively large tiller angle and fast growth rates at seedling and tillering stages, and more compact (smaller tiller and leaf angle) at later stages such that a high level of leaf area/unit land and thus a high photosynthesis rate are maintained throughout plant growth (Huang et al., 1983). The female parent, Lemont is a Southern US semidwarf commercial rice cultivar with good yield potential. It has smaller TA but large LA and FLA. However, Teqing yields 30 50% more than Lemont even grown under Southern US conditions (direct seeding). We found that such a big yield difference between the parents could have partially been attributable to their differences at many gene/qtls influencing plant type. Using DNA markers, we were able to identify a major gene and many QTLs which were largely responsible for the difference in these plant type related characters between the parentallines. Ta identified between RZ228 and RG667 on chromosome 9, has the largest effect on all three plant type characters. Unlike the mutant gene, La (lazy growth habit) which causes euph4862.tex; 3/08/1999; 11:05; p.5
6 84 extremely large tiller angle and reported locates on chromosome 11 (Jones & Adair, 1938; Takahashi et al., 1968; Kinoshita & Takahashi, 1991), Ta does not cause extreme spreading habit. Although the Teqing allele at Ta is associated with increased TA, LA and FLA, it has no negative effect on grain yield or its components (Li et al., 1997a, 1997b). The F 4 lines with very large TA (all fixed with Teqing allele at Ta) tended to grow more vigorously at earlier stages and produced more panicles, suggesting that the Teqing allele at this locus might be associated with strong seedling vigor. In addition to Ta, two QTLs, QFla2 andqfla5 also had large phenotypic effects. The Teqing allele at QFLa2 has large effects on both FLA and LA. A single recessive gene, er (o), for erect growth habit reportedly locates on chromosome 5, but its precise location on the chromosome 5 remains unknown (Takahashi et al., 1968; Kinoshita & Takahashi, 1991). QFla5 detected in this study is expected to have a large effect on the compactness of rice plants since it influences all three plant type characters studied. An additional QTL, QTa5 was mapped between gl-1 and RG403 on chromosome 5. The relationship between QFla5 or QTa5ander (o) remains unclear. It is interesting to note that the phynotypic effects of the detected genes/qtls on the three plant type characters appear to show different patterns. Ta had a very large effect on TA (detected with the largest LOD) behaving as a major gene, but relatively small effects on LA and FLA, acting as a QTL. In contrast, QFla2andQFla5 had greater effects on FLA (detected with much larger LOD scores) but smaller effects on TA and LA. Genetically, this could be due either to the differential pleiotropic effects of the same genes on different related traits, or to the tight linkage of several genes affecting different traits. Regardless, the parental allelic combinations at these QTLs, as a result of selection, has very significant consequences on the net photosynthesis rate of rice plants in different developmental stages. For instance, it is conceivable that at the early growth stages when total leaf area is small and solar radiation is less intense, an open plant structure caused by the Teqing allele at Ta may result in an increased photosynthetic rate at equivalent planting densities. At the later stages, the weaker effect of the Teqing allele on increased LA and FLA can be easily compensated by its alleles at other QTLs such as QFla2 andqfla5 which cause more erect growth habit and allow greater total leaf area/unit land without much shading. Such a multi-locus allelic combination at many genes/qtls might have conferred a well-balanced phenotype leading to a higher photosynthetic rate throughout the whole growth period and the new fast tillering and growing type with increased yield potential (Huang et al., 1983). With these plant type genes/qtls mapped with closely linked DNA markers, it is possible to select and combine different alleles at many loci through marker-assisted selection to create optimal ideotypes for a diverse range of target environments. Acknowledgement We thank S.D. Tanksley and S.R. McCouch of Cornell University for providing us with the DNA probes. This research was supported by Texas A&M University System Agricultural Research and Extension Center; Texas Rice Research Foundation; and through a grant (# ) from the Texas Advance Technology Program to Z Li/JW Stansel. References Donald, C.M., The breeding of crop ideotypes. Euphytica 17: Donald, C.M. & J. 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