QTL analysis of flag leaf in barley (Hordeum vulgare L.) for morphological traits and chlorophyll content

QTL analysis of flag leaf in barley ( Hordeum vulgare L.) for morphological traits and chlorophyll content 1 2 first-author 3 4 1 1 1 corresp ‡Corresponding Author ‡Corresponding Author †E-mail:zhanggp@zju.edu.cn †E-mail:zhanggp@zju.edu.cn zhanggp@zju.edu.cn Agronomy Department, Zhejiang University, Hangzhou 310029, China Agronomy Department, Zhejiang University, Hangzhou 310029, China College of Life and Environment Sciences, Hangzhou Normal University, Hangzhou 310036, China College of Life and Environment Sciences, Hangzhou Normal University, Hangzhou 310036, China College of Agronomy, Henan University of Science and Technology, Luoyang 471003, China College of Agronomy, Henan University of Science and Technology, Luoyang 471003, China Tasmanian Institute of Agricultural Research and School of Agricultural Science, University of Tasmania, Kings Meadows, TAS 7249, Australia Tasmanian Institute of Agricultural Research and School of Agricultural Science, University of Tasmania, Kings Meadows, TAS 7249, Australia To understand genetic patterns of the morphological and physiological traits in flag leaf of barley, a double haploid (DH) population derived from the parents Yerong and Franklin was used to determine quantitative trait loci (QTL) controlling length, width, length/width, and chlorophyll content of flag leaves. A total of 9 QTLs showing significantly additive effect were detected in 8 intervals on 5 chromosomes. The variation of individual QTL ranged from 1.9% to 20.2%. For chlorophyll content expressed as SPAD value, 4 QTLs were identified on chromosomes 2H, 3H and 6H; for leaf length and width, 2 QTLs located on chromosomes 5H and 7H, and 2 QTLs located on chromosome 5H were detected; and for length/width, 1 QTL was detected on chromosome 7H. The identification of these QTLs associated with the properties of flag leaf is useful for barley improvement in breeding programs. Barley ( Hordeum vulgare L.) Double haploid (DH) Flag leaf Quantitative trait loci (QTL) INTRODUCTION 1 Barley ( Hordeum vulgare L.) is one of the most important cereal crops in the world, ranking the forth in terms of planting area only after wheat, rice and maize (FAO, 2005 2005 ). It has wide use, mainly for malting, feed and food. With economic development, more and more barley will be needed for beer processing and animal feed. Hence, improvement of yield potential has been a major objective in barley breeding programs. Grain yield increase would be effectively rested with the basis of the capabilities of yield components and other closely associated traits (Sharma et al., 2003 2003 ). In cereal crops, the top three leaves on the stem, especially the top-most leaf, i.e., flag leaf, are the primary source of carbohydrates production (Sicher, 1993 1993 ). The flag leaf could produce a large proportion of the carbohydrates stored in grains (Li et al., 1998 1998 ). The morphological traits of flag leaf such as size and shape, and physiological traits of flag leaf such as chlorophyll content and photosynthesis capacity have been considered to be the important determinants of grain yield in cereals (Chen et al., 1995 1995 ; Hirota et al., 1990 1990 ). Therefore, flag leaf is one of the greatest components in determining grain yield potential in cereal crops. In barley, the importance of flag leaf in determining grain yield was also intensively studied (Thorne, 1965 1965 ; Tungland et al., 1987 1987 ; Yap and Harvey, 1972 1972 ; Zheng, 1999 1999 ). It was found that some flag leaf traits, such as length, width and angle, were inherited quantitatively (Yang and Lu, 1991 1991 ). Meanwhile, quantitative trait loci (QTL) mapping provides a powerful tool to study complex traits at the molecular level, and considerable progress has been made in the genetic research on yield, yield components, and malting quality traits in barley (Backes et al., 1995 1995 ; Baum et al., 2003 2003 ; Bezant et al., 1997 1997 ; Kjaer and Jensen, 1996 1996 ; Li J.Z. et al., 2005 2005 ; 2006 2006 ; Marquez-Cedillo et al., 2001 2001 ; Mather et al., 1997 1997 ; Sameri et al., 2006 2006 ; Thomas et al., 1995 1995 ; Yin et al., 1999 1999 ). However, little research has been done in understanding of genetic mechanisms for flag leaf traits in barley. The objectives in this study were to elucidate the genetics of length, width, length/width and chlorophyll content of flag leaf in barley by QTL mapping using a double haploid (DH) population. MATERIALS AND METHODS 1 Plant materials and growing conditions 2 A DH population was derived from a cross between Yerong (six-rowed) and Franklin (two-rowed) (Li H. et al., 2006 2006 ; Wenzl et al., 2006 2006 ). The two parents show the distinct difference in flag leaf traits. The 154 DH lines and their parent lines (Yerong and Franklin lines) were planted in the experimental farm of Huajiachi Campus, Zhejiang University, Hangzhou, China (30°10′ N, 120°12′ E) in the barley growing season. The seeds were sown on early November in 2006. The plot consisted of 156 lines with line length of 2 m and line interval of 0.25 m, and there were 3 replications for each DH line or parent. Fifty seeds were sown in a line. Prior to seeding, 70 kg/ha of N as urea and 180 kg/ha of potassium chloride were applied. Another 70 kg/ha of N was top-dressed at 4-leaf stage. Measurements 2 During 10 d after heading, 5 plants were randomly selected from each DH line and parent to measure flag leaf length (FL, from the base of ligula to the tip of leaf, in cm) and width (FW, the widest part of the leaf, in cm), and flag leaf length/width (FLW or FL/FW) was calculated. Meanwhile, chlorophyll content of flag leaf (FC) was determined with a non-destructive method at the mid position of flag leaf using a portable fluorometer (SPAD-502, Minolta, Japan). Data and QTL analysis 2 Population distribution and correlation analysis were performed using SPSS 11.0 statistical software for all the traits measured in this study. The genetic linkage map was constructed using a total of 408 DArT (diversity arrays technology), SSR (simple sequence repeat) and other markers as described by Wenzl et al.( 2006 2006 ). QTL analysis was performed using software QTLMapper 1.60 that was developed based on the mixed linear model approach (Wang et al., 1999 1999 ; 2003 2003 ) to identify QTL with main-effect. QTL was determined with threshold P < 0.005. The threshold of LOD (likelihood odds ratio) > 2.5 was chosen for claiming a putative QTL. The nomenclature of QTL followed the system of McCouch et al.( 1997 1997 ). RESULTS 1 Phenotypic variation and correlation analysis 2 Phenotypes of the DH lines and the two parents were evaluated for the 4 flag leaf traits, and the grand means, ranges, skewness and kurtosis of measured traits were summarized in Table 1 1 . For FC, FL and FLW of the two-rowed parent Franklin were 50.4, 20.2 cm and 14.4, respectively, being larger than those of the six-rowed parent Yerong (Table 1 1 ). The FC, FL, FW and FLW of 154 DH lines averaged 47.4, 15.5 cm, 1.4 cm and 11.1, respectively. The segregation of these traits was continuously distributed among all the DH lines, but showed significant transgressive distribution. The kurtosis and skewness for all the traits were less than 1, indicating their normal distribution. Additionally, transgressive segregation in both directions was observed for all traits, indicating that both parents transmitted favorable alleles for each trait (Table 1 1 ). FC: chlorophyll content of flag leaf; FL: flag leaf length; FW: flag leaf width; FLW: length/width of flag leaf 2 Trait 2 Yerong 2 Franklin 4 DH population Mean± SD Range Skewness Kurtosis  FC 46.9 50.4 47.4±0.27 37.8~55.1 −0.217 0.043  FL 13.4 cm 20.2 cm (15.5±0.26) cm 9.2~26.2 cm 0.861 0.639  FW 1.5 cm 1.4 cm (1.4±0.01) cm 1.0~2.0 cm 0.263 0.163  FLW 8.9 14.4 11.1±0.13 7.9~15.7 0.494 0.120 The results of correlation analysis between the flag leaf traits are shown in Table 2 2 . FL was significantly and positively correlated with FW ( r =0.679, P < 0.01) and FLW ( r =0.781, P < 0.01), but there was no significant correlation between FW and FLW. In addition, no significant correlation was detected between FC and FL, FW, although there was a positive correlation between FC and FLW ( r =0.171, P < 0.05), indicating that chlorophyll content in the flag leaves of barley was associated with flag leaf length/width. FC: chlorophyll content of flag leaf; FL: flag leaf length; FW: flag leaf width; FLW: length/width of flag leaf; NS: not significant significant at 95% probability level highly significant at 99% probability level Trait FC FL FW  FL NS  FW NS 0.679 ** **  FLW 0.171 * * 0.781 ** ** NS QTL analysis 2 A total of 9 QTLs for the examined flag leaf traits were mapped on barley chromosomes 2H, 3H, 5H, 6H and 7H. The main effects of these QTLs are shown in Table 3 3 and Fig. 1 1 . Individual QTL is designated with the italicized abbreviation of the trait and the chromosome number. When more than one QTL affecting a trait is identified on the same chromosome, they are distinguished by decimal numbers; Chromosome number; Maximum-likelihood LOD score for the QTL calculated by QTLMapper 1.60; Additive effect. The positive or negative value indicates that allele from Yerong or Franklin increases the trait score, respectively; Variation explained by the putative QTL Trait QTL a a Chr. b b Interval LOD c c Add. d d Var. (%) e e  FC qFC2.1 2H bPb-8750~bPb-4875 3.12 0.88 6.4   qFC2.2 2H Bmag0518~Bmac0093 8.86 1.56 20.2   qFC3 3H bPb-5892~bPb-7938 3.88 0.87 6.3   qFC6 6H bPb-3202~bPb-4246 2.77 −0.90 6.7  FL qFL5 5H bPb-7854~bPb-4971 3.08 0.76 5.7   qFL7 7H bPb-9563~bPb-9948 2.84 0.78 5.9  FW qFW5.1 5H bPb-9719~bPb-5532 15.34 0.08 18.3   qFW5.2 5H bPb-0171~bPb-7046 3.22 0.03 2.6  FLW qFLW7 7H bPb-9563~bPb-9948 3.21 0.22 1.9 FC: flag leaf chlorophyll content; FL: flag leaf length; FW: flag leaf width; FLW: flag leaf length/width. The distances between markers (cM) are listed to the left of each figure part Four putative QTLs for chlorophyll content were detected on chromosomes 2H, 3H and 6H. Of these, individual QTL explained the variation from 6.3% to 20.2% of the total phenotypic variation, with QTL qFC2.2 having the largest effect. The alleles in the direction of increasing FC for the QTL qFC6 came from Franklin, while those for the others ( qFC2.1 , qFC2.2 and qFC3 ) came from Yerong. Two putative QTLs ( qFL5 and qFL7 ) for flag leaf length were detected on chromosomes 5H and 7H, respectively. The additive effects of the two QTLs were positive, indicating that the alleles from Yerong increased the FL. Two QTLs ( qFW5.1 and qFW5.2 ) significantly affecting flag leaf width were detected on chromosome 5H and the additive effect was from Yerong allele. qFW5.1 was a major QTL, which could explain 18.3% of the total phenotypic variation. One QTL ( qFLW7 ) affecting flag leaf length/width was located on chromosome 7H, and its allele from Yerong could increase FLW. Interestingly, qFLW7 and qFL7 were located on the same region of chromosome 7H. DISCUSSION 1 The current results indicate that the 4 traits of flag leaf in the 2 parents and 154 DH lines were quantitatively inherited and could be controlled by multiple genes. The mean values of the population were quite close to the mid-parental values for all traits (Table 1 1 ). In addition, significant variation and normal distribution of all traits measured in this study suggest the suitability of the population for QTL analysis. The improvement in agronomic and physiological traits of flag leaf has been a major objective in rice breeding program. Analysis of QTL controlling morphological and agronomic traits of flag leaf in rice has been intensively investigated (Kang et al., 1999 1999 ; Kobayashi et al., 2003 2003 ; Li et al., 2000 2000 ; Mei et al., 2005 2005 ; Yue et al., 2006 2006 ). In barley, there were some reports concerning the relationships between yield and barley plant type, including flag leaf traits (Tungland et al., 1987 1987 ; Yap and Harvey, 1972 1972 ). However, genetic control of flag leaf traits has been rarely reported in barley up to date. Gyenis et al.( 2007 2007 ) detected 30 QTLs controlling 13 morphological traits including flag leaves at 2 to 4 environments using a BC 2 F 8 population from cultivated Harrington and wild accession OUH602 based on 113 SSR markers. They detected 3 QTLs for flag leaf length on chromosomes 3H, 5H and 7H, and 3 QTLs for flag leaf width on chromosomes 2H, 4H and 5H. In the present study, we detected 2 QTLs ( qFL5 and qFL7 ) for flag leaf length on the chromosomes 5H and 7H, and 2 QTLs ( qFW5.1 and qFW5.2 ) for leaf width on chromosome 5H. However, the QTLs controlling length on the chromosome 3H and the QTLs controlling width on chromosomes 2H and 4H were not found. Moreover, fine regions of these QTLs located on the same chromosomes cannot be compared due to the difference in parents, population types, and molecular markers used in the two studies. In addition, the QTL associated with FLW was detected on the same interval with qFL7 , and was also supported by significantly positive correlation ( r =0.781, P < 0.01) between the two traits. The result indicates that close linkage or pleiotropy existed for the two traits, and thus the locus may be useful for marker-assistant selection (MAS) in barley improvement. It was reported that leaf chlorophyll content was positively correlated with photosynthetic capacity (Araus et al., 1997 1997 ) and high chlorophyll content in leaves was considered as a favorable trait in crop production (Teng et al., 2004 2004 ). QTL for leaf chlorophyll content was rarely reported previously in barley. Chlorophyll content as a drought tolerance criterion was studied, and more than 10 QTLs were identified on chromosomes 2H, 4H, 5H, 6H and 7H using an RIL (recombinant inbred line) population under two water treatments (This et al., 2000 2000 ). However, the measurement of chlorophyll content was conducted at early growth stage in these studies. Recently, Guo et al.( 2008 2008 ) detected 5 QTLs on chromosomes 2H and 4H associated with chlorophyll content in flag leaves at post-flowering stage under well-watered and drought conditions using an RIL population with 194 lines. In the present study, a total of 4 QTLs controlling FC were mapped on chromosomes 2H, 3H and 6H. However, no similar QTL was found in the current study as that reported previously, indicating that the QTLs detected in the present study were new QTLs for chlorophyll content of flag leaf. In addition, the QTL ( qFC2.2 ) located within interval Bmag0518~Bmac0093 accounted for 20.2% of the phenotypic variation, indicating its importance in determining chlorophyll content of flag leaf and potential use in breeding programs. 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Effects of some photosynthetic organs on milking and grain yield of barley 10.1631/jzus.B0820105 Project supported by the National Natural Science Foundation of China (No. 30630047) and the Project on Absorption of Intellects by Institutions of Higher Education for Academic Disciplinary Innovations (the 111 Project) (No. B06014), China 2008-04-004 2008-11-17 2008-09-23 2022-01-05 Copyright © 2008, Journal of Zhejiang University Science 2008 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 12 09