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OsLG3 contributing to rice grain length and yield was mined by Ho-LAMap

View Article: PubMed Central - PubMed

ABSTRACT

Background: Most agronomic traits in rice are complex and polygenic. The identification of quantitative trait loci (QTL) for grain length is an important objective of rice genetic research and breeding programs.

Results: Herein, we identified 99 QTL for grain length by GWAS based on approximately 10 million single nucleotide polymorphisms from 504 cultivated rice accessions (Oryza sativa L.), 13 of which were validated by four linkage populations and 92 were new loci for grain length. We scanned the Ho (observed heterozygosity per locus) index of coupled-parents of crosses mapping the same QTL, based on linkage and association mapping, and identified two new genes for grain length. We named this approach as Ho-LAMap. A simulation study of six known genes showed that Ho-LAMap could mine genes rapidly across a wide range of experimental variables using deep-sequencing data. We used Ho-LAMap to clone a new gene, OsLG3, as a positive regulator of grain length, which could improve rice yield without influencing grain quality. Sequencing of the promoter region in 283 rice accessions from a wide geographic range identified four haplotypes that seem to be associated with grain length. Further analysis showed that OsLG3 alleles in the indica and japonica evolved independently from distinct ancestors and low nucleotide diversity of OsLG3 in indica indicated artificial selection. Phylogenetic analysis showed that OsLG3 might have much potential value for improvement of grain length in japonica breeding.

Conclusions: The results demonstrated that Ho-LAMap is a potential approach for gene discovery and OsLG3 is a promising gene to be utilized in genomic assisted breeding for rice cultivar improvement.

Electronic supplementary material: The online version of this article (doi:10.1186/s12915-017-0365-7) contains supplementary material, which is available to authorized users.

No MeSH data available.


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Breeding improvement of OsLG3. a Phylogenetic analysis of four grain length-related genes in 480 accessions. The phylogenetic tree of 480 varieties was constructed based on different functional SNPs or indels (listed in Additional file 32: Table S1) by MAGE 6.0. All varieties were categorized by allelic variations in the FNP of OsLG3, GS3, GW8, and TGW6. The red pentagram refers to the beneficial allele of gs3, yellow dot to the beneficial allele of OsLG3, blue triangle to the beneficial allele of GW8, purple prism to the beneficial allele of TGW6, black lines to landrace varieties and green lines to improved varieties. Different colors reflect the different subgroups, with its abbreviation as in Fig. 4. b Improvement of haplotype combination for four grain length-related genes, as in a. Top numbers indicate average grain length; bottom numbers correspond to accessions number with a type of haplotype combination in the subgroup. c Spectra of allele frequencies comparing landrace and improved varieties at the causal polymorphisms of GS3, OsLG3, GW8, and TGW6 during modern breeding in the respective subgroups. LAN landraces, IMP improved varieties
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Fig6: Breeding improvement of OsLG3. a Phylogenetic analysis of four grain length-related genes in 480 accessions. The phylogenetic tree of 480 varieties was constructed based on different functional SNPs or indels (listed in Additional file 32: Table S1) by MAGE 6.0. All varieties were categorized by allelic variations in the FNP of OsLG3, GS3, GW8, and TGW6. The red pentagram refers to the beneficial allele of gs3, yellow dot to the beneficial allele of OsLG3, blue triangle to the beneficial allele of GW8, purple prism to the beneficial allele of TGW6, black lines to landrace varieties and green lines to improved varieties. Different colors reflect the different subgroups, with its abbreviation as in Fig. 4. b Improvement of haplotype combination for four grain length-related genes, as in a. Top numbers indicate average grain length; bottom numbers correspond to accessions number with a type of haplotype combination in the subgroup. c Spectra of allele frequencies comparing landrace and improved varieties at the causal polymorphisms of GS3, OsLG3, GW8, and TGW6 during modern breeding in the respective subgroups. LAN landraces, IMP improved varieties

Mentions: To dissect the genetic interaction between OsLG3 and other genes controlling grain length, we analyzed the promoter sequences of OsLG3 and various haplotypes of GS3, GW8, TGW6, GW2, and GL3.1 in 498 accessions (Additional file 32: Table S1, Additional file 33: Table S2). By re-sequencing our germplasm resources, we found that the alleles of GW2 and GL3.1 responsible for longer grains were quite rare. We then investigated OsLG3, GS3, GW8, and TGW6 and analyzed the association between their grain length and allelic variants. All varieties were categorized by allelic variations in the functional nucleotide polymorphisms (FNPs) of OsLG3, GS3, GW8, and TGW6. The beneficial allele of OsLG3 had an epistatic effect on grain length for GW8 and TGW6; however, the beneficial allele of GS3 had a recessive epistatic effect on grain length for OsLG3 (Fig. 5a–c and Additional file 26: Figure S26). Our results suggest these loci cooperatively regulate grain length in rice, as accessions with the same haplotype for a given gene exhibited grain length diversity, and that variations at OsLG3 and GS3 are major factors affecting grain length diversity on a wide range of genetic backgrounds (Fig. 6a). Phylogenetic analysis showed that landrace varieties and improved varieties in the indica group were distinguished remarkably on account of improvement of grain length, although it fitted well within the japonica group. This indicated that grain length in indica rice has been widely improved by the presence of beneficial alleles of GS3 and OsLG3, whereas there remains room for improvement for grain length in japonica (Fig. 6a, c and Additional file 27: Figure S27). In the japonica group, grain of some improved varieties was significantly longer because of introgression of the beneficial allele of OsLG3 (Fig. 6a, b). Our results suggest that OsLG3 has potential for improvement of grain length in japonica.Fig. 5


OsLG3 contributing to rice grain length and yield was mined by Ho-LAMap
Breeding improvement of OsLG3. a Phylogenetic analysis of four grain length-related genes in 480 accessions. The phylogenetic tree of 480 varieties was constructed based on different functional SNPs or indels (listed in Additional file 32: Table S1) by MAGE 6.0. All varieties were categorized by allelic variations in the FNP of OsLG3, GS3, GW8, and TGW6. The red pentagram refers to the beneficial allele of gs3, yellow dot to the beneficial allele of OsLG3, blue triangle to the beneficial allele of GW8, purple prism to the beneficial allele of TGW6, black lines to landrace varieties and green lines to improved varieties. Different colors reflect the different subgroups, with its abbreviation as in Fig. 4. b Improvement of haplotype combination for four grain length-related genes, as in a. Top numbers indicate average grain length; bottom numbers correspond to accessions number with a type of haplotype combination in the subgroup. c Spectra of allele frequencies comparing landrace and improved varieties at the causal polymorphisms of GS3, OsLG3, GW8, and TGW6 during modern breeding in the respective subgroups. LAN landraces, IMP improved varieties
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5383996&req=5

Fig6: Breeding improvement of OsLG3. a Phylogenetic analysis of four grain length-related genes in 480 accessions. The phylogenetic tree of 480 varieties was constructed based on different functional SNPs or indels (listed in Additional file 32: Table S1) by MAGE 6.0. All varieties were categorized by allelic variations in the FNP of OsLG3, GS3, GW8, and TGW6. The red pentagram refers to the beneficial allele of gs3, yellow dot to the beneficial allele of OsLG3, blue triangle to the beneficial allele of GW8, purple prism to the beneficial allele of TGW6, black lines to landrace varieties and green lines to improved varieties. Different colors reflect the different subgroups, with its abbreviation as in Fig. 4. b Improvement of haplotype combination for four grain length-related genes, as in a. Top numbers indicate average grain length; bottom numbers correspond to accessions number with a type of haplotype combination in the subgroup. c Spectra of allele frequencies comparing landrace and improved varieties at the causal polymorphisms of GS3, OsLG3, GW8, and TGW6 during modern breeding in the respective subgroups. LAN landraces, IMP improved varieties
Mentions: To dissect the genetic interaction between OsLG3 and other genes controlling grain length, we analyzed the promoter sequences of OsLG3 and various haplotypes of GS3, GW8, TGW6, GW2, and GL3.1 in 498 accessions (Additional file 32: Table S1, Additional file 33: Table S2). By re-sequencing our germplasm resources, we found that the alleles of GW2 and GL3.1 responsible for longer grains were quite rare. We then investigated OsLG3, GS3, GW8, and TGW6 and analyzed the association between their grain length and allelic variants. All varieties were categorized by allelic variations in the functional nucleotide polymorphisms (FNPs) of OsLG3, GS3, GW8, and TGW6. The beneficial allele of OsLG3 had an epistatic effect on grain length for GW8 and TGW6; however, the beneficial allele of GS3 had a recessive epistatic effect on grain length for OsLG3 (Fig. 5a–c and Additional file 26: Figure S26). Our results suggest these loci cooperatively regulate grain length in rice, as accessions with the same haplotype for a given gene exhibited grain length diversity, and that variations at OsLG3 and GS3 are major factors affecting grain length diversity on a wide range of genetic backgrounds (Fig. 6a). Phylogenetic analysis showed that landrace varieties and improved varieties in the indica group were distinguished remarkably on account of improvement of grain length, although it fitted well within the japonica group. This indicated that grain length in indica rice has been widely improved by the presence of beneficial alleles of GS3 and OsLG3, whereas there remains room for improvement for grain length in japonica (Fig. 6a, c and Additional file 27: Figure S27). In the japonica group, grain of some improved varieties was significantly longer because of introgression of the beneficial allele of OsLG3 (Fig. 6a, b). Our results suggest that OsLG3 has potential for improvement of grain length in japonica.Fig. 5

View Article: PubMed Central - PubMed

ABSTRACT

Background: Most agronomic traits in rice are complex and polygenic. The identification of quantitative trait loci (QTL) for grain length is an important objective of rice genetic research and breeding programs.

Results: Herein, we identified 99 QTL for grain length by GWAS based on approximately 10 million single nucleotide polymorphisms from 504 cultivated rice accessions (Oryza sativa L.), 13 of which were validated by four linkage populations and 92 were new loci for grain length. We scanned the Ho (observed heterozygosity per locus) index of coupled-parents of crosses mapping the same QTL, based on linkage and association mapping, and identified two new genes for grain length. We named this approach as Ho-LAMap. A simulation study of six known genes showed that Ho-LAMap could mine genes rapidly across a wide range of experimental variables using deep-sequencing data. We used Ho-LAMap to clone a new gene, OsLG3, as a positive regulator of grain length, which could improve rice yield without influencing grain quality. Sequencing of the promoter region in 283 rice accessions from a wide geographic range identified four haplotypes that seem to be associated with grain length. Further analysis showed that OsLG3 alleles in the indica and japonica evolved independently from distinct ancestors and low nucleotide diversity of OsLG3 in indica indicated artificial selection. Phylogenetic analysis showed that OsLG3 might have much potential value for improvement of grain length in japonica breeding.

Conclusions: The results demonstrated that Ho-LAMap is a potential approach for gene discovery and OsLG3 is a promising gene to be utilized in genomic assisted breeding for rice cultivar improvement.

Electronic supplementary material: The online version of this article (doi:10.1186/s12915-017-0365-7) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus