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Download references. Ambika, Venkatraman Hegde, C. You can also search for this author in PubMed Google Scholar. All authors read and approved the final manuscript.
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Sci Rep 11, Download citation. Received : 09 May Accepted : 27 October Published : 08 November Anyone you share the following link with will be able to read this content:.
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If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate. Advanced search. Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily. Skip to main content Thank you for visiting nature. Download PDF. Subjects Agricultural genetics Plant breeding Plant genetics. Abstract Chickpea Cicer arietinum L. Introduction Chickpea Cicer arietinum L.
Following were the main objectives of this study: i To confirm and elucidate the genetics of semi-determinant growth habit, and ii To identify molecular markers linked to stem growth habit using bulked segregant analysis BSA.
Figure 1. Full size image. Table 1 Segregation for stem growth habit in F 2 of a chickpea cross involving indeterminate and semi-determinate parents. Full size table. Table 2 Segregation for stem growth habit in F 3 of a chickpea cross involving indeterminate and semi-determinate parents.
Figure 2. Figure 3. Genetics of stem growth habit F 1 and F 2 plants along with parental genotypes were screened for the trait stem growth habit for inheritance studies. Gel electrophoresis and visualization of amplicons Amplified PCR products were separated on 3 per cent agarose media.
Parental polymorphic survey and bulked segregant analysis Parental polymorphism between BG and BG was examined using SSR markers 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 Supplementary Table S1. Data availability All data generated or analysed during this study are included in this published article and its Supplementary Information files. References 1. Article Google Scholar 5. Article Google Scholar 7.
Article Google Scholar 8. Google Scholar 9. Article Google Scholar Google Scholar Nimmy Authors Ambika View author publications. View author publications. Ethics declarations Competing interests The authors declare no competing interests. Additional information Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information. Supplementary Tables. There was an error. General Comment Yeah, it's addiction. He just keeps taking drug after drug. And wants someone to save him.
General Comment Song is one of my favorites Too bad its like the only song I actually like from this band. That and maybe Tightrope Ikno2love on July 19, Link. Artists - A. Rate These Lyrics. The major components of growth habit are sensitivity to vernalization and photoperiod, and these environmental signals are associated with tolerance to low temperature reviewed by [ 12 ] and [ 13 ].
In general, maximum cold tolerance is achieved in genotypes with winter growth habit during the vegetative growth stage. In contrast, the flowering time of spring habit varieties is not accelerated by vernalization.
Spring growth habit types may vary in their response to photoperiod, but they all have a limited capacity to tolerate low temperature stresses. Varieties with facultative growth habit can be either fall- or spring-planted since they are not vernalization sensitive.
They can be as cold tolerant as winter types [ 14 ]. The photoperiod sensitivity of the facultative growth habit class varies, although sensitivity to short photoperiod is advantageous from the standpoint of delaying the vegetative to reproductive transition [ 15 ] and thus ensuring the maximum capacity for low temperature tolerance [ 16 ]. Deletions spanning putative cis -elements in the intron I are the functional polymorphisms at VRN-H1 accounting for the vernalization-insensitive dominant alleles [ 14 , 21 , 22 ].
The basis of the recessive late-flowering long-day insensitivity phenotype is a SNP mutation affecting a conserved residue in the CCT domain [ 25 ]. Delayed flowering under short-day conditions a recessive phenotype is due to gene deletion [ 24 , 26 , 27 ].
The two-rowed and six-rowed inflorescence types refer to the number of fertile florets per rachis node in the barley spike. The presence of a recessive allele at the VRS1 locus is sufficient to cause the wild type two-rowed barley to become six-rowed barley Lundqvist et al. Multiple loss-of-function mutations in the HvHOX1 gene VRS1 cause a cessation of suppression of lateral-spikelet development and thus lead to the recessive six-rowed phenotype [ 32 ].
Previous attempts to use genome-wide AM to identify loci determining growth habit [ 4 , 10 ] have identified significant associations with SNP markers in the vicinity of some of the determinant genes but not the genes themselves.
Cockram et al. In this report we describe, in essentially chronological order, the results of genotyping, phenotyping, and analyzing the resulting data from barley germplasm sets varying in size and composition. At the same time - in order to fully characterize genes involved in morphology, growth and development - a subset of 12 genes were re-sequenced or genotyped in the CAP Core.
Functional polymorphism assays were based on re-sequencing of target genes in the germplasm array and based on these results, genotyping for specific SNPs and InDels. The CAP Core was phenotyped for inflorescence type and vernalization sensitivity under long-day greenhouse conditions. This provided 2, accessions phenotyped for inflorescence type and accessions phenotyped for vernalization sensitivity.
The SNP and phenotype data from the larger populations were then used for AM and analysis of interactions. Our objective was to empirically assess the effects of population size, population type, and analysis of interactions on detection of genes determining the principal germplasm groups of barley.
In the greenhouse, under unvernalized and long-day photoperiod conditions, 91 of the accessions flowered between days after planting Additional File 1. These genotypes are vernalization-insensitive and are therefore of spring or facultative growth habit. Eleven accessions did not flower within days, at which point the experiment was terminated. These 11 genotypes are vernalization-sensitive and have winter growth habit.
All of the two-rowed accessions but one Charles are vernalization-insensitive. In the six-rowed group, there are 37 vernalization-insensitive and 10 vernalization-sensitive genotypes. Sequences of the non-primer portion of each amplicon were deposited with GenBank and accession numbers are given in Additional File 2. Additional File 3 shows the gene-specific primers used for PCR amplification and fragment sequencing. Neighbor-joining phylogenetic cluster analyses are shown in Additional file 4.
Detailed description of the results from the re-sequencing of the 12 genes can be found in Additional File 5. With specific reference to vernalization sensitivity and row-type, re-sequencing the promoter region, exon 1 and intron 1 of VRN-H1 from the accessions revealed the five previously characterized intron 1 deletion types Additional file 6 [ 14 , 21 , 22 , 35 ].
Comparison of the intron 1-deletion types and the haplotypes showed that some haplotypes have more than one deletion type. Seventeen accessions - six with spring and 11 with winter growth habit - contained all three of the ZCCT-H genes.
Eighteen vernalization-insensitive genotypes contained just the c form of the ZCCT-H gene family but had complete deletions of the a and b forms. Sequence alignment of the proposed functional polymorphism in HvFT1 intron 1 from accessions varying in growth habit revealed that the proposed functional polymorphism [ 23 ] does not account for phenotypic variation in growth habit in the CAP Core germplasm. Six of these haplotypes correspond to previously described alleles [ 32 ].
Four six-rowed accessions have a novel VRS1 haplotype. Because this novel recessive allele cannot be explained by simple mutation of any previously-described dominant alleles, we designate this allele vrs1.
The deduced polypeptide sequence of vrs1. The 14 deficiens accessions in the germplasm array all have the Vrs1. The average extent of LD is aproximately 0. Therefore, for this group the LD threshold was set at an r 2 value of 1 and no estimation of the extension of LD was possible. Scatter plots of linkage disequilibrium r 2 as a function of genetic distance cM within chromosomes.
Significance threshold is represented as an horizontal line. The four sub-populations roughly correspond to winter six-rowed, spring six-rowed, and two groups of spring two-rowed genotypes. One group of spring two-rowed genotypes is comprised of Baronesse, eight Baronesse-derived genetic stocks BISON , and four other varieties with Baronesse in their parentage.
The first two components in the Principal Components Analysis PCA confirmed this division by row type and growth habit, but no subgroups within the spring two-rowed genotypes were detected Figure 2.
There is a degree of admixture, with some accessions appearing in sub-populations that do not correspond to their growth habit or row type. For example, Charles winter two-rowed is clustered with the spring two-rowed; OWB-Dominant spring two-rowed is clustered with winter six-rowed; 88Ab and 88AbB winter six-rowed with Morex parentage are clustered with spring six-rowed; and Washford, Belford, Steptoe and OWB-Recessive spring six-rowed are clustered with winter six-rowed. First two axes are represented.
Most of the spring 6-rowed lines are clustered in the first quadrant. Most of the spring two-rowed lines are clustered in the fourth quadrant and most of the winter 6-rowed lines are clustered in the third quadrant. In both cases, the degree of admixture is higher among lines with the same growth habit than it is among lines with the same row type.
Growth habit and inflorescence traits are the main determinants of population structure in the CAP Core and including population structure in the model used for AM will diminish the ability to detect the genetic determinants of these traits. Circles represent -log p values of the individual markers in consensus map position. Due to the coding of the deletion alleles as missing data, these loci fell below the quality threshold for selecting suitable markers for AM.
In order to have markers in high LD with the described functional polymorphism s in the VRN-H and VRS1 loci, we developed genotype assays based on our re-sequencing data and conducted a second round of AM. For each trait we selected all markers with p -values below a threshold of 0. Based on this criterion, markers were selected for inflorescence type and 59 for vernalization sensitivity.
For all possible two-way combinations of markers for each of the two traits, we performed likelihood ratio tests LRTs. For vernalization sensitivity, the interactions between five markers, out of the 1, possible two-way combinations, showed a remarkable increase in the -log p score compared with the others Table 2. Both have identical distributions of alleles within the CAP Core. Ten two-way interactions, out of the 19, possible, predicted perfectly the row type in the CAP Core.
To determine if these loci or linked loci are determinants of the two-rowed vs. The parents of this population are two-rowed OWB-dominant and six-rowed OWB-recessive and the allele types at the four markers in these two accessions fits the same pattern as observed for the CAP Core and a larger population of CAP lines see next section.
However, in the OWB doubled haploid mapping population, the only locus with a perfect association with inflorescence type is VRS1. Six additional interactions also predicted perfectly the row type Table 3. Detailed information about the SNP markers detected in the interaction analysis can be found in Additional File 8.
All these lines and accessions had been genotyped with BOPA 1 and 2. For inflorescence type, there were significant associations on chromosomes 2H and 1H Figure 3B , and these associations correspond to the same regions identified in the CAP Core using the allele type marker of VRS1 and interaction analysis. There was no pattern for allele type in the six-rowed germplasm. These associations were found in the same genome regions as in the CAP Core, except for those found in 2H. Molecular analyses of 12 genes from seven loci known to be involved in the genetic determination of growth habit and inflorescence type - the two major traits causing strong population structuring - from a unique set of barley accessions revealed high sequence diversity and complex haplotypes.
Identification of these haplotypes in marker-assisted breeding programs will require the use of multiple SNPs per gene, or alternative assays. Even more genetic diversity was found when we considered multi-locus haplotypes of loci involved in the regulation of growth habit. Based on the proposed functional polymorphisms, we determined multi-locus haplotypes of the three VRN-H and two PPD-H loci and found 16 of the possible allele combinations Additional File 1.
Thirty-two out of the 85 spring growth habit cultivars had "spring" alleles at all five loci, while 41 spring growth habit genotypes had recessive winter vrn-h3 HvFT1 and "spring" alleles at the other four loci.
The abundance of the winter vrn-h3 allele in cultivated spring growth habit germplasm was unexpected since allelic variants at the VRN-H3 locus were previously reported only in exotic barley genotypes [ 17 ].
Seven out of 11 winter growth habit genotypes had "winter" alleles at the five loci. In total, vernalization-insensitive spring and facultative growth habit genotypes had 13 multi-locus haplotypes and vernalization-sensitive winter growth habit genotypes had three. Our results show that a large number of single-locus and multi-locus haplotypes are involved in determining flowering time and thus growth habit.
The CAP Core is a limited sample of heterogeneous germplasm. The array is comprised of accessions representing a range of growth habit, row type, usage and origin. However, this set is representative of the array of lines usually used in barley breeding programs of North America. We used row type and growth habit as measured by flowering time of non vernalized plants under long photoperiod as models for genome-wide association analysis for several reasons. These phenotypes exemplify two different genetic scenarios.
The genes determining vernalization sensitivity interact epistatically and the functional basis is known. The two phenotypes can be scored unequivocally. Finally, growth habit and row type are the two traits considered world-wide to define germplasm structure in barley.
Even after accounting for structure in the CAP Core, we were able to identify markers associated with the two traits because there was some degree of admixture. The limited admixture between the three subgroups representing combinations of growth habit and row type spring two-rowed, spring six-rowed, and winter six-rowed is likely due to the tendency of geographically dispersed breeding programs to limit germplasm exchange.
Accessions from the same structure group will have a more similar history of selection for genomic regions that control row type and growth habit than accessions from other groups. Within each structure group, accessions from any given breeding program will also tend to be more similar. However, the extent of LD within each group was reduced by the fact that accessions within each group came from different programs.
The reduced estimated extension of LD in the winter six-rowed group may also be due to the small sample size 33 individuals. Barley, a self-pollinated species, is reported to have a sufficiently high level of LD that, with sufficient marker coverage, association mapping should be effective [ 2 , 11 , 40 ].
Since the average marker density is 0.
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