Dataset Information

Waxy phenotype evolution in the allotetraploid cereal broomcorn millet: mutations at the GBSSI locus in their functional and phylogenetic context.

ABSTRACT: Waxy mutants, in which endosperm starch contains ~100% amylopectin rather than the wild-type composition of ~70% amylopectin and ~30% amylose, occur in many domesticated cereals. The cultivation of waxy varieties is concentrated in east Asia, where there is a culinary preference for glutinous-textured foods that may have developed from ancient food processing traditions. The waxy phenotype results from mutations in the GBSSI gene, which catalyzes amylose synthesis. Broomcorn or proso millet (Panicum miliaceum L.) is one of the world's oldest cultivated cereals, which spread across Eurasia early in prehistory. Recent phylogeographic analysis has shown strong genetic structuring that likely reflects ancient expansion patterns. Broomcorn millet is highly unusual in being an allotetraploid cereal with fully waxy varieties. Previous work characterized two homeologous GBSSI loci, with multiple alleles at each, but could not determine whether both loci contributed to GBSSI function. We first tested the relative contribution of the two GBSSI loci to amylose synthesis and second tested the association between GBSSI alleles and phylogeographic structure inferred from simple sequence repeats (SSRs). We evaluated the phenotype of all known GBSSI genotypes in broomcorn millet by assaying starch composition and protein function. The results showed that the GBSSI-S locus is the major locus controlling endosperm amylose content, and the GBSSI-L locus has strongly reduced synthesis capacity. We genotyped 178 individuals from landraces from across Eurasia for the 2 GBSSI and 16 SSR loci and analyzed phylogeographic structuring and the geographic and phylogenetic distribution of GBSSI alleles. We found that GBSSI alleles have distinct spatial distributions and strong associations with particular genetic clusters defined by SSRs. The combination of alleles that results in a partially waxy phenotype does not exist in landrace populations. Our data suggest that broomcorn millet is a system in the process of becoming diploidized for the GBSSI locus responsible for grain amylose. Mutant alleles show some exchange between genetic groups, which was favored by selection for the waxy phenotype in particular regions. Partially waxy phenotypes were probably selected against-this unexpected finding shows that better understanding is needed of the human biology of this phenomenon that distinguishes cereal use in eastern and western cultures.

SUBMITTER: Hunt HV

PROVIDER: S-EPMC3533377 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Waxy phenotype evolution in the allotetraploid cereal broomcorn millet: mutations at the GBSSI locus in their functional and phylogenetic context.

Hunt Harriet V HV Moots Hannah M HM Graybosch Robert A RA Jones Huw H Parker Mary M Romanova Olga O Jones Martin K MK Howe Christopher J CJ Trafford Kay K

Molecular biology and evolution 20120830 1

Waxy mutants, in which endosperm starch contains ~100% amylopectin rather than the wild-type composition of ~70% amylopectin and ~30% amylose, occur in many domesticated cereals. The cultivation of waxy varieties is concentrated in east Asia, where there is a culinary preference for glutinous-textured foods that may have developed from ancient food processing traditions. The waxy phenotype results from mutations in the GBSSI gene, which catalyzes amylose synthesis. Broomcorn or proso millet (Pan ...[more]

PMID: 22936718

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Project description:Waxy varieties of the tetraploid cereal broomcorn millet (Panicum miliaceum L.) have endosperm starch granules lacking detectable amylose. This study investigated the basis of this phenotype using molecular and biochemical methods. Iodine staining of starch granules in 72 plants from 38 landrace accessions found 58 nonwaxy and 14 waxy phenotype plants. All waxy types were in plants from Chinese and Korean accessions, a distribution similar to that of the waxy phenotype in other cereals. Granule-bound starch synthase I (GBSSI) protein was present in the endosperm of both nonwaxy and waxy individuals, but waxy types had little or no granule-bound starch synthase activity compared with the wild types. Sequencing of the GBSSI (Waxy) gene showed that this gene is present in two different forms (L and S) in P. miliaceum, which probably represent homeologues derived from two distinct diploid ancestors. Protein products of both these forms are present in starch granules. We identified three polymorphisms in the exon sequence coding for mature GBSSI peptides. A 15-bp deletion has occurred in the S type GBSSI, resulting in the loss of five amino acids from glucosyl transferase domain 1 (GTD1). The second GBSSI type (L) shows two sequence polymorphisms. One is the insertion of an adenine residue that causes a reading frameshift, and the second causes a cysteine-tyrosine amino acid polymorphism. These mutations appear to have occurred in parallel from the ancestral allele, resulting in three GBSSI-L alleles in total. Five of the six possible genotype combinations of the S and L alleles were observed. The deletion in the GBSSI-S gene causes loss of protein activity, and there was 100% correspondence between this deletion and the waxy phenotype. The frameshift mutation in the L gene results in the loss of L-type protein from starch granules. The L isoform with the tyrosine residue is present in starch granules but is nonfunctional. This loss of function may result from the substitution of tyrosine for cysteine, although it could not be determined whether the cysteine isoform of L represents the functional type. This is the first characterization of mutations that occur in combination in a functionally polyploid species to give a fully waxy phenotype.

Project description:Broomcorn millet (BM), one of the earliest domesticated cereal crops originating in northern China, can tolerate extreme conditions, such as drought and high temperatures, which are prevalent in saline-alkali, arid, and barren landscapes. However, its adaptive mechanism to alkali stress is yet to be comprehensively understood. In this study, 80 and 40 mM standard alkali stress concentrations were used to, respectively, evaluate the alkali tolerance at the germination and seedling stages of 296 BM genotypes. Principal component analysis (PCA), Pearson's correlation analysis, and F-value comprehensive analysis were performed on the germination parameters (germination potential, germination index, germination rate, vigor index, root length/weight, sprout length/weight, and alkali damage rate). Based on their respective F-values, the BM genotypes were divided into five categories ranging from highly alkali resistant to alkali sensitive. To study the response of seedlings to alkaline stress, we investigated the phenotypic parameters (plant height, green leaf area, biomass, and root structure) of 111 genotypes from the above five categories. Combining the parameters of alkali tolerance at the germination and seedling stages, these 111 genotypes were further subdivided into three groups with different alkali tolerances. Variations in physiological responses of the different alkali-tolerant genotypes were further investigated for antioxidant enzyme activity, soluble substances, malondialdehyde (MDA) content, electrolyte leakage rate, and leaf structure. Compared with alkali-sensitive genotypes, alkali-tolerant genotypes had high antioxidant enzyme activity and soluble osmolyte content, low MDA content and electrolyte leakage rate, and a more complete stomata structure. Taken together, this study provides a comprehensive and reliable method for evaluating alkali tolerance and will contribute to the improvement and restoration of saline-alkaline soils by BM.

Dataset Information

Waxy phenotype evolution in the allotetraploid cereal broomcorn millet: mutations at the GBSSI locus in their functional and phylogenetic context.

Publications

Waxy phenotype evolution in the allotetraploid cereal broomcorn millet: mutations at the GBSSI locus in their functional and phylogenetic context.

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