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Dhurrin metabolism in the developing grain of Sorghum bicolor (L.) Moench investigated by metabolite profiling and novel clustering analyses of time-resolved transcriptomic data.

ABSTRACT: BACKGROUND:The important cereal crop Sorghum bicolor (L.) Moench biosynthesize and accumulate the defensive compound dhurrin during development. Previous work has suggested multiple roles for the compound including a function as nitrogen storage/buffer. Crucial for this function is the endogenous turnover of dhurrin for which putative pathways have been suggested but not confirmed. RESULTS:In this study, the biosynthesis and endogenous turnover of dhurrin in the developing sorghum grain was studied by metabolite profiling and time-resolved transcriptome analyses. Dhurrin was found to accumulate in the early phase of grain development reaching maximum amounts 25 days after pollination. During the subsequent maturation period, the dhurrin content was turned over, resulting in only negligible residual dhurrin amounts in the mature grain. Dhurrin accumulation correlated with the transcript abundance of the three genes involved in biosynthesis. Despite the accumulation of dhurrin, the grains were acyanogenic as demonstrated by the lack of hydrogen cyanide release from macerated grain tissue and by the absence of transcripts encoding dhurrinases. With the missing activity of dhurrinases, the decrease in dhurrin content in the course of grain maturation represents the operation of hitherto uncharacterized endogenous dhurrin turnover pathways. Evidence for the operation of two such pathways was obtained by metabolite profiling and time-resolved transcriptome analysis. By combining cluster- and phylogenetic analyses with the metabolite profiling, potential gene candidates of glutathione S-transferases, nitrilases and glycosyl transferases involved in these pathways were identified. The absence of dhurrin in the mature grain was replaced by a high content of proanthocyanidins. Cluster- and phylogenetic analyses coupled with metabolite profiling, identified gene candidates involved in proanthocyanidin biosynthesis in sorghum. CONCLUSIONS:The results presented in this article reveal the existence of two endogenous dhurrin turnover pathways in sorghum, identify genes putatively involved in these transformations and show that dhurrin in addition to its insect deterrent properties may serve as a storage form of reduced nitrogen. In the course of sorghum grain maturation, proanthocyanidins replace dhurrin as a defense compound. The lack of cyanogenesis in the developing sorghum grain renders this a unique experimental system to study CNglc synthesis as well as endogenous turnover.

SUBMITTER: Nielsen LJ

PROVIDER: S-EPMC5154151 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Dhurrin metabolism in the developing grain of Sorghum bicolor (L.) Moench investigated by metabolite profiling and novel clustering analyses of time-resolved transcriptomic data.

Nielsen Lasse Janniche LJ Stuart Peter P Pičmanová Martina M Rasmussen Simon S Olsen Carl Erik CE Harholt Jesper J Møller Birger Lindberg BL Bjarnholt Nanna N

BMC genomics 20161213 1

<h4>Background</h4>The important cereal crop Sorghum bicolor (L.) Moench biosynthesize and accumulate the defensive compound dhurrin during development. Previous work has suggested multiple roles for the compound including a function as nitrogen storage/buffer. Crucial for this function is the endogenous turnover of dhurrin for which putative pathways have been suggested but not confirmed.<h4>Results</h4>In this study, the biosynthesis and endogenous turnover of dhurrin in the developing sorghum ...[more]

PMID: 27964718

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Project description:Main conclusionDevelopmental and organ-specific expression of genes in dhurrin biosynthesis, bio-activation, and recycling offers dynamic metabolic responses optimizing growth and defence responses in Sorghum. Plant defence models evaluate the costs and benefits of resource investments at different stages in the life cycle. Poor understanding of the molecular regulation of defence deployment and remobilization hampers accuracy of the predictions. Cyanogenic glucosides, such as dhurrin are phytoanticipins that release hydrogen cyanide upon bio-activation. In this study, RNA-seq was used to investigate the expression of genes involved in the biosynthesis, bio-activation and recycling of dhurrin in Sorghum bicolor. Genes involved in dhurrin biosynthesis were highly expressed in all young developing vegetative tissues (leaves, leaf sheath, roots, stems), tiller buds and imbibing seeds and showed gene specific peaks of expression in leaves during diel cycles. Genes involved in dhurrin bio-activation were expressed early in organ development with organ-specific expression patterns. Genes involved in recycling were expressed at similar levels in the different organ during development, although post-floral initiation when nutrients are remobilized for grain filling, expression of GSTL1 decreased > tenfold in leaves and NITB2 increased > tenfold in stems. Results are consistent with the establishment of a pre-emptive defence in young tissues and regulated recycling related to organ senescence and increased demand for nitrogen during grain filling. This detailed characterization of the transcriptional regulation of dhurrin biosynthesis, bioactivation and remobilization genes during organ and plant development will aid elucidation of gene regulatory networks and signalling pathways that modulate gene expression and dhurrin levels. In-depth knowledge of dhurrin metabolism could improve the yield, nitrogen use efficiency and stress resilience of Sorghum.

Project description:Sorghum production is affected by a wide array of biotic constraints, of which sorghum shoot fly, Atherigona soccata is the most important pest, which severely damages the sorghum crop during the seedling stage. Host plant resistance is one of the major components to control sorghum shoot fly, A. soccata. To understand the nature of gene action for inheritance of shoot fly resistance, we evaluated 10 parents, 45 F1's and their reciprocals in replicated trials during the rainy and postrainy seasons. The genotypes ICSV 700, Phule Anuradha, ICSV 25019, PS 35805, IS 2123, IS 2146, and IS 18551 exhibited resistance to shoot fly damage across seasons. Crosses between susceptible parents were preferred for egg laying by the shoot fly females, resulting in a susceptible reaction. ICSV 700, ICSV 25019, PS 35805, IS 2123, IS 2146, and IS 18551 exhibited significant and negative general combining ability (gca) effects for oviposition, deadheart incidence, and overall resistance score. The plant morphological traits associated with expression of resistance/susceptibility to shoot fly damage such as leaf glossiness, plant vigor, and leafsheath pigmentation also showed significant gca effects by these genotypes, suggesting the potential for use as a selection criterion to breed for resistance to shoot fly, A. soccata. ICSV 700, Phule Anuradha, IS 2146 and IS 18551 with significant positive gca effects for trichome density can also be utilized in improving sorghums for shoot fly resistance. The parents involved in hybrids with negative specific combining ability (sca) effects for shoot fly resistance traits can be used in developing sorghum hybrids with adaptation to postrainy season. The significant reciprocal effects of combining abilities for oviposition, leaf glossy score and trichome density suggested the influence of cytoplasmic factors in inheritance of shoot fly resistance. Higher values of variance due to specific combining ability (σ(2)s), dominance variance (σ(2)d), and lower predictability ratios than the variance due to general combining ability (σ(2)g) and additive variance (σ(2)a) for shoot fly resistance traits indicated the predominance of dominance type of gene action, whereas trichome density, leaf glossy score, and plant vigor score with high σ(2)g, additive variance, predictability ratio, and the ratio of general combining ability to the specific combining ability showed predominance of additive type of gene action indicating importance of heterosis breeding followed by simple selection in breeding shoot fly-resistant sorghums. Most of the traits exhibited high broadsense heritability, indicating high inheritance of shoot fly resistance traits.

Project description:Genotype by environment (G×E) interaction is a major factor limiting the success of germplasm selection and identification of superior genotypes for use in plant breeding programs. Similar to the case in other crops, G×E complicates the improvement of sorghum, and hence it should be determined and used in decision-making programs. The present study aimed at assessing the G×E interaction, and the correlation between traits for superior sorghum genotypes. Three hundred twenty sorghum landraces and four improved varieties were used in alpha lattice experimental design-based field trial across three environments (Melkassa, Mieso and Mehoni) in Ethiopia. Phenotypic data were collected for days to flowering (DTF), plant height (PH), panicle length (PALH), panicle width (PAWD), panicle weight (PAWT) and grain yield (GY). The results revealed that the variance due to genotype, environment and G×E interaction were highly significant (P < 0.001) for all traits. GY and PAWT were highly affected by environments and G×E whereas DTF, PALH, PAWD and PH were mainly affected by genotypic variation. Therefore, multi-environment testing is needed for taking care of G × E interaction to identify high yielding and stable sorghum landraces. GY and PAWT revealed highly significant positive correlations indicating the possibility of effective selection of the two traits simultaneously. Among the studied populations, South Wello, West Hararghe and Shewa zones had highly diverse genotypes that were distributed across all clusters. Hence, these areas can be considered as hotspots for identifying divergent sorghum landraces that could be used in breeding programs. Melkassa was the most representative environment whereas Mieso was the most discriminating. Five genotypes (G148, G123, G110, G203 and G73) were identified as superior across the test environments for grain yield with farmer-preferred trait, such as plant height. The identified stable and high yielding genotypes are valuable genetic resources that should be used in sorghum breeding programs.

Dataset Information

Dhurrin metabolism in the developing grain of Sorghum bicolor (L.) Moench investigated by metabolite profiling and novel clustering analyses of time-resolved transcriptomic data.

Publications

Dhurrin metabolism in the developing grain of Sorghum bicolor (L.) Moench investigated by metabolite profiling and novel clustering analyses of time-resolved transcriptomic data.

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