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Common metabolic networks contribute to carbon sink strength of sorghum internodes: implications for bioenergy improvement.

ABSTRACT: Background:Sorghum bicolor (L.) is an important bioenergy source. The stems of sweet sorghum function as carbon sinks and accumulate large amounts of sugars and lignocellulosic biomass and considerable amounts of starch, therefore providing a model of carbon allocation and accumulation for other bioenergy crops. While omics data sets for sugar accumulation have been reported in different genotypes, the common features of primary metabolism in sweet genotypes remain unclear. To obtain a cohesive and comparative picture of carbohydrate metabolism between sorghum genotypes, we compared the phenotypes and transcriptome dynamics of sugar-accumulating internodes among three different sweet genotypes (Della, Rio, and SIL-05) and two non-sweet genotypes (BTx406 and R9188). Results:Field experiments showed that Della and Rio had similar dynamics and internode patterns of sugar concentration, albeit distinct other phenotypes. Interestingly, cellulose synthases for primary cell wall and key genes in starch synthesis and degradation were coordinately upregulated in sweet genotypes. Sweet sorghums maintained active monolignol biosynthesis compared to the non-sweet genotypes. Comparative RNA-seq results support the role of candidate Tonoplast Sugar Transporter gene (TST), but not the Sugars Will Eventually be Exported Transporter genes (SWEETs) in the different sugar accumulations between sweet and non-sweet genotypes. Conclusions:Comparisons of the expression dynamics of carbon metabolic genes across the RNA-seq data sets identify several candidate genes with contrasting expression patterns between sweet and non-sweet sorghum lines, including genes required for cellulose and monolignol synthesis (CesA, PTAL, and CCR), starch metabolism (AGPase, SS, SBE, and G6P-translocator SbGPT2), and sucrose metabolism and transport (TPP and TST2). The common transcriptome features of primary metabolism identified here suggest the metabolic networks contributing to carbon sink strength in sorghum internodes, prioritize the candidate genes for manipulating carbon allocation with bioenergy purposes, and provide a comparative and cohesive picture of the complexity of carbon sink strength in sorghum stem.

SUBMITTER: Li Y

PROVIDER: S-EPMC6868837 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundBioenergy sorghum accumulates 75% of shoot biomass in stem internodes. Grass stem internodes are formed during vegetative growth and elongate in response to developmental and environmental signals. To identify genes and molecular mechanisms that modulate the extent of internode growth, we conducted microscopic and transcriptomic analyses of four successive sub-apical vegetative internodes representing different stages of internode development of the bioenergy sorghum genotype R.07020.ResultsStem internodes of sorghum genotype R.07020 are formed during the vegetative phase and their length is enhanced by environmental signals such as shade and floral induction in short days. During vegetative growth, the first visible and youngest sub-apical internode was ~0.7 cm in length, whereas the fourth fully expanded internode was ~5 cm in length. Microscopic analyses revealed that all internode tissue types including pith parenchyma and vascular bundles are present in the four successive internodes. Growth in the first two sub-apical internodes occurred primarily through an increase in cell number consistent with expression of genes involved in the cell cycle and DNA replication. Growth of the 3rd internode was associated with an increase in cell length and growth cessation in the 4th internode was associated with up-regulation of genes involved in secondary cell wall deposition. The expression of genes involved in hormone metabolism and signaling indicates that GA, BR, and CK activity decreased while ethylene, ABA, and JA increased in the 3rd/4th internodes. While the level of auxin appears to be increasing as indicated by the up-regulation of ARFs, down-regulation of TIR during development indicates that auxin signaling is also modified. The expression patterns of transcription factors are closely associated with their role during the development of the vegetative internodes.ConclusionsMicroscopic and transcriptome analyses of four successive sub-apical internodes characterized the developmental progression of vegetative stem internodes from initiation through full elongation in the sorghum genotype R.07020. Transcriptome profiling indicates that dynamic variation in the levels and action of GA, CK, IAA, BR, ethylene, ABA, and JA modulate gene expression and growth during internode growth and development. This study provides detailed microscopic and transcriptomic data useful for identifying genes and molecular pathways regulating internode elongation in response to various developmental and environmental signals.

Project description:With high productivity and stress tolerance, numerous grass genera of the Andropogoneae have emerged as candidates for bioenergy production. To optimize these candidates, research examining the genetic architecture of yield, carbon partitioning, and composition is required to advance breeding objectives. Significant progress has been made developing genetic and genomic resources for Andropogoneae, and advances in comparative and computational genomics have enabled research examining the genetic basis of photosynthesis, carbon partitioning, composition, and sink strength. To provide a pivotal resource aimed at developing a comparative understanding of key bioenergy traits in the Andropogoneae, we have established and characterized an association panel of 390 racially, geographically, and phenotypically diverse Sorghum bicolor accessions with 232,303 genetic markers. Sorghum bicolor was selected because of its genomic simplicity, phenotypic diversity, significant genomic tools, and its agricultural productivity and resilience. We have demonstrated the value of sorghum as a functional model for candidate gene discovery for bioenergy Andropogoneae by performing genome-wide association analysis for two contrasting phenotypes representing key components of structural and non-structural carbohydrates. We identified potential genes, including a cellulase enzyme and a vacuolar transporter, associated with increased non-structural carbohydrates that could lead to bioenergy sorghum improvement. Although our analysis identified genes with potentially clear functions, other candidates did not have assigned functions, suggesting novel molecular mechanisms for carbon partitioning traits. These results, combined with our characterization of phenotypic and genetic diversity and the public accessibility of each accession and genomic data, demonstrate the value of this resource and provide a foundation for future improvement of sorghum and related grasses for bioenergy production.

Project description:BACKGROUND:Sugarcane is a major crop producing about 80% of sugar globally. Increasing sugar content is a top priority for sugarcane breeding programs worldwide, however, the progress is extremely slow. Owing to its commercial significance, the physiology of sucrose accumulation has been studied extensively but it did not lead to any significant practical outcomes. Recent molecular studies are beginning to recognize genes and gene networks associated with this phenomenon. To further advance our molecular understanding of sucrose accumulation, we altered sucrose content of sugarcane genotypes with inherently large variation for sucrose accumulation using a sugarcane ripener, ethylene, and studied their transcriptomes to identify genes associated with the phenomenon. RESULTS:Sucrose content variation in the experimental genotypes was substantial, with the top-performing clone producing almost 60% more sucrose than the poorest performer. Ethylene treatment increased stem sucrose content but that occurred only in low-sugar genotype. Transcriptomic analyses have identified about 160,000 unigenes of which 86,000 annotated genes were classified into functional groups associated with carbohydrate metabolism, signaling, localization, transport, hydrolysis, growth, catalytic activity, membrane and storage, suggesting the structural and functional specification, including sucrose accumulation, occurring in maturing internodes. About 25,000 genes were differentially expressed between all genotypes and treatments combined. Genotype had a dominant effect on differential gene expression than ethylene treatment. Sucrose and starch metabolism genes were more responsive to ethylene treatment in low-sugar genotype. Ethylene caused differential gene expression of many stress-related transcription factors, carbohydrate metabolism, hormone metabolism and epigenetic modification. Ethylene-induced expression of ethylene-responsive transcription factors, cytosolic acid- and cell wall-bound invertases, and ATPase was more pronounced in low- than in high-sugar genotype, suggesting an ethylene-stimulated sink activity and consequent increased sucrose accumulation in low-sugar genotype. CONCLUSION:Ethylene-induced sucrose accumulation is more pronounced in low-sugar sugarcane genotype, and this is possibly achieved by the preferential activation of genes such as invertases that increase sink strength in the stem. The relatively high enrichment of differentially expressed genes associated with hormone metabolism and signaling and stress suggests a strong hormonal regulation of source-sink activity, growth and sucrose accumulation in sugarcane.

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Common metabolic networks contribute to carbon sink strength of sorghum internodes: implications for bioenergy improvement.

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