Trehalose 6-Phosphate Regulates Photosynthesis and Assimilate Partitioning in Reproductive Tissue

Oszvald, Mária; Primavesi, Lucia F.; Griffiths, Cara A.; Cohn, Jonathan; Basu, Subhash; Nuccio, Michael L.; Paul, M. J.

doi:10.1104/pp.17.01673

Cited by 120 publications

(108 citation statements)

References 40 publications

(12 reference statements)

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“…Furthermore, one of the current models for T6P in regulating plant growth and yield is primarily based on T6P functioning as a nutrient‐sensing factor, which directs sugar from source to sink tissues for plant growth. Overexpressing TPP and decreasing T6P level maintained photosynthesis rate in leaves, increased sugars and amino acids in florets and substantially improved yield in maize (Nuccio et al ., ; Oszvald et al ., ). Although TPP is an important regulator for T6P, here we present evidence that the T6P level also could be controlled by NAC7 through TPS.…”

Section: Discussionmentioning

confidence: 97%

Identification and characterization of a novel stay‐green QTL that increases yield in maize

Zhang

Fengler

Hemert

et al. 2019

Plant Biotechnology Journal

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SummaryFunctional stay‐green is a valuable trait that extends the photosynthetic period, increases source capacity and biomass and ultimately translates to higher grain yield. Selection for higher yields has increased stay‐green in modern maize hybrids. Here, we report a novel QTL controlling functional stay‐green that was discovered in a mapping population derived from the Illinois High Protein 1 (IHP1) and Illinois Low Protein 1 (ILP1) lines, which show very different rates of leaf senescence. This QTL was mapped to a single gene containing a NAC‐domain transcription factor that we named nac7. Transgenic maize lines where nac7 was down‐regulated by RNAi showed delayed senescence and increased both biomass and nitrogen accumulation in vegetative tissues, demonstrating NAC7 functions as a negative regulator of the stay‐green trait. More importantly, crosses between nac7 RNAi parents and two different elite inbred testers produced hybrids with prolonged stay‐green and increased grain yield by an average 0.29 megagram/hectare (4.6 bushel/acre), in 2 years of multi‐environment field trials. Subsequent RNAseq experiments, one employing nac7 RNAi leaves and the other using leaf protoplasts overexpressing Nac7, revealed an important role for NAC7 in regulating genes in photosynthesis, chlorophyll degradation and protein turnover pathways that each contribute to the functional stay‐green phenotype. We further determined the putative target of NAC7 and provided a logical extension for the role of NAC7 in regulating resource allocation from vegetative source to reproductive sink tissues. Collectively, our findings make a compelling case for NAC7 as a target for improving functional stay‐green and yields in maize and other crops.

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Section: Discussionmentioning

confidence: 97%

Identification and characterization of a novel stay‐green QTL that increases yield in maize

Zhang

Fengler

Hemert

et al. 2019

Plant Biotechnology Journal

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“…Differences in T6P dynamics could determine in part sink strength and sugar accumulation in sweet sorghum stems. Furthermore, our observation in R9188, based on overlapping patterns with Arabidopsis and maize gene sets (Figures , S13), implies that the T6P signal in R9188 was turned over possibly by either BTx406‐introgressed candidates, such as the TPP and bZIP genes, or differentially expressed TPS , TPP and C‐group bZIP s. Still, this analysis might possibly underestimate the numbers of genes regulated by the T6P/SnRK1‐pathways due to (i) limited numbers of gene IDs convertible to Arabidopsis gene IDs, (ii) evolutionary convergence and divergence in sugar signalling between the three species, (iii) tissue‐dependent effects of T6P and the different tissues/systems used in the present study (Oszvald et al ., ; Wingler et al ., ; Zhang et al ., ), (iv) technical difficulties in separating primary effects from secondary, long‐term or adaptive effects.…”

Section: Discussionmentioning

confidence: 98%

“…Such relationships were not observed with Arabidopsis sucrose-and glucose-responsive gene sets, demonstrating that the R9188 transcriptome was partially reprogrammed by the T6P/SnRK1-mediated signalling pathway. We also compared sorghum co-expression modules with maize gene sets generated from floret and pith of developing cob, which were generated with ectopic expression of rice TREHALOSE PHOSPHATE PHOSPHATASE1 (TPP1; Oszvald et al, 2018). Significant overlaps were observed with the maize pith but not with floret gene sets ( Figure 4b).…”

Section: T6p/snrk1 Regulated Genesmentioning

confidence: 99%

Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

Wang

Feng

et al. 2018

Plant Biotechnology Journal

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Sweet sorghum accumulates large amounts of soluble sugar in its stem. However, a system-based understanding of this carbohydrate allocation process is lacking. Here, we compared the dynamic transcriptome and metabolome between the conversion line R9188 and its two parents, sweet sorghum RIO and grain sorghum BTx406 that have contrasting sugar-accumulating phenotypes. We identified two features of sucrose metabolism, stable concentrations of sugar phosphates in RIO and opposite trend of trehalose-6-phosphate (T6P) between RIO vs R9188/BTx406. Integration of transcriptome and metabolome revealed R9188 is partially active in starch metabolism together with medium sucrose level, whereas sweet sorghum had the highest sucrose concentration and remained highly active in sucrose, starch, and cell wall metabolism post-anthesis. Similar expression pattern of genes involved in sucrose degradation decreased the pool of sugar phosphates for precursors of starch and cell wall synthesis in R9188 and BTx406. Differential T6P signal between RIO vs R9188/BTx406 is associated with introgression of T6P regulators from BTx406 into R9188, including C-group bZIP and trehalose 6-phosphate phosphatase (TPP). The inverted T6P signalling in R9188 appears to down-regulate sucrose and starch metabolism partly through transcriptome reprogramming, whereas introgressed metabolic genes could be related to reduced cell wall metabolism. Our results show that coordinated primary metabolic pathways lead to high sucrose demand and accumulation in sweet sorghum, providing us with targets for genetic improvements of carbohydrate allocation in bioenergy crops.

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“…Activation is shown by blue dashed lines with triangular arrowheads, and inhibition by red dashed lines with solid bars. Elevated T6P levels decrease sink strength and growth in sink tissues via inhibition of SnRK1 and via direct inhibition of SUS‐mediated sucrolysis. SnRK1 is responsible for SUS transcriptional activation , and may also regulate expression of sucrose transporters (SUTs and SWEETS) and cell wall invertase .…”

Section: Resultsmentioning

confidence: 99%

“…Stress-resistant plant traits have recently been developed that have been linked to T6P and sucrose metabolism. For example, T6P phosphatase (TPP) overexpression, which reduces T6P levels, may improve the survival of submerged rice seedlings, reduce kernel abortion in drought-stressed maize, and increase maize yield under both droughtstressed and well-watered conditions [6][7][8]. The molecular mechanisms that maintain the link between sucrose and T6P are not fully understood, and their elucidation promises to accelerate the further development of crops with enhanced traits.In sink tissues, such as developing fruits, seeds, and tubers, imported sucrose can either be hydrolyzed to glucose and fructose by invertase or cleaved by sucrose synthase (SUS) to produce UDP-glucose (UDPG) and fructose in a UDP-dependent manner.…”

mentioning

confidence: 99%

The signal metabolite trehalose‐6‐phosphate inhibits the sucrolytic activity of sucrose synthase from developing castor beans

et al. 2018

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In plants, trehalose 6-phosphate (T6P) is a key signaling metabolite that functions as both a signal and negative feedback regulator of sucrose levels. The mode of action by which T6P senses and regulates sucrose is not fully understood. Here, we demonstrate that the sucrolytic activity of RcSUS1, the dominant sucrose synthase isozyme expressed in developing castor beans, is allosterically inhibited by T6P. The feedback inhibition of SUS by T6P may contribute to the control of sink strength and sucrolytic flux in heterotrophic plant tissues.

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Trehalose 6-Phosphate Regulates Photosynthesis and Assimilate Partitioning in Reproductive Tissue

Cited by 120 publications

References 40 publications

Identification and characterization of a novel stay‐green QTL that increases yield in maize

Identification and characterization of a novel stay‐green QTL that increases yield in maize

Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes

The signal metabolite trehalose‐6‐phosphate inhibits the sucrolytic activity of sucrose synthase from developing castor beans

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