The Regulation of Metabolic Flux to Cellulose, a Major Sink for Carbon in Plants

doi:10.1006/mben.2001.0206

Metabolic Engineering

Volume 4, Issue 1, January 2002, Pages 22-28

https://doi.org/10.1006/mben.2001.0206 Get rights and content

Abstract

Cellulose is an important component of the cell walls of higher plants and the world's most abundant organic compound. As a major sink for carbon on earth, it is of interest to examine possible means by which the quality or quantity of cellulose deposited in various plant parts might be manipulated by metabolic engineering techniques. This review outlines basic knowledge about the genes and proteins that are involved in cellulose biosynthesis and presents a model that summarizes our current thinking on the overall cellulose biosynthesis pathway. Strategies that might be used for altering the flux of carbon into this pathway are discussed.

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Cotton fiber is an important natural textile raw material, and its quality directly affects spinning performance. Phosphorus (P) deficiency reduces fiber quality, particularly fiber strength. Fiber strength formation relies on sucrose supplied by the leaf subtending to cotton boll (LSCB), and low P may affect it by regulating sucrose supply and utilization in LSCB and fiber.
Our study aimed to investigate how P regulates the formation of fiber bundle strength through essential carbohydrate metabolic pathways.
A three-year experiment on Lu 54 (low-P sensitive) and Yuzaomian 9110 (low-P tolerant) was carried out to study the influence of P on sucrose synthesis and export in LSCB, sucrose absorption and utilization in fiber under 0 (Deficient P), 100 (Critical P), and 200 (Excessive P) kg P₂O₅ ha⁻¹ in soil with 16.9 mg kg⁻¹ available P.
P application significantly increased fiber bundle strength (8.9 %−14.6 %), primarily attributed to the enhanced sucrose supply and utilization in LSCB and fiber during the crucial period for fiber bundle strength formation (17–24 days post anthesis). During this period, P application promoted the sucrose synthesis in LSCB by improving the net photosynthetic rate (9.0 %−16.8 %), and sucrose phosphate synthase (6.3 %−12.4 %) and sucrose synthase (10.0 %−17.4 %) activities. Concomitantly, P application up-regulated the expressions of sucrose transporter genes in LSCB and fiber, promoting sucrose transport and increasing the sucrose content (28.1 %−54.0 %) in fiber. Furthermore, P application markedly enhanced the sucrose utilization in fiber by increasing sucrose synthase (9.7 %−19.2 %) and invertase (14.0 %−35.7 %) activities, improving cellulose content (6.7 %−11.5 %) and fiber bundle strength. Lu 54 exhibited a greater sensitivity to P in the carbohydrate metabolism of LSCB and fiber than Yuzaomian 9110, making its cellulose content and fiber bundle strength increase more. Incremental effects of unit P on the above measurements attenuated markedly with P rates. The critical P content in LSCB (LPC) required for effective fiber bundle strength formation was 0.40 % for Lu 54 versus 0.36 % for Yuzaomain 9110, on the basis of the content of sucrose (the key substrate) in LSCB and fiber.
P application increased cotton fiber bundle strength mainly by enhancing sucrose synthesis in LSCB, sucrose transport between LSCB and fiber, and sucrose utilization in fiber during the crucial period.
This report revealed the crucial carbohydrate metabolic path by which P regulated the fiber bundle strength formation and quantified its LPC demand during the crucial period, providing theoretical support for P diagnosis and regulation in cotton cultivation.
A review of recent advances in biomedical applications of smart cellulose-based hydrogels
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In biomedical engineering, smart materials act as media to communicate physiological signals inspired by environmentally responsive stimuli with outer indicators for timely scrutiny and precise therapy. Various physical and chemical processes are applied in the design of specific smart functions. Hydrogels are polymeric networks consisting of hydrophilic chains and chemical groups and they have contributed their unique features in biomedical application as one of the most used smart materials. Numerous raw materials can form hydrogels, in which cellulose and its derivatives have been extensively exploited in biomedicine due to their high hydrophilicity, availability, renewability, biodegradability, biocompatibility, and multifunctional reactivity. This review collates cellulose-based hydrogels and their extensive applications in the biomedical domain, specifically benefiting from the “SMART” concept in their design, synthesis and device assembly. The first section discusses the physical and chemical crosslinking and electrospinning techniques used in the fabrication of smart cellulose-based hydrogels. The second section describes the performance of these hydrogels, and the final section is a comprehensive discussion of their biomedical applications.
Wheat NILs contrasting in grain size show different expansin expression, carbohydrate and nitrogen metabolism that are correlated with grain yield
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Citation Excerpt :
SPS activity reflects the ability of flag leaves to convert photosynthate into sucrose (Champigny, 1995). SuSy activity reflects the sink strength because the enzyme catalyzes sucrose degradation in sink tissues (Delmer and Haigler, 2002; Schaffer and Petreikov, 1997). Higher starch accumulation and sugar metabolism in + GS grains (Fig. 4 and 5) may be due to high SPS and SuSy (Fig. 6) and up-regulation of starch-synthesis-related genes (Fig. 7).
Two wheat near-isogenic lines (NILs; -GS (small grain size) and + GS (large grain size)) were obtained by backcrossing. We found that the grain volume and weight of + GS were significantly higher than those of -GS. There was a corresponding increase in grain yield associated with the + GS line. For analysis of causes, we investigated and compared the anatomic and physiological characteristics of two NILs during the grain filling stage. The bigger grain size in + GS likely resulted from the longer endosperm cells, which is related to the higher IAA content and expansin activity accompanied by the up-regulation of some expansin-related genes. For the higher grain weight of + GS, starch accumulation was higher in + GS than in -GS, which was consistent with relatively higher glucose (Glu), fructose (Fru), and sucrose (Suc) contents. Elevated sugar level may be correlated with sucrose synthase (SuSy) activity and up-regulation of GBSS I, SSS III, and SBE I. The amount of soluble protein in + GS grains also exceeded that in -GS grains, possibly because of increased NR, NiR, and GS activities and up-regulation of nitrogen assimilation and nitrate transporter genes in + GS grains. Furthermore, the photosynthetic rate was higher in + GS and -GS at the early filling stage before 21 DAA. The same trends were observed in sugar content (Suc, Fru, and Glu) and SPS activity. However, the increase in the rate of grain length and width in + GS plants at the late filling stage was significantly higher than that at the early filling periods. These suggest that high accumulation of dry matter (such as starch and protein) at early filling stage was the important factor in achieving the final increased size of wheat grains, besides cell expansion.
Effects of planting dates and shading on carbohydrate content, yield, and fiber quality in cotton with respect to fruiting positions
2018, Journal of Integrative Agriculture
Two cotton (Gossypium hirsutum L.) cultivars, Kemian 1 (cool temperature-tolerant) and Sumian 15 (cool temperature-sensitive) were used to study the effects of cool temperature on carbohydrates, yield, and fiber quality in cotton bolls located at different fruiting positions (FP). Cool temperatures were created using late planting and low light. The experiment was conducted in 2010 and 2011 using two planting dates (OPD, the optimized planting date, 25 April; LPD, the late planting date, 10 June) and two shading levels of crop relative light rate (CRLR, 100 and 60%). Compared with fruiting position 1 (FP1), cotton yield and yield components (fiber quality, leaf sucrose and starch content, and fiber cellulose) were all decreased on FP3 under all treatments. Compared with OPD-CRLR 100%, other treatments (OPD-CRLR 60%, LPD-CRLR 100%, and LPD-CRLR 60%) had significantly decreased lint yield at both FPs of both cultivars, but especially at FP3 and in Sumian 15; this decrease was mainly caused by a large decline in boll number. All fiber quality indices decreased under late planting and shading except fiber length at FP1 with OPD-CRLR 60%, and a greater reduction was observed at FP3 and in Sumian 15. Sucrose content of the subtending leaf and fiber increased under LPD compared to OPD, whereas it decreased under CRLR 60% compared to CRLR 100%, which led to decreased fiber cellulose content. Therefore, shading primarily decreased the “source” sucrose content in the subtending leaf whereas late planting diminished translocation of sucrose towards cotton fiber. Notably, as planting date was delayed and light was decreased, more carbohydrates were distributed to leaf and bolls at FP1 than those at FP3, resulting in higher yield and better fiber quality at FP1, and a higher proportion of bolls and carbohydrates allocated at FP3 of Kemian 1 compared to that of Sumian 15. In conclusion, cotton yield and fiber quality were reduced less at FP1 compared to those at FP3 under low temperature and low light conditions. Thus, reduced cotton yield and fiber quality loss can be minimized by selecting low temperature tolerant cultivars under both low temperature and light conditions.
Carbon Supply and the Regulation of Cell Wall Synthesis
2018, Molecular Plant
Citation Excerpt :
Several factors have been reported to alter the rate of cell wall deposition including developmental progression (Refrégier et al., 2004; Derbyshire et al., 2007), hormone signaling including auxin (Ray, 1962; Baker and Ray, 1965; Ray and Baker, 1965; Edelmann et al., 1989; Edelmann and Fry, 1992c), gibberellins (Huang et al., 2015), and brassinosteroids (Xie et al., 2011; Wolf et al., 2012; Sánchez-Rodríguez et al., 2017), light, and, more specifically, phytochrome signaling (Kutschera, 1990; Bischoff et al., 2011), osmotic and salt stress (Crowell et al., 2009; Wormit et al., 2012; Endler et al., 2015), cell wall integrity signaling (Hématy et al., 2007; Wormit et al., 2012; Voxeur and Höfte, 2016; Xiao et al., 2016; Van der Does et al., 2017), hyperpolarization of the plasma membrane (Yeats et al., 2016), and the C supply (Fujimoto et al., 2015; Ishihara et al., 2015; Ivakov et al., 2017). It is to be expected that cell wall synthesis, as the single largest sink for C in plants (Delmer and Haigler, 2002), would be regulated by the C supply. However, the picture in the literature is rather confused.
All plant cells are surrounded by a cell wall that determines the directionality of cell growth and protects the cell against its environment. Plant cell walls are comprised primarily of polysaccharides and represent the largest sink for photosynthetically fixed carbon, both for individual plants and in the terrestrial biosphere as a whole. Cell wall synthesis is a highly sophisticated process, involving multiple enzymes and metabolic intermediates, intracellular trafficking of proteins and cell wall precursors, assembly of cell wall polymers into the extracellular matrix, remodeling of polymers and their interactions, and recycling of cell wall sugars. In this review we discuss how newly fixed carbon, in the form of UDP-glucose and other nucleotide sugars, contributes to the synthesis of cell wall polysaccharides, and how cell wall synthesis is influenced by the carbon status of the plant, with a focus on the model species Arabidopsis (Arabidopsis thaliana).
Co-occurring elevated temperature and waterlogging stresses disrupt cellulose synthesis by altering the expression and activity of carbohydrate balance-associated enzymes during fiber development in cotton
2017, Environmental and Experimental Botany
Citation Excerpt :
Callose synthase gene family contains more than 12 isoforms, and CalS-5 has been reported to play a vital role in callose synthesis in many publications (Herburger and Holzinger, 2015; Shi et al., 2015). In most higher plants the enzymes sucrose synthase (SuSy, EC 2.4.1.13), invertase (Inv, EC 3.2.1.26) and sucrose-phosphate synthase (SPS; EC 2.4.1.14) are involved in sucrose metabolism (Carnachan and Harris, 2000; Delmer and Haigler, 2002; Sturm, 1999). Sucrose synthase (SuSy) can channel UDPG to cellulose synthesis by forming a complex with cellulose synthase (Salnikov et al., 2001).
Soil waterlogging events and elevated temperature conditions occur frequently in the Yangtze River Valley, yet the effects of these co-occurring stresses on fiber development have received little attention. In this study, combined elevated temperature (34.1/29.0 °C) and soil waterlogging (3, 6 days) on fiber cellulose synthesis was investigated during flowering and boll development. The coupling of elevated temperature (ET) and soil waterlogging (SW) more negatively impacted final cellulose content (reduced by 9.5–27.5%) than either stress individually, and the effect of SW alone was greater than ET alone (34.1/29.0 °C). Treatment of ET alone mainly limited cellulose synthesis by decreasing activities of sucrose degrading enzymes, especially sucrose synthase. The combination of ET and SW disrupted deposition of sucrose and cellulose but increased the callose content of developing fibers. Increased sucrose synthase (SuSy) activity was the dominant factor influencing sucrose degradation in the fiber under the combination of ET and SW. Both sucrose phosphate synthase (SPS) and acid/alkaline Invertase activities were decreased under combined stresses of ET and SW and SPS was the most sensitive to the aforementioned stresses. GhSuSy-A and GhSPS-1 were the key gene isoforms closely associated with fiber sucrose metabolism under combined stresses. Co-occurring elevated temperature and waterlogging stresses highly up-regulated GhCalS-5 and β-1,3-glucanase expression levels, which led to increased fiber callose content. Thus, we concluded that concomitant exposure to elevated temperature and waterlogging limited cellulose synthesis not only by lowering sucrose metabolism enzyme activities but also by favoring the conversion of UDPG to callose rather than cellulose.

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Regular ArticleThe Regulation of Metabolic Flux to Cellulose, a Major Sink for Carbon in Plants

Abstract

J. Biol. Chem.

Curr. Biol.

Phytochemistry

FEBS Lett.

Arch. Biochem. Biophys.

A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants

Proc. Natl. Acad. Sci. USA

Molecular analysis of cellulose biosynthesis in Arabidopsis

Science

Biosynthesis of β-glucans in growing cotton (Gossypium arboreum L., and Gossypium hirsutum L.) fibers

Virus-induced silencing of a plant cellulose synthase gene

Plant Cell

Evidence for plasma membrane-associated forms of sucrose synthase in maize

Mol. Gen. Genet.

Cellulose synthesis: Exciting times for a difficult field

Annu. Rev. Plant Physiol. Plant Mol. Biol.

Cellulose biosynthesis in developing cotton fibers

Expression analysis of the ten cellulose synthase (CesA) genes of Arabidopsis thaliana

Proceedings of Plant Biology 200

Transgenic Arabidopsis plants with decreased activity of fructose-6-phosphate, 2-kinase/fructose-2,6-bisphosphatase have altered carbon partitioning

Plant Physiol.

Procuste1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis

Plant Cell

A “futile” cycle of sucrose synthesis and degradation is involved in regulating partitioning between sucrose, starch, and respiration in cotyledons of germinating Ricinus communis L. seedlings when phloem transport is inhibited

Planta

Cultured cotton ovules as models for cotton fiber development under low temperatures

Plant Physiol.

Transgenic cotton over expressing sucrose phosphate synthase produces higher quality fibers with increased cellulose content and has enhanced seed cotton yield

Proceedings of Plant Biology 2000

Carbon partitioning to cellulose synthesis

Plant Mol. Biol.

Extractable activities and protein content of sucrose-phosphate-synthase and neutral invertase in trunk tissues of Robinia pseudoacacia L. are related to cambial wood production and heartwood formation

Planta

Evidence that the rug3 locus of pea (Pisum sativum L.) encodes plastidial phosphoglucomutase confirms that the imported substrate for starch synthesis in pea amyloplasts is glucose-6-phosphate

Plant J.

Rapid cycling of triose phosphates in oak stem tissue

Plant Cell Environ.

A comparative analysis of the plant cellulose synthase (CesA) gene family

Plant Physiol.

Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees

Nat. Biotechnol.

Sugar and metabolic regulation of genes for sucrose metabolism: Potential influence of maize sucrose synthase and soluble invertase responses on carbon partitioning and sugar sensing

J. Exp. Bot.

Temperature-sensitive alleles of RSW1 link the KORRIGAN endo-1,4-β-glucanase to cellulose synthesis and cytokinesis in Arabidopsis

Plant Physiol.

Regular Article
The Regulation of Metabolic Flux to Cellulose, a Major Sink for Carbon in Plants