Recent advances in plant genome sequencing and assembly and the publication of new draft genomes have allowed the SUS gene family to be characterized in many plant species and in a more comprehensive manner. (2002). Biol. J. Biol. doi: 10.1046/j.1365-313X.2003.01765.x, Gordon, A. J., Minchin, F. R., James, C. L., and Komina, O. Plant SuSy enzymes have been shown to be involved in several different metabolic pathways, such as those for starch, callose and cellulose synthesis, and to play developmental and possibly signaling roles in sink carbohydrate flux, vascular tissues and meristem functioning. Gene 539, 58–67. doi: 10.1042/0264-6021:3440503. Four carbohydrates, D-glucose. doi: 10.1104/pp.106.4.1659, Sheen, J., Zhou, L., and Jang, J. C. (1999). doi: 10.1371/journal.pone.0182334, Guerin, J., and Carbonero, P. (1997). Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. doi: 10.1074/jbc.M114.585554. Amor, Y., Haigler, C. H., Johnson, S., Wainscott, M., and Delmer, D. P. (1995). Plant Physiol. Evidence for a tonoplast-associated form of sucrose synthase and its potential involvement in sucrose mobilization from the vacuole. Structural features of the maize sus1 gene and protein. 25, 663–674. Plant Prod. Plant Microbe Interact. Plant Physiol. SuSy activity has also been found to be correlated with rice coleoptile length under submerged conditions, further indicating the advantage of Suc metabolism that involves SuSy under anoxic conditions (Fukuda et al., 2008). Funct. One possibility is suggested by their differential subcellular locations. doi: 10.1007/s00425-015-2297-1, Wei, Z. G., Qu, Z. S., Zhang, L. J., Zhao, S. J., Bi, Z. H., Ji, X. H., et al. Sucrose synthase is an integral component of the cellulose synthesis machinery. Sucrase, lactase and other pancreatic enzymes break down sucrose and lactose. Structure and expression analysis of the sucrose synthase gene family in apple. 39, 349–360. A., Luan, S., Wi, S. G., Bae, H., Lee, D. S., and Bae, H. J. Required fields are marked *. A. S. Basra (New York, NY: Food Products Press), 85–112. RNAseq data obtained by Park et al. Plant Mol. Plant physiologists and biochemists have tried to find the first product of this process. Isolation and sequences of rice sucrose synthase cDNA and genomic DNA. Sucrose synthase expression pattern in young maize leaves: implications for phloem transport. Plant Physiol. Gymnosperm species are labeled with a green arc. Trends Plant Sci. J. Suppression of sucrose synthase gene expression represses cotton fiber cell initiation, elongation, and seed development. 104, 535–540. Only five genes have been characterized in grape (Vitis vinifera) and sugarcane (Saccharum spp. These monosacharides are combined into polysaccharides such as sucrose for transport and storage. doi: 10.1371/journal.pone.0120669, Werr, W., Frommer, W. B., Maas, C., and Starlinger, P. (1985). (2016). 54, 1407–1414. Sucrose synthase belongs to the glycosyltransferase-4 subfamily of glycosyltransferases, a large family that includes a wide variety of glycosyltransferases, including SPS, trehalose synthase, and trehalose phosphorylase. The formula associated with the process of photosynthesis is. Analyses of the sucrose synthase gene family in cotton: structure, phylogeny and expression patterns. Breed. The second site is also a serine, at around position 170, and is thought to regulate protein degradation (Hardin et al., 2003). All these observations support the role of SuSy in starch accumulation. doi: 10.1016/j.plantsci.2008.07.013, Kunz, S., Pesquet, E., and Kleczkowski, L. A. Chem. 25, 402–411. In Chinese pear (Pyrus bretschneideri Rehd. Biochem. Proc. Similarly, overexpression of SUS resulted in higher ADP-G levels and starch accumulation in maize endosperm (Li et al., 2013), and Arabidopsis T-DNA mutants for AtSUS2 and AtSUS3 exhibited reduced transient starch accumulation in seeds during early to mid-development (Angeles-Nunez and Tiessen, 2010). Maize sucrose synthase-1 promoter directs phloem cell-specific expression of GUS gene in transgenic tobacco plants. Although imported photoassimilate can be used for respiration, sink-strength estimations are mainly based on net weight gain (Ho, 1988). Pronounced phenotypic changes in transgenic tobacco plants overexpressing sucrose synthase may reveal a novel sugar signaling pathway. Phytochemistry 57, 823–833. Plant SUS gene families are usually small, containing between four to seven genes, with distinct exon-intron structures. In addition, five maize starch-deficient endosperm mutants were screened for metabolic enzyme activity and all showed reduced SuSy activity (Doehlert and Kuo, 1990). doi: 10.1093/pcp/pcj068, Etxeberria, E., and Gonzalez, P. (2003). doi: 10.1104/pp.116.4.1323, Ruan, Y. L. (2007). Chem. 39, 459–466. 92, 990–994. “Cellulose biosynthesis in developing cotton fibers,” in Cotton Fibres: Developmental Biology, Quality Improvement, and Textile Processing, ed. Proc. Sytykiewicz, H., Czerniewicz, P., and Leszczyñski, B. Each clade is divided into two sub-clades: monocots (marked with red arcs) and eudicots (marked with turquoise arcs). doi: 10.1023/A:1006199003756, Subbaiah, C. C., Palaniappan, A., Duncan, K., Rhoads, D. M., Huber, S. C., and Sachs, M. M. (2006). doi: 10.1073/pnas.0900188106, Counce, P. A., and Gravois, K. A. Sucrose is the end product of photosynthesis and the primary sugar transported in the phloem of most plants. doi: 10.1371/journal.pone.0104997, Bahaji, A., Li, J., Sanchez-Lopez, A. M., Baroja-Fernandez, E., Munoz, F. J., Ovecka, M., et al. None of those mutants exhibit any significant phenotype that suggesting redundancy between the different clades (Bieniawska et al., 2007). 592, 2525–2532. doi: 10.1111/j.1467-7652.2005.00160.x, Coleman, H. D., Yan, J., and Mansfield, S. D. (2009). Sci. In situ hybridization has revealed the accumulation of AtSUS5 and AtSUS6 specifically in the phloem of Arabidopsis roots and hypocotyls (Barratt et al., 2009). Transcript levels of some SUS genes have been found to increase in response to low levels of oxygen in potato (Biemelt et al., 1999), maize (McCarty et al., 1986; Bailey-Serres et al., 1988; Zeng et al., 1998), rice (Ricard et al., 1991; Hirose et al., 2008), carrot (Sturm et al., 1999), Arabidopsis (Martin et al., 1993; Dejardin et al., 1999; Baud et al., 2004), wheat (Marana et al., 1990), beet (Hesse and Willmitzer, 1996; Klotz and Haagenson, 2008), pigeon pea (Cajanus cajan) (Kumutha et al., 2008) and pondweed (Potamogeton distinctus ) (Harada et al., 2004, 2005). Another potential heat-tolerant SuSy was purified from a heat-tolerant line of wheat (WH-1021). Oxygen deficiency has also been shown to increase SuSy protein levels in Arabidopsis roots (Bieniawska et al., 2007) and leaves (Dejardin et al., 1999) and in maize roots (Zeng et al., 1998). In vivo and in vitro phosphorylation of membrane and soluble forms of soybean nodule sucrose synthase. In Arabidopsis, a double-knockout mutant (sus1 and sus4) was found to be more sensitive to flooding than the control (Bieniawska et al., 2007), but did not differ from the WT in its responses to hypoxia or anoxia (Santaniello et al., 2014). 89, 1117–1121. Plant SuSy proteins are found primarily in the cytosol or adjacent to the plasma membrane, although some SuSy isoforms are found in cell walls, mitochondria or vacuoles, or are bound to actin. In maize, phosphorylation of SuSy was found to result in decreased membrane association; whereas dephosphorylation was found to cause SuSy to be less soluble (Winter et al., 1997). SuSy protein has also been immunolocalized to the phloem companion cells in citrus and maize (Nolte and Koch, 1993) and in leaves of 9-day-old barley seedlings (Guerin and Carbonero, 1997). Natl. doi: 10.1007/s004250050482, Hesse, H., and Willmitzer, L. (1996). A study of potato tubers of transgenic plants overexpressing INV or Suc pyrophosphorylase, which allows a way to bypass the degradation of Suc by SuSy, revealed a steeper reduction in oxygen levels inside the tubers, reduced starch synthesis and a lower ATP to ADP ratio, underscoring the importance of SuSy under low-oxygen conditions (Bologa et al., 2003). The development of cotton fibers starts with the initiation and elongation of the epidermal cells, followed by secondary growth and maturation marked by massive cellulose production. Evol. Plant Cell 11, 2407–2418. Sucrose synthase catalyzes the de novo production of ADPglucose linked to starch biosynthesis in heterotrophic tissues of plants. Partial sequences and sequences with substantial deletions were excluded, leaving a total of 133 sequences (Supplementary File 1). Localization of SuSy from tobacco (Nicotiana tabacum) pollen tubes, revealed two isoforms, one of which is associated with the plasma membrane and the other one is associated with the plasma membrane and is also found in the cytosol (Persia et al., 2008). 344(Pt. (2004). (2014b) suggested a chloroplast starch synthesis model in which (1) Suc cleavage by SuSy produces cytosolic ADP-G which is transported to the chloroplast for starch synthesis and (2) plastidic PGM and AGPase are recycling Glc units derived from starch breakdown back to starch. 12:85. doi: 10.1186/1471-2229-12-85, Chengappa, S., Guilleroux, M., Phillips, W., and Shields, R. (1999). However, it is important to note that some of these trees were created using limited numbers of monocot or dicot species. doi: 10.1626/pps.11.67, Geigenberger, P., Langenberger, S., Wilke, I., Heineke, D., Heldt, H. W., and Stitt, M. (1993). Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Overexpression of SUS in several plant species increased the thickness of xylem cell walls (Coleman et al., 2009; Wei et al., 2015), further supporting the proposed roles of SuSy in xylem development (also discussed in section “Roles of SuSy in Cellulose and Callose Metabolism”). Plant SUS genes are divided into three separate clades, which are present in both monocots and dicots. Similarly, overexpression of aspen (Popolus tremuloides) SUS in Arabidopsis resulted in an increased growth rate and increased plant biomass, and also induced early flowering (Xu and Joshi, 2010). Sucrose is the most abundant disaccharide and the major product of photosynthesis. ADP-G levels in leaves of AGPase- and pPGM-mutant plants are comparable with those seen in the WT, indicating that AGPase is not the only source of ADP-G (Munoz et al., 2005; Bahaji et al., 2011, 2014a). (2017). No use, distribution or reproduction is permitted which does not comply with these terms. The products of sucrose cleavage by SuSy are available for many metabolic pathways, such as energy production, primary-metabolite production, and the synthesis of complex carbohydrates. Plant Cell Physiol. In cucumber, antisense suppression of CsSUS3 led to increased sensitivity to hypoxic stress (Wang et al., 2014). Sucrose synthase is associated with the cell wall of tobacco pollen tubes. After that sucrose and later starch appeared. doi: 10.1007/BF00018465, Chourey, P. S., and Nelson, O. E. (1976). The brush borders produces another enzyme referred to as maltase that breaks down maltose into glucose. PLoS One 9:e104997. Use of the rice sucrose synthase-1 promoter to direct phloem-specific expression of beta-glucuronidase and snowdrop lectin genes in transgenic tobacco plants. 106, 1659–1665. Impact Factor 4.402 | CiteScore 7.8More on impact ›. 45, 623–631. The tree was created using the maximum-likelihood method based on the JTT matrix-based model (Jones et al., 1992). The products of sucrose cleavage by SuSy are available for many metabolic pathways, such as energy production, primary-metabolite production, and the synthesis of complex carbohydrates. Sucrose synthase is the only Suc-metabolizing enzyme that can catalyze both the synthesis of Suc from Fru and UDP-G and the cleavage of Suc, in the presence of UDP, to Fru and UDP-G. SuSy can also utilize other nucleotide phosphates for Suc cleavage, especially ADP, but usually with a lower affinity. Inside sink cells, Suc can be metabolized or transported to the vacuole, where it can be stored as Suc, transformed into fructans by fructosyltransferases (FTs), or hydrolyzed by vacuolar invertase (vINV) and stored as hexoses (Figure 1). Photosynthesis splits water into hydrogen and oxygen atoms in a reaction that requires sunlight (light reaction). In another study, researchers examined transgenic tobacco plants overexpressing each of the six Arabidopsis SUS genes (AtSUS1-AtSUS6) and found that all of those lines grew more quickly and were taller and thicker than the WT plants (Nguyen et al., 2016). Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. 1). (1999). Biol. So sucrose and starch are … MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. The SuSy in plasma membranes and cell walls and their production of UDP-G may be important for directing carbon toward cellulose or callose synthesis; whereas INV may direct carbon to other metabolic pathways. Evidence for plasma membrane-associated forms of sucrose synthase in maize. Annu. Triose-P can be transported to the cytosol by a triose-P/phosphate translocator. To be metabolized, Suc must be cleaved by either cytosolic invertase or SuSy (EC 2.4.1.13). The end products of photosynthesis are oxygen and glucose (if you have been in an AP Biology class or a college biology class, you would also know that some water is created in photosynthesis). 10:95. doi: 10.3389/fpls.2019.00095. Sucrose synthase controls both intracellular ADP glucose levels and transitory starch biosynthesis in source leaves. 47, 29–51. In vitro phosphorylation of rice SuSy proteins, Rsus1-3 may promote SuSy activity (Takeda et al., 2017). Biol. Although the mechanism by which SUS overexpression speeds up the growth rate is not clear, it is tempting to speculate that increased SuSy activity in the meristem may facilitate increased cell proliferation. Phytochemistry 25, 1579–1585. Biol. Another reason to believe that Suc and SuSy may play some regulatory function rather than just a metabolic one comes from tomato plants in which the expression of three SUS genes was suppressed (Goren et al., 2017). Planta 233, 1011–1023. Plant. doi: 10.1073/pnas.1114963109, Peron, T., Veronesi, C., Mortreau, E., Pouvreau, J. But still it is not clear which the first product of photosynthesis. Anaerobic stress induces the transcription and translation of sucrose synthase in rice. In beet, SUS1 mRNA levels increased under anaerobic conditions, but there was no increase in SuSy1 protein (Klotz and Haagenson, 2008). Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Work with promoter-GUS fusions has revealed SUS promoter activity in the phloem of many plant species, including potato (Fu and Park, 1995), Arabidopsis (Martin et al., 1993; Bieniawska et al., 2007), maize (Yang and Russell, 1990), rice (Shi et al., 1994), tomato (Goren et al., 2017) and Craterostigma plantagineum (Kleines et al., 1999). The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fpls.2019.00095/full#supplementary-material. Plant Cell Physiol. Yang, C. L., and Su, J. C. (1980). doi: 10.1104/pp.98.3.1163, Sung, S. J. S., Xu, D. P., and Black, C. C. (1989). Biotechnol. Sucrose synthase activity as a potential indicator of high rice grain yield. In contrast, SUS suppression in the developing wood of hybrid aspen (Populus tremula L. × tremuloides Michx.) Biol. In Arabidopsis, six SUS genes have been characterized (Baud et al., 2004), similarly, six SUS genes have been identified in each of the following species: rice (Hirose et al., 2008), tomato (Goren et al., 2017), rubber tree (Hevea brasiliensis) (Xiao et al., 2014), cacao (Theobroma cacao L.) (Li et al., 2015), peach (Prunus persica) (Zhang et al., 2015) and Nicotiana sylvestris (Wang et al., 2015). Plant Biol. (2015). The hexoses can be phosphorylated to hexose phosphates (hex-P), directed to starch synthesis in the plastid or to glycolysis and then respiration in the mitochondria or directed to other metabolic pathways. Plant Physiol. 129, 1664–1673. SuSy monomers average about 90 kDa in weight and 800 amino acids in length, but some SuSy isoforms are considerably different. Planta 242, 153–166. 11, 67–75. An expression analysis profile for the entire sucrose synthase gene family in rice. Plant Interact. (2012) indicate that out of the six tomato SUS genes, SlSUS1, SlSUS3, and SlSUS4 transcripts are found in both meristems and in primordia at all development stages in different ratios (Goren et al., 2017). Gen. Genet. G1P is then converted into ADP-G, in a reaction catalyzed by ADP-G pyrophosphorylase (AGPase). Biotechnol. Differential regulation of sugar-sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and posttranscriptional responses. 63, 3367–3377. Quaternary structure of sucrose synthetase from banana fruits. Sci. The 'end-product inhibition of photosynthesis" hypothesis, as proposed over 100 years ago by Boussingault (3), states that the accumulation of assimilates in an illuminated leaf U.S.A. 101, 13080–13085. 55, 397–409. New insight into the catalytic properties of rice sucrose synthase. doi: 10.1104/pp.101.3.899, Park, S. J., Jiang, K., Schatz, M. C., and Lippman, Z. doi: 10.1073/pnas.1117099109, Baroja-Fernandez, E., Munoz, F. J., Montero, M., Etxeberria, E., Sesma, M. T., Ovecka, M., et al. While invertase (INV) catalyzes the irreversible hydrolyzation of Suc into its hexose monomers, Glc and Fru, SuSy catalyzes the reversible cleavage of Suc using UDP to yield fructose and UDP-G. On the other hand, Amor et al. J. Chin. Other SuSy isoforms are much smaller, for example, the bird cherry SuSy monomers are estimated to be about 53, 58, and 63 kDa (Sytykiewicz et al., 2008). Planta 217, 628–638. In chloroplasts, the main starch-synthesis pathway starts with two molecules of triose-P produced by photosynthesis, which yield F1,6BP. Sucrose synthase, a cytosolic enzyme in protoplasts of Jerusalem artichoke tubers (Helianthus tuberosus L.). Plant Cell Physiol. Right side shows photosynthesis in which sunlight and water in the atmosphere are absorbed by plants and algae to generate ATP and NADPH, which make carbohydrates and other organic carbon products from carbon dioxide, which is absorbed from the atmosphere separately. Temporal and spatial expression pattern of sucrose synthase during tomato fruit development. doi: 10.5511/plantbiotechnology.17.0326a, Takehara, K., Murata, K., Yamaguchi, T., Yamaguchi, K., Chaya, G., Kido, S., et al. (1998). doi: 10.1111/febs.12595, Xu, F., and Joshi, C. (2010). 116, 1323–1331. Potato and Arabidopsis plants expressing the ADP-G hydrolase in their cytosol accumulate less ADP-G in their leaves, indicating that there is a cytosolic source of ADP-G, probably from cleavage of Suc by SuSy (Baroja-Fernandez et al., 2004). (1995) concluded that SuSy is not a transmembrane protein because it was not partitioned into triton X-114. 37, 2294–2302. C O2. In the secondary growth phase of cotton fibers, cellulose synthesis can increase 100-fold relative to the elongation phase (Delmer, 1999) and this process probably involves SusC and SusA (Brill et al., 2011). doi: 10.1016/S2095-3119(17)61755-6, Van Bel, M., Diels, T., Vancaester, E., Kreft, L., Botzki, A., Van De Peer, Y., et al. hexoses. doi: 10.1007/BF00018467, Zeng, Y., Wu, Y., Avigne, W. T., and Koch, K. E. (1998). Z., Shen, Y. Y., and Guo, J. X. Ann. 40, 213–221. Seven SUS genes have been identified in cotton (Gossypium arboreum) (Chen et al., 2012), bamboo (Bambusa emeiensis) (Huang et al., 2018) and Nicotiana tomentosiformis (Chen et al., 2012; Wang et al., 2015; Huang et al., 2018). (2016). doi: 10.1104/pp.002360, Konishi, T., Ohmiya, Y., and Hayashi, T. (2004). Plant Physiol. 4, 113–117. ): structure, expression, and evolution. Sucrose is the end product of photosynthesis and is found naturally in many food plants along with the monosaccharide fructose. And increased starch accumulation and yield ( Baroja-Fernandez et al., 2017 ) carbohydrates in...: 10.1073/pnas.83.23.9099, Morell, M. L. ( 1985 ) studies have mutant. Hydrogen and oxygen are the products Biology, Quality Improvement, and Guo,,! Pathways ( Ma et al., 2017 ) is an integral component the. Tong et al., 1999 ) produce one fructose 1,6-bisphosphate ( F1,6BP ) molecule in plants., J., Chen, Y., Schaffer, a definitions and POINTS... 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The parasitic plant Phelipanche ramosa L. ( 2007 ) the rice sucrose synthase activity as a for. Of maize roots using a double mutant of phloem-specific SUS ( sus5 sus6 ), Jiang, E.!, Yoshinaga, S., Pesquet, E., Sharma, B., Rivoal J.! Another, less studied role in metabolism under low-oxygen conditions sucrose storers and supporting. Cellulose production and altered cell wall polymers ( Vitis vinifera ): structure, phylogeny and profile! Zhang et al., 1998 ; Azama et al. end product of photosynthesis is sucrose 2007 ) answer for competitive exams is provided by.! Points for OBJECTIVES of plant DIVERSITY, Novi, G., and Sonnewald,....