1932

Abstract

Sucrose metabolism plays pivotal roles in development, stress response, and yield formation, mainly by generating a range of sugars as metabolites to fuel growth and synthesize essential compounds (including protein, cellulose, and starch) and as signals to regulate expression of microRNAs, transcription factors, and other genes and for crosstalk with hormonal, oxidative, and defense signaling. This review aims to capture the most exciting developments in this area by evaluating () the roles of key sucrose metabolic enzymes in development, abiotic stress responses, and plant–microbe interactions; () the coupling between sucrose metabolism and sugar signaling from extra- to intracellular spaces; () the different mechanisms by which sucrose metabolic enzymes could perform their signaling roles; and () progress on engineering sugar metabolism and transport for high yield and disease resistance. Finally, the review outlines future directions for research on sugar metabolism and signaling to better understand and improve plant performance.

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2014-04-29
2024-03-29
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Literature Cited

  1. Altenbach D, Rudiño-Pinera E, Olvera C, Boller T, Wiemken A. 1.  et al. 2009. An acceptor-substrate binding site determining glycosyl transfer emerges from mutant analysis of a plant vacuolar invertase and a fructosyltransferase. Plant Mol. Biol. 69:47–56 [Google Scholar]
  2. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP. 2.  1995. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc. Natl. Acad. Sci. USA 92:9353–57 [Google Scholar]
  3. Andersen MN, Asch F, Wu Y, Jensen CR, Naested H. 3.  et al. 2002. Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiol. 130:591–604 [Google Scholar]
  4. Antony G, Zhou J, Huang S, Li T, Liu B. 4.  et al. 2010. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22:3864–76 [Google Scholar]
  5. Antunes WC, Provart NJ, Williams TCR, Loureiro ME. 5.  2012. Changes in stomatal function and water use efficiency in potato plants with altered sucrolytic activity. Plant Cell Environ. 35:747–59 [Google Scholar]
  6. Babb VM, Haigler CH. 6.  2001. Sucrose phosphate synthase activity rises in correlation with high-rate cellulose synthesis in three heterotrophic systems. Plant Physiol. 127:1234–42 [Google Scholar]
  7. Balibra Lara ME, Gonzalez Garcia MC, Fatima T, Ehneß R, Lee TK. 7.  et al. 2004. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16:1276–87 [Google Scholar]
  8. Baroja-Fernández E, Muñoz FJ, Li J, Almagroa G, Montero M. 8.  et al. 2012. Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc. Natl. Acad. Sci. USA 109:321–26 [Google Scholar]
  9. Barratt DH, Derbyshire P, Findlay K, Pike M, Wellner N. 9.  et al. 2009. Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc. Natl. Acad. Sci. USA 106:13124–29 [Google Scholar]
  10. Bate NJ, Niu X, Wang Y, Reimann KS, Helentjaris TG. 10.  2004. An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development. Plant Physiol. 134:246–54 [Google Scholar]
  11. Berger S, Sinha AK, Roitsch T. 11.  2007. Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. J. Exp. Bot. 58:4019–26 [Google Scholar]
  12. Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P. 12.  1993. Physiological signals that induce flowering. Plant Cell 5:1147–55 [Google Scholar]
  13. Bhaskar PB, Wu L, Busse JS, Whitty BR, Hamernik AJ. 13.  et al. 2010. Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol. 154:939–48 [Google Scholar]
  14. Bieniawska Z, Paul Barratt DH, Garlick AP, Thole V, Kruger NJ. 14.  et al. 2007. Analysis of the sucrose synthase gene family in Arabidopsis. Plant J. 49:810–28 [Google Scholar]
  15. Bonfig KB, Gablera A, Simon UK, Luschin-Ebengreuth N, Hatzc M. 15.  et al. 2010. Post-translational derepression of invertase activity in source leaves via down-regulation of invertase inhibitor expression is part of the plant defense response. Mol. Plant 3:1037–48 [Google Scholar]
  16. Boyer JS, McLaughlin JE. 16.  2007. Functional reversion to identify controlling genes in multigenic responses: analysis of floral abortion. J. Exp. Bot. 58:267–77 [Google Scholar]
  17. Brill E, van Thournout M, White RG, Llewellyn D, Campbell P. 17.  et al. 2011. A novel isoform of sucrose synthase is targeted to the cell wall during secondary cell wall synthesis in cotton fibre. Plant Physiol. 157:40–54 [Google Scholar]
  18. Cabib E, Leloir LF. 18.  1958. The biosynthesis of trehalose phosphate. J. Biol. Chem. 231:259–75 [Google Scholar]
  19. Cai G, Faleri C, Del Casino C, Emons AM, Cresti M. 19.  2011. Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiol. 155:1169–90 [Google Scholar]
  20. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML. 20.  et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–32 [Google Scholar]
  21. Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S. 21.  et al. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–11 [Google Scholar]
  22. Cheng WH, Chourey PS. 22.  1999. Genetic evidence that invertase-mediated release of hexoses is critical for appropriate carbon partitioning and normal seed development in maize. Theor. Appl. Genet. 98:485–95 [Google Scholar]
  23. Cheng WH, Tallercio EW, Chourey PS. 23.  1996. The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8:971–83 [Google Scholar]
  24. Chiou TJ, Bush DR. 24.  1998. Sucrose is a signal molecule in assimilate partitioning. Proc. Natl. Acad. Sci. USA 95:4784–88 [Google Scholar]
  25. Cho YH, Yoo SD. 25.  2011. Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genet 7:e1001263 [Google Scholar]
  26. Cho YH, Yoo SD, Sheen J. 26.  2006. Regulatory functions of nuclear hexokinase 1 complex in glucose signaling. Cell 127:579–89 [Google Scholar]
  27. Chourey PS, Taliercio EW, Carlson SJ, Ruan Y-L. 27.  1998. Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol. Gen. Genet 259:88–96 [Google Scholar]
  28. Chu Z, Fu B, Yang H, Xu C, Li Z. 28.  et al. 2006. Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor. Appl. Genet 112:455–61 [Google Scholar]
  29. Chu Z, Yuan M, Yao J, Ge X, Yuan B. 29.  et al. 2006. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev 20:1250–55 [Google Scholar]
  30. Coleman HD, Yan J, Mansfield SD. 30.  2009. Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc. Natl. Acad. Sci. USA 106:13118–23 [Google Scholar]
  31. D'Aoust MA, Yelle S, Nguyen-Quoc B. 31.  1999. Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and the sucrose unloading capacity of young fruit. Plant Cell 11:2407–18 [Google Scholar]
  32. Drigo B, Pijl AS, Duyts H, Kielak AM, Gamper HA. 32.  et al. 2010. Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. Proc. Natl. Acad. Sci. USA 107:10938–42 [Google Scholar]
  33. Duncan KA, Huber SC. 33.  2007. Sucrose synthase oligomerization and F-actin association are regulated by sucrose concentration and phosphorylation. Plant Cell Physiol. 48:1612–23 [Google Scholar]
  34. Eveland AL, Jackson DP. 34.  2012. Sugars, signalling, and plant development. J. Exp. Bot. 63:3367–77 [Google Scholar]
  35. Fallahi H, Scofield GN, Badger MR, Chow WS, Furbank RT. 35.  et al. 2008. Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J. Exp. Bot. 59:3283–95 [Google Scholar]
  36. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ. 36.  et al. 2003. The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol. 132:821–29 [Google Scholar]
  37. Foyer CH, Shigeoka S. 37.  2011. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 155:93–100 [Google Scholar]
  38. Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D. 38.  2004. Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305:1786–89 [Google Scholar]
  39. Fu H, Park WD. 39.  1995. Sink- and vascular-associated sucrose synthase functions are encoded by different gene classes in potato. Plant Cell 7:1369–85 [Google Scholar]
  40. Fujii S, Hayashi T, Mizuno K. 40.  2010. Sucrose synthase is an integral component of the cellulose synthesis machinery. Plant Cell Physiol. 51:294–301 [Google Scholar]
  41. Gisel A, Barella S, Hempel FD, Zambryski PC. 41.  1999. Temporal and spatial regulation of symplastic trafficking during development in Arabidopsis thaliana apices. Development 126:1879–89 [Google Scholar]
  42. Godt DE, Roitsch T. 42.  1997. Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol. 115:273–82 [Google Scholar]
  43. Goetz M, Godt DE, Guivarch A, Kahmann U, Chriqui D. 43.  et al. 2001. Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc. Natl. Acad. Sci. USA 986522–27
  44. Greiner S, Krausgrill S, Rausch T. 44.  1998. Cloning of a tobacco apoplasmic invertase inhibitor: proof of function of the recombinant protein and expression analysis during plant development. Plant Physiol. 116:733–42 [Google Scholar]
  45. Greiner S, Rausch T, Sonnewald U, Herbers K. 45.  1999. Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers. Nat. Biotechnol. 17:708–11 [Google Scholar]
  46. Hardin SC, Winter H, Huber SC. 46.  2004. Phosphorylation of the amino terminus of maize sucrose synthase in relation to membrane association and enzyme activity. Plant Physiol. 134:1427–38 [Google Scholar]
  47. Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B. 47.  et al. 2011. A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–23 [Google Scholar]
  48. Herbers K, Meuwly P, Frommer WB, Métraux JP, Sonnewald U. 48.  1996. Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803 [Google Scholar]
  49. Heyer AG, Raap M, Schroeer B, Marty B, Willmitzer L. 49.  2004. Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana. Plant J. 39:161–69 [Google Scholar]
  50. Hothorn M, Van den Ende W, Lammens W, Rybin V, Scheffzek K. 50.  2010. Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein. Proc. Natl. Acad. Sci. USA 107:17427–32 [Google Scholar]
  51. Huber SC, Huber JL. 51.  1996. Role and regulation of sucrose phosphate synthase in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47431–44
  52. Ji X, Shiran B, Wan J, Lewis DC, Jenkins CLD. 52.  et al. 2010. Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ. 33:926–42 [Google Scholar]
  53. Ji X, Van den Ende W, Van Laere A, Cheng S, Bennett J. 53.  2005. Structure, evolution, and expression of the two invertase gene families of rice. J. Mol. Evol. 60:615–34 [Google Scholar]
  54. Jia L, Zhang B, Mao C, Li J, Wu Y. 54.  et al. 2008. OsCYT-INV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.). Planta 228:51–59 [Google Scholar]
  55. Jiang Y, Guo W, Zhu H, Ruan Y-L, Zhang TZ. 55.  2012. Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality. Plant Biotechnol. J. 10:301–12 [Google Scholar]
  56. Jin Y, Ni DA, Ruan Y-L. 56.  2009. Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21:2072–89 [Google Scholar]
  57. Jonik C, Sonnewald U, Hajirezaei MR, Flügge UI, Ludewig F. 57.  2012. Simultaneous boosting of source and sink capacities doubles tuber starch yield of potato plants. Plant Biotechnol. J. 10:1088–98 [Google Scholar]
  58. Kakumanu A, Ambavaram MMR, Klumas C, Krishnan A, Batlang U. 58.  et al. 2012. Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol. 160846–67
  59. Kebrom TH, Chandler PM, Swain SM, King RW, Richards RA, Spielmeyer W. 59.  2012. Inhibition of tiller bud outgrowth in the tin mutant of wheat is associated with precocious internode development. Plant Physiol. 160:308–18 [Google Scholar]
  60. Keunen E, Peshev D, Vangronsveld J, Van Den Ende W, Cuypers A. 60.  et al. 2013. Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ. 36:1242–55 [Google Scholar]
  61. Kim M, Lim JH, Chang SA, Park K, Kim GT. 61.  et al. 2006. Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18:2341–55 [Google Scholar]
  62. Kircher S, Schopfer P. 62.  2012. Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis. Proc. Natl. Acad. Sci. USA 109:11217–21 [Google Scholar]
  63. Klann EM, Chetelat RT, Bennett AB. 63.  1993. Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiol. 103:863–70 [Google Scholar]
  64. Klann EM, Hall B, Bennett AB. 64.  1996. Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiol. 112:1321–30 [Google Scholar]
  65. Koch KE. 65.  1996. Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:509–40 [Google Scholar]
  66. Koch KE. 66.  2004. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7:235–46 [Google Scholar]
  67. Kohorn BD, Kobayashi M, Johansen S, Riese J, Huang LF. 67.  et al. 2006. An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. Plant J. 46:307–16 [Google Scholar]
  68. Koonjul PK, Minhas JS, Nunes C, Sheoran IS, Saini HS. 68.  2005. Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. J. Exp. Bot. 56:179–90 [Google Scholar]
  69. Lalonde S, Beebe DU, Saini HS. 69.  1997. Early signs of disruption of wheat anther development associated with the induction of male sterility by meiotic-stage water deficit. Sex. Plant Reprod. 10:40–48 [Google Scholar]
  70. Le Roy K, Lammens W, Verhaest M, De Coninck B, Rabijns A. 70.  et al. 2007. Unraveling the difference between invertases and fructan exohydrolases: A single amino acid (Asp-239) substitution transforms Arabidopsis cell wall invertase1 into a fructan 1-exohydrolase. Plant Physiol 145:616–25 [Google Scholar]
  71. Le Roy K, Vergauwen R, Struyf T, Yuan S, Lammens W. 71.  et al. 2013. Understanding the role of defective invertases in plants: Tobacco Nin88 fails to degrade sucrose. Plant Physiol. 161:1670–81 [Google Scholar]
  72. Leloir LF, Cardini CE. 72.  1955. The biosynthesis of sucrose phosphate. J. Biol. Chem. 214:157–65 [Google Scholar]
  73. Leslie M. 73.  2013. Dead enzymes show signs of life. Science 340:25–27 [Google Scholar]
  74. Li B, Liu H, Zhang Y, Kang T, Zhang L. 74.  et al. 2013. Constitutive expression of cell wall invertase genes increases grain yield and starch content in maize. Plant Biotechnol. J. 11:1080–91 [Google Scholar]
  75. Li C, Wei J, Lin Y, Chen H. 75.  2012. Gene silencing using the recessive rice bacterial blight resistance gene xa13 as a new paradigm in plant breeding. Plant Cell Rep. 31:851–62 [Google Scholar]
  76. Li T, Liu B, Spalding MH, Weeks DP, Yang B. 76.  2012. High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 30:390–92 [Google Scholar]
  77. Li ZM, Palmer WM, Martin AP, Wang RQ, Rainsford F. 77.  et al. 2012. High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit. J. Exp. Bot. 63:1155–66 [Google Scholar]
  78. Liu YH, Offler CE, Ruan Y-L. 78.  2013. Regulation of fruit and seed response to heat and drought by sugars as nutrients and signals. Front. Plant Sci. 4:282 [Google Scholar]
  79. Lou Y, Gou JY, Xue HW. 79.  2007. PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar mediated root growth. Plant Cell 19:163–81 [Google Scholar]
  80. Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R. 80.  et al. 2006. Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem. J. 397:139–48 [Google Scholar]
  81. Martin MV, Fiol DF, Sundaresan V, Zabaleta EJ, Pagnussata DC. 81.  2013. oiwa, a female gametophytic mutant impaired in a mitochondrial manganese-superoxide dismutase, reveals crucial roles for reactive oxygen species during embryo sac development and fertilization in Arabidopsis. Plant Cell 25:1573–91 [Google Scholar]
  82. Masuda H, Takahashi T, Sugawara S. 82.  1987. The occurrence and properties of alkaline invertase in mature roots of sugar beets. Agric. Biol. Chem. 51:2309–14 [Google Scholar]
  83. McLaughlin JE, Boyer JS. 83.  2004. Glucose localization in maize ovaries when kernel number decreases at low water potential and sucrose is fed to the stems. Ann. Bot. 94:75–86 [Google Scholar]
  84. McLaughlin JE, Boyer JS. 84.  2004. Sugar-responsive gene expression, invertase activity, and senescence in aborting maize ovaries at low water potentials. Ann. Bot. 94:675–89 [Google Scholar]
  85. Micallef BJ, Haskins KA, Vanderveer PJ, Roh KS, Shewmaker CK. 85.  et al. 1995. Altered photosynthesis, flowering, and fruiting in transgenic tomato plants that have an increased capacity for sucrose synthesis. Planta 196:327–34 [Google Scholar]
  86. Mishra BS, Singh M, Aggrawal P, Laxmi A. 86.  2009. Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS ONE 4:e4502 [Google Scholar]
  87. Mudgil Y, Uhrig JF, Zhou J, Temple B, Jiang K. 87.  et al. 2009. Arabidopsis N-MYC DOWNREGULATED-LIKE1, a positive regulator of auxin transport in a G protein–mediated pathway. Plant Cell 21:3591–609 [Google Scholar]
  88. Muller B, Pantin F, Génard M, Turc O, Freixes S. 88.  et al. 2011. Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J. Exp. Bot. 62:1715–29 [Google Scholar]
  89. Murayama S, Handa H. 89.  2007. Genes for alkaline/neutral invertase in rice: Alkaline/neutral invertases are located in plant mitochondria and also in plastids. Planta 225:1193–203 [Google Scholar]
  90. Nägele T, Stutz S, Hörmiller II, Heyer AG. 90.  2012. Identification of a metabolic bottleneck for cold acclimation in Arabidopsis thaliana. Plant J. 72:102–14 [Google Scholar]
  91. Nunes C, O'Hara LE, Primavesi LF, Delatte TL, Schluepmann H. 91.  et al. 2013. The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol. 162:1720–32 [Google Scholar]
  92. O'Hara LE, Paul MJ, Wingler A. 92.  2013. How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol. Plant 6:261–74 [Google Scholar]
  93. Oliver SN, Dennis ES, Dolferus R. 93.  2007. ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant Cell Physiol. 48:1319–30 [Google Scholar]
  94. Patrick JW. 94.  1997. Phloem unloading: sieve element unloading and post-sieve element transport. Annu. Rev. Plant Physiol. Plant Mol. Biol. 148:191–222 [Google Scholar]
  95. Patrick JW, Botha FC, Birch RG. 95.  2013. Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnol. J. 11:142–56 [Google Scholar]
  96. Paul MJ, Primavesi LF, Jhurreea D, Zhang Y. 96.  2008. Trehalose metabolism and signaling. Annu. Rev. Plant Biol. 59:417–41 [Google Scholar]
  97. Pelleschi S, Rocher JP, Prioul JL. 97.  1997. Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant Cell Environ. 20:493–503 [Google Scholar]
  98. Pfeffer PE, Douds DD Jr, Bécard G, Shachar-Hill Y. 98.  1999. Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 120:587–98 [Google Scholar]
  99. Pien S, Wyrzykowska J, Fleming AJ. 99.  2001. Novel marker genes for early leaf development indicate spatial regulation of carbohydrate metabolism within the apical meristem. Plant J. 25:663–74 [Google Scholar]
  100. Pressey R. 100.  1966. Separation and properties of potato invertase and invertase inhibitor. Arch. Biochem. Biophys. 113:667–74 [Google Scholar]
  101. Pressman E, Peet MM, Pharr DM. 101.  2002. The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in developing anthers. Ann. Bot. 90:631–36 [Google Scholar]
  102. Pugh DA, Offler CE, Talbot MJ, Ruan Y-L. 102.  2010. Evidence for the role of transfer cells in the evolutionary increase of seed and fiber biomass yield in cotton. Mol. Plant 3:1075–86 [Google Scholar]
  103. Rausch T, Greiner S. 103.  2004. Plant protein inhibitors of invertases. Biochim. Biophys. Acta 1696:253–61 [Google Scholar]
  104. Reinhold H, Soyk S, Šimková K, Hostettler C, Marafino J. 104.  et al. 2011. β-Amylase-like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell 23:1391–403 [Google Scholar]
  105. Roitsch T, González MC. 105.  2004. Function and regulation of plant invertases: sweet sensations. Trends Plant Sci. 9:606–13 [Google Scholar]
  106. Rolland F, Baena-Gonzalez E, Sheen J. 106.  2006. Sugar sensing and signalling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57:675–709 [Google Scholar]
  107. Rothstein SJ. 107.  2007. Returning to our roots: making plant biology research relevant to future challenges in agriculture. Plant Cell 19:2695–99 [Google Scholar]
  108. Ruan Y-L. 108.  1993. Fruit set, young fruit and leaf growth of Citrus unshiu in relation to assimilate supply. Sci. Hortic. 53:99–107 [Google Scholar]
  109. Ruan Y-L. 109.  2007. Rapid cell expansion and cellulose synthesis regulated by plasmodesmata and sugar: insights from the single-celled cotton fibre. Funct. Plant Biol. 34:1–10 [Google Scholar]
  110. Ruan Y-L, Jin Y, Yang YJ, Li GJ, Boyer JS. 110.  2010. Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol. Plant 3:942–55 [Google Scholar]
  111. Ruan Y-L, Llewellyn DJ, Furbank RT. 111.  2001. The control of single-celled cotton fibre elongation by developmentally reversible gating of plasmodesmata and coordinated expression of sucrose and K+ transporters and expansin. Plant Cell 13:47–63 [Google Scholar]
  112. Ruan Y-L, Llewellyn DJ, Furbank RT. 112.  2003. Suppression of sucrose synthase expression represses cotton fibre cell initiation, elongation and seed development. Plant Cell 15:952–64 [Google Scholar]
  113. Ruan Y-L, Llewellyn DJ, Furbank RT, Chourey PS. 113.  2005. The delayed initiation and slow elongation of fuzz-like short fibre cells in relation to altered patterns of sucrose synthase expression and plasmodesmata gating in a lintless mutant of cotton. J. Exp. Bot. 56:977–84 [Google Scholar]
  114. Ruan Y-L, Llewellyn DJ, Liu Q, Xu SM, Wu LM. 114.  et al. 2008. Expression of sucrose synthase in the developing endosperm is essential for early seed development in cotton. Funct. Plant Biol. 35:382–93 [Google Scholar]
  115. Ruan Y-L, Patrick JW. 115.  1995. The cellular pathway of postphloem sugar transport in developing tomato fruit. Planta 196:434–44 [Google Scholar]
  116. Ruan Y-L, Patrick JW, Bouzayen M, Osorio S, Fernie AR. 116.  2012. Molecular regulation of seed and fruit set. Trends Plant Sci. 17:656–65 [Google Scholar]
  117. Ruhlmann JM, Kram BW, Carter CJ. 117.  2010. CELL WALL INVERTASE 4 is required for nectar production in Arabidopsis. J. Exp. Bot. 61:395–404 [Google Scholar]
  118. Saini HS, Westgate ME. 118.  2000. Reproductive development in grain crops during drought. Adv. Agron. 68:59–96 [Google Scholar]
  119. Sairanen I, Novák O, Pěnčík A, Ikeda Y, Jones B. 119.  et al. 2012. Soluble carbohydrates regulate auxin biosynthesis via PIF proteins in Arabidopsis. Plant Cell 24:4907–16 [Google Scholar]
  120. Salzer P, Hager A. 120.  1991. Sucrose utilization of the ectomycorrhizal fungi Amanita muscaria and Hebeloma crustuliniforme depends on the cell wall-bound invertase activity of their host Picea abies. Bot. Acta 104:439–45 [Google Scholar]
  121. Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D. 121.  2006. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441:227–30 [Google Scholar]
  122. Schaarschmidt S, González MC, Roitsch T, Strack D, Sonnewald U. 122.  et al. 2007. Regulation of arbuscular mycorrhization by carbon. The symbiotic interaction cannot be improved by increased carbon availability accomplished by root-specifically enhanced invertase activity. Plant Physiol. 143:1827–40 [Google Scholar]
  123. Schaarschmidt S, Roitsch T, Hause B. 123.  2006. Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J. Exp. Bot. 57:4015–23 [Google Scholar]
  124. Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ. 124.  et al. 2013. Using membrane transporters to improve crops for sustainable food production. Nature 497:60–66 [Google Scholar]
  125. Schwimmer S, Makower RU, Rorem ES. 125.  1961. Invertase and invertase inhibitor in potato. Plant Physiol. 36:313–16 [Google Scholar]
  126. Sergeeva LI, Keurentjes JJ, Bentsink L, Vonk J, van der Plas LH. 126.  et al. 2006. Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. Proc. Natl. Acad. Sci. USA 103:2994–99 [Google Scholar]
  127. Sheoran IS, Saini HS. 127.  1996. Drought-induced sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex. Plant Reprod. 9:161–69 [Google Scholar]
  128. Slewinski TL. 128.  2011. Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol. Plant 4:641–62 [Google Scholar]
  129. Smeekens S, Ma J, Hanson J, Rolland F. 129.  2010. Sugar signals and molecular networks controlling plant growth. Curr. Opin. Plant Biol. 13:273–78 [Google Scholar]
  130. Smidansky ED, Clancy M, Meyer FD, Lanning SP, Blake NK. 130.  et al. 2002. Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc. Natl. Acad. Sci. USA 99:1724–29 [Google Scholar]
  131. Smith SE, Smith FA. 131.  2011. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62:227–50 [Google Scholar]
  132. Sonnewald U, Hajirezaei MR, Kossmann J, Heyer A, Trethewey RN. 132.  et al. 1997. Increased potato tuber size resulting from apoplastic expression of a yeast invertase. Nat. Biotechnol. 15:794–97 [Google Scholar]
  133. Stitt M. 133.  2013. Progress in understanding and engineering primary plant metabolism. Curr. Opin. Biotechnol. 24:229–38 [Google Scholar]
  134. Sturm A. 134.  1999. Invertases: primary structures, functions and roles in plant development and sucrose partitioning. Plant Physiol 121:1–7 [Google Scholar]
  135. Sun L, Yang DL, Kong Y, Chen Y, Li XZ. 135.  et al. 2014. Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defence in rice. Mol. Plant Pathol 15:161–73 [Google Scholar]
  136. Sutton PN, Gilbert MJ, Williams LE, Hall JL. 136.  2007. Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol. Plant 129:787–95 [Google Scholar]
  137. Sutton PN, Henry MJ, Hall JL. 137.  1999. Glucose, and not sucrose, is transported from wheat to wheat powdery mildew. Planta 208:426–30 [Google Scholar]
  138. Tang GQ, Luscher M, Sturm A. 138.  1999. Antisense repression and vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11:177–89 [Google Scholar]
  139. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y. 139.  et al. 2002. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–213 [Google Scholar]
  140. Urano D, Phan N, Jones JC, Yang J, Huang J. 140.  et al. 2012. Endocytosis of the seven-transmembrane RGS1 protein activates G-protein-coupled signalling in Arabidopsis. Nat. Cell Biol. 14:1079–88 [Google Scholar]
  141. Voegele RT, Struck C, Hahn M, Mendgen K. 141.  2001. The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc. Natl. Acad. Sci. USA 98:8133–38 [Google Scholar]
  142. Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T. 142.  et al. 2013. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–7 [Google Scholar]
  143. Wang E, Wang J, Zhu X, Hao W, Wang L. 143.  et al. 2008. Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat. Genet. 40:1370–74 [Google Scholar]
  144. Wang E, Xu X, Zhang L, Zhang H, Lin L. 144.  et al. 2010. Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication. BMC Evol. Biol. 10:108 [Google Scholar]
  145. Wang JW, Czech B, Weigel D. 145.  2009. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–49 [Google Scholar]
  146. Wang L, Li XR, Lian H, Ni DA, He YK. 146.  et al. 2010. Evidence that high activity of vacuolar invertase is required for cotton fiber and Arabidopsis root elongation through osmotic dependent and independent pathways, respectively. Plant Physiol. 154:744–56 [Google Scholar]
  147. Wang L, Ruan Y-L. 147.  2012. New insights into roles of cell wall invertase in early seed development revealed by comprehensive spatial and temporal expression patterns of GhCWIN1 in cotton. Plant Physiol. 160:777–87 [Google Scholar]
  148. Wang L, Ruan Y-L. 148.  2013. Regulation of cell division and expansion by sugar and auxin signaling. Front. Plant Sci. 4:163 [Google Scholar]
  149. Wang X, Sager R, Cui W, Zhang C, Lu H. 149.  et al. 2013. Salicylic acid regulates plasmodesmata closure during innate immune responses in Arabidopsis. Plant Cell 25:2315–29 [Google Scholar]
  150. Weber H, Borisjuk L, Heim U, Wobus U. 150.  1997. Sugar import and metabolism during seed development. Trends Plant Sci. 2:169–74 [Google Scholar]
  151. Weber H, Borisjuk L, Wobus U. 151.  1996. Controlling seed development and seed size in Vicia faba: a role for seed coat-associated invertases and carbohydrate state. Plant J. 10:823–34 [Google Scholar]
  152. Weber H, Borisjuk L, Wobus U. 152.  2005. Molecular physiology of legume seed development. Annu. Rev. Plant Biol. 56:253–79 [Google Scholar]
  153. Welham T, Pike J, Horst I, Flemetakis E, Katinakis P. 153.  et al. 2009. A cytosolic invertase is required for normal growth and cell development in the model legume, Lotus japonicus. J. Exp. Bot. 60:3353–65 [Google Scholar]
  154. Wingenter K, Schulz A, Wormit A, Wic S, Trentmann O. 154.  et al. 2010. Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitioning, sugar signaling, and seed yield in Arabidopsis. Plant Physiol. 154:665–77 [Google Scholar]
  155. Wirth J, Poletti S, Aeschlimann B, Yakandawala N, Drosse B. 155.  et al. 2009. Rice endosperm iron biofortification by targeted and synergistic action of nicotianamine synthase and ferritin. Plant Biotechnol. J. 7:631–44 [Google Scholar]
  156. Xiang L, Le Roy K, Bolouri-Moghaddam M-R, Vanhaecke M, Lammens W. 156.  et al. 2011. Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana. J. Exp. Bot. 62:3849–62 [Google Scholar]
  157. Xiong Y, McCormack M, Li L, Hall Q, Xiang C. 157.  et al. 2013. Glucose–TOR signalling reprograms the transcriptome and activates meristems. Nature 496:181–87 [Google Scholar]
  158. Xu SM, Brill E, Llewellyn DJ, Furbank RT, Ruan Y-L. 158.  2012. Overexpression of a potato sucrose synthase gene in cotton accelerates leaf expansion, reduces seed abortion, and enhances fiber production. Mol. Plant 5:430–41 [Google Scholar]
  159. Yang L, Xu M, Koo Y, He J, Poethig RS. 159.  2013. Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. eLife 2:e00260 [Google Scholar]
  160. Yu S, Cao L, Zhou CM, Zhang TQ, Lian H. 160.  et al. 2013. Sugar is an endogenous cue for juvenile-to-adult phase transition in plants. eLife 2:e00269 [Google Scholar]
  161. Zanor MI, Osorio S, Nunes-Nesi A, Carrarib F, Lohse M. 161.  et al. 2009. RNA interference of LIN5 in Solanum lycopersicum confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiol. 150:1204–18 [Google Scholar]
  162. Zinselmeier C, Jeong BR, Boyer JS. 162.  1999. Starch and the control of kernel number in maize at low water potentials. Plant Physiol. 121:25–35 [Google Scholar]
  163. Zrenner R, Salanoubat M, Willimitzer L, Sonnewald U. 163.  1995. Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J. 7:97–107 [Google Scholar]
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