SUGAR SENSING AND SIGNALING

Supported by the NSF IBN Program and the NIH

Summary

Our laboratory has been interested in elucidating the molecular mechanisms underlying sugar functions as central signaling molecules in controlling physiology, metabolism, cell cycle, development, and gene expression in plants. Using Arabidopsis thaliana as a model plant, we are elucidating the molecular basis of sugar responses that influence many vital processes in the plant life cycle from germination, root and leaf development, flowering, embryogenesis, to senescence. Using a combination of molecular, cellular, biochemical, genetic and genomic approaches, we have first demonstrated that sugars trigger a global repression of photosynthesis gene transcription in plants. We have further shown that some sugar signals are mediated through the sugar sensor hexokinase (HXK), which has dual functions as an enzyme and as a signal transmitter. Transgenic Arabidopsis plants with altered HXK levels exhibit either sugar insensitivity or hypersensitivity based on the analysis of diverse gene expression and glucose-induced developmental arrest. Recent analysis of two null AtHXK1 mutants has provided further genetic evidence that HXK is the sugar sensor mediating a wide spectrum of sugar signaling pathways that control photosynthesis, gene expression, leaf and root development, and senescence in plants. The manipulation of plant sugar sensors may offer new opportunities to control plant growth and production relevant to agricultural and environmental needs.

We are currently studying the molecular basis of HXK function as a sugar sensor in a protein complex that may be uncoupled from the conventional role of HXK as a cytosolic and metabolic enzyme in glycolysis. We are also establishing the genetic pathways that control plant sugar sensing and signaling based on genetic, phenotypical, and molecular analyses of the glucose insensitive (gin) and glucose over-sensitive (glo) mutants. The characterization of corresponding genes has revealed surprising and exciting complexity of the sugar signal transduction pathways that are connected to multiple hormonal and stress signaling pathways in plants.

Signaling Pathway Illustrations

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Education powerpoint file

ASPB talk: Sugar signalling

Review

Emerging connections in the ethylene-signaling network. Trends in Plant Science. 14: 270-279.PDF

Baena-González, E., Rolland, F., and Sheen, J. 2008. KIN10/11 are master regulators of the convergent stress transcriptome. In: Photosynthesis. Energy from the Sun: 14th International Congress on Photosynthesis (J.F. Allen, E. Gantt, J.H. Golbeck & B. Osmond, eds.), Springer, New York, NY, pp. 1337-1344. PDF

Baena-González, E., and Sheen, J. 2008. Convergent energy and stress signaling. Trends in Plant Science 13: 474-482  PDF

Ramon, M., Rolland, F., and Sheen, J. October 22, 2008 Sugar Sensing and Signaling. The Arabidopsis Book (TAB), ISSN: 1543-8120   http://www.aspb.org/publications/arabidopsis/   pages 1-22 PDF

Müller, B. and Sheen, J. 2007. Advances in Cytokinin Signaling. Science 318:68-69 PDF

Yoo, S.-D., Cho, Y.-H., and Sheen, J. 2007. Arabidopsis Mesophyll Protoplasts: A Versitile Cell System for Transient Gene Expression Analysis. Nature Protocols 2:1565-1572 PDF

Rolland, F., Baena-González, E., and Sheen, J. 2006. Sugar Sensing and Signaling in Plants: Conserved and Novel Mechanisms. Annual Review of Plant Biology Volume 57: 676-709. PDF

Rolland, F., Sheen J. 2005. Sugar Sensing and and Signalling Networks in Plants. Biochemical Society: 269-271 PDF

Rolland, F., Moore, D.B., and Sheen, J. 2002. Sugar Sensing and Signaling in Plants. Plant Cell 14 (suppl): S185-S205

Sheen, J., Zhou, L., and Jang, J.-C. 1999. Sugar as a signaling molecule. Curr. Opin. Plant Biol. 2:410-418.

Moore, D.B. and Sheen, J. 1999. Plant sugar sensing and signaling-a complex reality. Trends in Plant Science 4:250.

Jang, J.-C. and Sheen, J. 1997. Sugar sensing in higher plants. Trends in Plant Science 2: 208-214.

Sheen, J. 1994. Feedback control of gene expression. Photosynth. Res. 39: 427-438.

Articles

Cho, Y.H., Sheen, J., and Yoo, S.D. 2010. Low Glucose Uncouples HXK1-dependent Signaling from Stress and Hormone Responses in Arabidopsis.Plant Physiology 152:1180-1182 PDF

Li, J.F., Li, L. and Sheen, J. 2010. An economical and rapid DNA purification protocol serving multi-purpose DNA extraction needs in plant research.Plant Methods 6:1-8 PDF

Cho, J-I., Ryoo, N., Eom, J-S., Lee, D-W., Kim, H-B., Jeong, S-W., Lee, Y-H., Kwon, Y-K., Cho, M-H., Bhoo, S-H., Hahn, T-R., Park, Y-I., Hwang, I., Sheen, J. and Jeon, J-S. 2009. Role of the Rice Hexokinases OsHXK5 and OsHXK6 as Glucose SensorsPlant Physiology 149: 745-759 PDF

Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.-Y., Cutler, S.R., Sheen, J., Rodriguez, P.L. an Zhu, J.-K. 2009. In vitro reconstitution of an abscisic acid signaling pathway. Nature. 462: 660-664. PDF SUPP

Müller, B. and Sheen, J. 2008. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453: 1094-1097 PDF  SUPP

Yoo, S-D., Cho Y-H., Tena G., Xiong. Y. and Sheen, J. 2008. Dual control of nuclear EIN3 by bifurcate MAPK cascades in C₂H₄ signalling. Nature 451: 789-795 PDF  SUPP

Karve, A., Rauh, B.L., Xia, X., Kandasamy, M., Meagher, R.B., Sheen, J. and Moore, B.D. 2008. Expression and evolutionary features of the hexokinase gene family in ArabidipsisPlanta 228: 411-425 PDF

Cho, Y.-H., and Yoo, S.-D. 2007. ETHYLENE RESPONSE 1 Histidine Kinase Activity of Arabidopsis Promotes Plant Growth. Plant Physiology 143: 612-616 PDF

Baena-Gonzalez, E., Rolland, F., Thevelein, J.M. and Sheen, J. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938-943 PDF SUPP

Cho, Y.-H., Yoo, S.-D., Sheen, J. 2006. Regulatory Functions of Nuclear Hexokinase1 Complex in Glucose Signaling. Cell 127 579-589 PDF SUPP.

Kim, H.J., Ryu, H., Hong, S.H., Woo, H.R., Lim, P.O., Lee, I.C., Sheen, J., Nam, H.G. and Hwang, I. 2006. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. PNAS 103(3): 814-819 PDF

Yanagisawa, S., Yoo, S.-D., and Sheen, J. 2003. Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. Nature 425 521-525 PDF

Moore, B., Zhou, L.,Rolland, F., Hall, Q., Cheng, W.-H., Liu, Y.-X., Hwang, I., Jones, T., Sheen, J. 2003. Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling. Science 14 332-336 Abstract Full Text SUPP.

Wan-Hsing Cheng, Akira Endo, Li Zhou, Jessica Penney, Huei-Chi Chen, Analilia Arroyo, Patricia Leon, Eiji Nambara, Tadao Asami, Mitsunori Seo, Tomokazu Koshiba, and Jen Sheen 2002. A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions. Plant Cell 14 2723-2743 PDF

Hwang, I. and Sheen, J. 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413(6854):383-9 PDF

Arenas-Huertero, F., Arroyo-Becerra, A., Zhou, L, Sheen, J., and León P, 2000. Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes & Dev. 14: 2085-2096.

Xiao, W., Sheen, J., and Jang, J-C. 2000. Multiple sugar signal transduction pathways in plants, Plant Mol. Biol. 44: 451-461.

Zhou, L., Jang, J.-C., Jones, T. and Sheen, J. 1998. Glucose and ethylene signal transduction cross-talk revealed by an Arabidopsis glucose-insensitve mutant. PNAS 95, 10294-9.

Jang, J.-C. Leon, P., Zhou, L.,Sheen, J. 1997. Hexokinase as a sugar sensor in higher plants. Plant Cell 9: 5-19

Jang, J-C., Sheen, J. 1994. Sugar sensing in higher plants. Plant Cell 6: 1665-1679.

Sheen, J.1990. Metabolic repression of transcription in higher plants. Plant Cell 2: 1027- 1038.