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PLANT CELL 13 (5): 1127-1141

Copyright © 2001 by the American Society of Plant Physiologists.

Plant Cell, Vol. 13, 1127-1141, May 2001, Copyright © 2001, American Society of Plant Physiologists Sucrose Export Defective1 Encodes a Novel Protein Implicated in Chloroplast-to-Nucleus Signaling Laurel Mezitt Provencher, Long Miao, Neelima Sinha, and William J. Lucas Section of Plant Biology, Division of Biological Sciences, University of California, One Shields Avenue, Davis, California 95616 William J. Lucas, wjlucas{at} (E-mail), 530-752-5410 (fax)

The Sucrose export defective1 (Sxd1) gene of maize was cloned and shown to encode a novel protein conserved between plants and cyanobacteria. The structure of the Sxd1 locus was determined in wild-type plants and two independent sxd1 alleles. Expression analysis demonstrated that the gene was transcribed in all green tissues, with highest levels in maturing leaf blades. In situ hybridization studies revealed high levels of Sxd1 mRNA in bundle sheath cells, with lower levels within the mesophyll. The SXD1 protein was localized to chloroplasts, in both bundle sheath and mesophyll cells. Levels of sucrose, glucose, and fructose were compared between wild-type and sxd1 plants. Mutant plants were fully capable of producing sucrose and accumulated all three sugars at concentrations above those measured in wild-type plants. Despite these increased sugar concentrations, photosynthetic gene expression was not significantly downregulated in affected areas of sxd1 leaf blades. These results are consistent with photosynthate being trapped within anthocyanin-accumulating regions of sxd1 leaves due to plasmodesmal occlusion at the bundle sheath–vascular parenchyma boundary of the minor veins. A model for SXD1 function is proposed in which the protein is involved in a chloroplast-to-nucleus signaling pathway necessary for proper late-stage differentiation of maize bundle sheath cells, including the developmentally regulated modification of plasmodesmata.

Increased Expression of a Phloem Membrane Protein Encoded by NHL26 Alters Phloem Export and Sugar Partitioning in Arabidopsis.
F. Vilaine, P. Kerchev, G. Clement, B. Batailler, T. Cayla, L. Bill, L. Gissot, and S. Dinant (2013)
PLANT CELL 25, 1689-1708
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Tie-dyed2 Encodes a Callose Synthase That Functions in Vein Development and Affects Symplastic Trafficking within the Phloem of Maize Leaves.
T. L. Slewinski, R. F. Baker, A. Stubert, and D. M. Braun (2012)
Plant Physiology 160, 1540-1550
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Plasmodesmata formation and cell-to-cell transport are reduced in decreased size exclusion limit 1 during embryogenesis in Arabidopsis.
M. Xu, E. Cho, T. M. Burch-Smith, and P. C. Zambryski (2012)
PNAS 109, 5098-5103
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Redox States of Plastids and Mitochondria Differentially Regulate Intercellular Transport via Plasmodesmata.
S. Stonebloom, J. O. Brunkard, A. C. Cheung, K. Jiang, L. Feldman, and P. Zambryski (2012)
Plant Physiology 158, 190-199
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Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis.
A. Bilska and P. Sowinski (2010)
Ann. Bot. 106, 675-686
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Structural and Metabolic Transitions of C4 Leaf Development and Differentiation Defined by Microscopy and Quantitative Proteomics in Maize.
W. Majeran, G. Friso, L. Ponnala, B. Connolly, M. Huang, E. Reidel, C. Zhang, Y. Asakura, N. H. Bhuiyan, Q. Sun, et al. (2010)
PLANT CELL 22, 3509-3542
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The Psychedelic Genes of Maize Redundantly Promote Carbohydrate Export From Leaves.
T. L. Slewinski and D. M. Braun (2010)
Genetics 185, 221-232
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Tocochromanol functions in plants: antioxidation and beyond.
J. Falk and S. Munne-Bosch (2010)
J. Exp. Bot. 61, 1549-1566
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Replacement of {alpha}-Tocopherol by {beta}-Tocopherol Enhances Resistance to Photooxidative Stress in a Xanthophyll-Deficient Strain of Chlamydomonas reinhardtii.
A. Sirikhachornkit, J. W. Shin, I. Baroli, and K. K. Niyogi (2009)
Eukaryot. Cell 8, 1648-1657
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Loss of the plant DEAD-box protein ISE1 leads to defective mitochondria and increased cell-to-cell transport via plasmodesmata.
S. Stonebloom, T. Burch-Smith, I. Kim, D. Meinke, M. Mindrinos, and P. Zambryski (2009)
PNAS 106, 17229-17234
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Genetic Control of Carbon Partitioning in Grasses: Roles of Sucrose Transporters and Tie-dyed Loci in Phloem Loading.
D. M. Braun and T. L. Slewinski (2009)
Plant Physiology 149, 71-81
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Tie-dyed1 Encodes a Novel, Phloem-Expressed Transmembrane Protein That Functions in Carbohydrate Partitioning.
Y. Ma, T. L. Slewinski, R. F. Baker, and D. M. Braun (2009)
Plant Physiology 149, 181-194
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Tie-dyed2 Functions with Tie-dyed1 to Promote Carbohydrate Export from Maize Leaves.
R. F. Baker and D. M. Braun (2008)
Plant Physiology 146, 1085-1097
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Tocopherols Modulate Extraplastidic Polyunsaturated Fatty Acid Metabolism in Arabidopsis at Low Temperature.
H. Maeda, T. L. Sage, G. Isaac, R. Welti, and D. DellaPenna (2008)
PLANT CELL 20, 452-470
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Specific Roles of {alpha}- and {gamma}-Tocopherol in Abiotic Stress Responses of Transgenic Tobacco.
A.-R. Abbasi, M. Hajirezaei, D. Hofius, U. Sonnewald, and L. M. Voll (2007)
Plant Physiology 143, 1720-1738
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tie-dyed1 Regulates Carbohydrate Accumulation in Maize Leaves.
D. M. Braun, Y. Ma, N. Inada, M. G. Muszynski, and R. F. Baker (2006)
Plant Physiology 142, 1511-1522
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Tocopherols Play a Crucial Role in Low-Temperature Adaptation and Phloem Loading in Arabidopsis.
H. Maeda, W. Song, T. L. Sage, and D. DellaPenna (2006)
PLANT CELL 18, 2710-2732
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{alpha}-Tocopherol Plays a Role in Photosynthesis and Macronutrient Homeostasis of the Cyanobacterium Synechocystis sp. PCC 6803 That Is Independent of Its Antioxidant Function.
Y. Sakuragi, H. Maeda, D. DellaPenna, and D. A. Bryant (2006)
Plant Physiology 141, 508-521
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Tocopherol Cyclase (VTE1) Localization and Vitamin E Accumulation in Chloroplast Plastoglobule Lipoprotein Particles.
P.-A. Vidi, M. Kanwischer, S. Baginsky, J. R. Austin, G. Csucs, P. Dormann, F. Kessler, and C. Brehelin (2006)
J. Biol. Chem. 281, 11225-11234
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Alterations in Tocopherol Cyclase Activity in Transgenic and Mutant Plants of Arabidopsis Affect Tocopherol Content, Tocopherol Composition, and Oxidative Stress.
M. Kanwischer, S. Porfirova, E. Bergmuller, and P. Dormann (2005)
Plant Physiology 137, 713-723
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RNAi-Mediated Tocopherol Deficiency Impairs Photoassimilate Export in Transgenic Potato Plants.
D. Hofius, M.-R. Hajirezaei, M. Geiger, H. Tschiersch, M. Melzer, and U. Sonnewald (2004)
Plant Physiology 135, 1256-1268
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Vitamin E Is Essential for Seed Longevity and for Preventing Lipid Peroxidation during Germination.
S. E. Sattler, L. U. Gilliland, M. Magallanes-Lundback, M. Pollard, and D. DellaPenna (2004)
PLANT CELL 16, 1419-1432
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Engineering Vitamin E Content: From Arabidopsis Mutant to Soy Oil.
A. L. Van Eenennaam, K. Lincoln, T. P. Durrett, H. E. Valentin, C. K. Shewmaker, G. M. Thorne, J. Jiang, S. R. Baszis, C. K. Levering, E. D. Aasen, et al. (2003)
PLANT CELL 15, 3007-3019
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Vitamin E-Defective Mutants of Arabidopsis Tell Tales of Convergent Evolution.
N. A. Eckardt (2003)
PLANT CELL 15, 2233-2235
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Characterization of Tocopherol Cyclases from Higher Plants and Cyanobacteria. Evolutionary Implications for Tocopherol Synthesis and Function.
S. E. Sattler, E. B. Cahoon, S. J. Coughlan, and D. DellaPenna (2003)
Plant Physiology 132, 2184-2195
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Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis.
S. Porfirova, E. Bergmuller, S. Tropf, R. Lemke, and P. Dormann (2002)
PNAS 99, 12495-12500
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Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana.
I. Kim, F. D. Hempel, K. Sha, J. Pfluger, and P. C. Zambryski (2002)
Development 129, 1261-1272
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