The starch granule-associated protein EARLY STARVATION1 is required for the control of starch degradation in Arabidopsis thaliana leaves

Plant Cell

Volumn 28, Issue 6, 2016, Pages 1472-1489

  Feike, Doreen ^a   Seung, David ^b   Graf, Alexander ^a,c   Bischof, Sylvain ^b,d   Ellick, Tamaryn ^b   Coiro, Mario ^b   Soyk, Sebastian ^b,e   Eicke, Simona ^b   Mettler Altmann, Tabea ^b,f   Lu, Kuan Jen ^b   Trick, Martin ^a   Zeeman, Samuel C ^b   Smith, Alison M ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b ETH ZURICH   (Switzerland)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Simons Center for Quantitative Biology   (United States)

^f HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; STARCH;

ARABIDOPSIS; CHLOROPLAST; GENETICS; METABOLISM; MUTATION; PLANT LEAF; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; MUTATION; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; STARCH;

EID: 84978137603     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.16.00011     Document Type: Article

References (77)

1. Andriotis, V.M., Pike, M.J., Kular, B., Rawsthorne, S., and Smith, A.M. (2010). Starch turnover in developing oilseed embryos. New Phytol. 187: 791-804.
2. Baunsgaard, L., Lütken, H., Mikkelsen, R., Glaring, M.A., Pham, T.T., and Blennow, A. (2005). A novel isoform of glucan, water dikinase phosphorylates pre-phosphorylated alpha-glucans and is involved in starch degradation in Arabidopsis. Plant J. 41: 595-605.
3. Bayer, R.G., Stael, S., Csaszar, E., and Teige, M. (2011). Mining the soluble chloroplast proteome by affinity chromatography. Proteomics 11: 1287-1299.
4. Bläsing, O.E., Gibon, Y., Günther, M., Höhne, M., Morcuende, R., Osuna, D., Thimm, O., Usadel, B., Scheible, W.R., and Stitt, M. (2005). Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 17: 3257-3281.
5. Blennow, A., and Engelsen, S.B. (2010). Helix-breaking news: fighting crystalline starch energy deposits in the cell. Trends Plant Sci. 15: 236-240.
6. Caspar, T., Huber, S.C., and Somerville, C. (1985). Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol. 79: 11-17.
7. Caspar, T., Lin, T.-P., Kakefuda, G., Benbow, L., Preiss, J., and Somerville, C. (1991). Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol. 95: 1181-1188.
8. Chatterton, N.J., and Silvius, J.E. (1981). Photosynthate partitioning into starch in soybean leaves. II. Irradiance level and daily photosynthetic period duration effects. Plant Physiol. 67: 257-260.
9. Chia, T., Thorneycroft, D., Chapple, A., Messerli, G., Chen, J., Zeeman, S.C., Smith, S.M., and Smith, A.M. (2004). A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J. 37: 853-863.
10. Christiansen, C., Abou Hachem, M., Janeček, S., Viksø-Nielsen, A., Blennow, A., and Svensson, B. (2009). The carbohydratebinding module family 20--diversity, structure, and function. FEBS J. 276: 5006-5029.
11. Cockburn, D., Wilkens, C., Ruzanski, C., Andersen, S., Nielsen, J.W., Smith, A.M., Field, R.A., Willemöes, M., Hachem, M.A., and Svensson, B. (2013). Analysis of surface binding sites (SBSs) in carbohydrate active enzymes with focus on glycoside hydrolase families 13 and 77: a mini-review. Biologia 69: 705-712.
12. Comparot-Moss, S., et al. (2010). A putative phosphatase, LSF1, is required for normal starch turnover in Arabidopsis leaves. Plant Physiol. 152: 685-697.
13. Corbesier, L., Lejeune, P., and Bernier, G. (1998). The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant. Planta 206: 131-137.
14. Critchley, J.H., Zeeman, S.C., Takaha, T., Smith, A.M., and Smith, S.M. (2001). A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J. 26: 89-100.
15. Crumpton-Taylor, M., Grandison, S., Png, K.M.Y., Bushby, A.J., and Smith, A.M. (2012). Control of starch granule numbers in Arabidopsis chloroplasts. Plant Physiol. 158: 905-916.
16. Crumpton-Taylor, M., Pike, M., Lu, K.J., Hylton, C.M., Feil, R., Eicke, S., Lunn, J.E., Zeeman, S.C., and Smith, A.M. (2013). Starch synthase 4 is essential for coordination of starch granule formation with chloroplast division during Arabidopsis leaf expansion. New Phytol. 200: 1064-1075.
17. Delatte, T., Trevisan, M., Parker, M.L., and Zeeman, S.C. (2005). Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant J. 41: 815-830.
18. Denyer, K., Sidebottom, C., Hylton, C.M., and Smith, A.M. (1993). Soluble isoforms of starch synthase and starch-branching enzyme also occur within starch granules in developing pea embryos. Plant J. 4: 191-198.
19. Eimert, K., Wang, S.M., Lue, W.I., and Chen, J. (1995). Monogenic recessive mutations causing both late floral initiation and excess starch accumulation in Arabidopsis. Plant Cell 7: 1703-1712.
20. Fujihira, K., Kurata, T., Watahiki, M.K., Karahara, I., and Yamamoto, K.T. (2000). An agravitropic mutant of Arabidopsis, endodermal-amyloplast less 1, that lacks amyloplasts in hypocotyl endodermal cell layer. Plant Cell Physiol. 41: 1193-1199.
21. Fulton, D.C., et al. (2008). β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040-1058.
22. Gibon, Y., Bläsing, O.E., Palacios-Rojas, N., Pankovic, D., Hendriks, J.H.M., Fisahn, J., Höhne, M., Günther, M., and Stitt, M. (2004). Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADPglucose pyrophosphorylase in the following light period. Plant J. 39: 847-862.
23. Gibon, Y., Pyl, E.T., Sulpice, R., Lunn, J.E., Höhne, M., Günther, M., and Stitt, M. (2009). Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ. 32: 859-874.
24. Gibon, Y., Usadel, B., Blaesing, O.E., Kamlage, B., Hoehne, M., Trethewey, R., and Stitt, M. (2006). Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol. 7: R76.
25. Glaring, M.A., Baumann, M.J., Abou Hachem, M., Nakai, H., Nakai, N., Santelia, D., Sigurskjold, B.W., Zeeman, S.C., Blennow, A., and Svensson, B. (2011). Starch-binding domains in the CBM45 family-low-affinity domains from glucan, water dikinase and α-amylase involved in plastidial starch metabolism. FEBS J. 278: 1175-1185.
26. Graf, A., Schlereth, A., Stitt, M., and Smith, A.M. (2010). Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc. Natl. Acad. Sci. USA 107: 9458-9463.
27. Grimaud, F., Rogniaux, H., James, M.G., Myers, A.M., and Planchot, V. (2008). Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis. J. Exp. Bot. 59: 3395-3406.
28. Hanson, K.R., and McHale, N.A. (1988). A starchless mutant of Nicotiana sylvestris containing a modified plastid phosphoglucomutase. Plant Physiol. 88: 838-844.
29. Hejazi, M., Fettke, J., Haebel, S., Edner, C., Paris, O., Frohberg, C., Steup, M., and Ritte, G. (2008). Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilization. Plant J. 55: 323-334.
30. Hejazi, M., Fettke, J., Paris, O., and Steup, M. (2009). The two plastidial starch-related dikinases sequentially phosphorylate glucosyl residues at the surface of both the A- and B-type allomorphs of crystallized maltodextrins but the mode of action differs. Plant Physiol. 150: 962-976.
31. Hejazi, M., Fettke, J., Kötting, O., Zeeman, S.C., and Steup, M. (2010). The Laforin-like dual-specificity phosphatase SEX4 from Arabidopsis hydrolyzes both C6- and C3-phosphate esters introduced by starch-related dikinases and thereby affects phase transition of alpha-glucans. Plant Physiol. 152: 711-722.
32. Hou, X., Li, L., Peng, Z., Wei, B., Tang, S., Ding, M., Liu, J., Zhang, F., Zhao, Y., Gu, H., and Qu, L.-J. (2010). A platform of highdensity INDEL/CAPS markers for map-based cloning in Arabidopsis. Plant J. 63: 880-888.
33. Johnson, M.T.J., et al. (2012). Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS One 7: e50226.
34. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
35. Karpowicz, S.J., Prochnik, S.E., Grossman, A.R., and Merchant, S.S. (2011). The GreenCut2 resource, a phylogenomically derived inventory of proteins specific to the plant lineage. J. Biol. Chem. 286: 21427-21439.
36. Katoh, K., and Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30: 772-780.
37. Kleffmann, T., Russenberger, D., von Zychlinski, A., Christopher, W., Sjölander, K., Gruissem, W., and Baginsky, S. (2004). The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 14: 354-362.
38. Kötting, O., Pusch, K., Tiessen, A., Geigenberger, P., Steup, M., and Ritte, G. (2005). Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 137: 242-252.
39. Kötting, O., Santelia, D., Edner, C., Eicke, S., Marthaler, T., Gentry, M.S., Comparot-Moss, S., Chen, J., Smith, A.M., Steup, M., Ritte, G., and Zeeman, S.C. (2009). STARCH-EXCESS4 is a laforinlike Phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21: 334-346.
40. Li, H., Ruan, J., and Durbin, R. (2008). Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18: 1851-1858.
41. Lin, T.P., Caspar, T., Somerville, C., and Preiss, J. (1988). Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L.) Heynh, lacking ADPglucose pyrophosphorylase activity. Plant Physiol. 86: 1131-1135.
42. Lu, Y., Gehan, J.P., and Sharkey, T.D. (2005). Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol. 138: 2280-2291.
43. Martinis, J., Glauser, G., Valimareanu, S., Stettler, M., Zeeman, S.C., Yamamoto, H., Shikanai, T., and Kessler, F. (2014). ABC1K1/PGR6 kinase: a regulatory link between photosynthetic activity and chloroplast metabolism. Plant J. 77: 269-283.
44. Meekins, D.A., Guo, H.F., Husodo, S., Paasch, B.C., Bridges, T.M., Santelia, D., Kötting, O., Vander Kooi, C.W., and Gentry, M.S. (2013). Structure of the Arabidopsis glucan phosphatase LIKE SEX FOUR2 reveals a unique mechanism for starch dephosphorylation. Plant Cell 25: 2302-2314.
45. Meekins, D.A., Raththagala, M., Husodo, S., White, C.J., Guo, H.F., Kötting, O., Vander Kooi, C.W., and Gentry, M.S. (2014). Phosphoglucan-bound structure of starch phosphatase Starch Excess4 reveals the mechanism for C6 specificity. Proc. Natl. Acad. Sci. USA 111: 7272-7277.
46. Mu-Forster, C., Huang, R., Powers, J.R., Harriman, R.W., Knight, M., Singletary, G.W., Keeling, P.L., and Wasserman, B.P. (1996). Physical association of starch biosynthetic enzymes with starch granules of maize endosperm. Granule-associated forms of starch synthase I and starch branching enzyme II. Plant Physiol. 111: 821-829.
47. Mugford, S.T., Fernandez, O., Brinton, J., Flis, A., Krohn, N., Encke, B., Feil, R., Sulpice, R., Lunn, J.E., Stitt, M., and Smith, A.M. (2014). Regulatory properties of ADP glucose pyrophosphorylase are required for adjustment of leaf starch synthesis in different photoperiods. Plant Physiol. 166: 1733-1747.
48. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37: D987-D991.
49. Osuna, D., Usadel, B., Morcuende, R., Gibon, Y., Bläsing, O.E., Höhne, M., Günter, M., Kamlage, B., Trethewey, R., Scheible, W.R., and Stitt, M. (2007). Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbondeprived Arabidopsis seedlings. Plant J. 49: 463-491.
50. Palopoli, N., Busi, M.V., Fornasari, M.S., Gomez-Casati, D., Ugalde, R., and Parisi, G. (2006). Starch-synthase III family encodes a tandem of three starch-binding domains. Proteins 65: 27-31.
51. Peltier, J.B., Cai, Y., Sun, Q., Zabrouskov, V., Giacomelli, L., Rudella, A., Ytterberg, A.J., Rutschow, H., and van Wijk, K.J. (2006). The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol. Cell. Proteomics 5: 114-133.
52. Pfister, B., Lu, K.J., Eicke, S., Feil, R., Lunn, J.E., Streb, S., and Zeeman, S.C. (2014). Genetic evidence that chain length and branch point distributions are linked determinants of starch granule formation in Arabidopsis. Plant Physiol. 165: 1457-1474.
53. Ritte, G., Lloyd, J.R., Eckermann, N., Rottmann, A., Kossmann, J., and Steup, M. (2002). The starch-related R1 protein is an a -glucan, water dikinase. Proc. Natl. Acad. Sci. USA 99: 7166-7171.
54. Roldán, I., Wattebled, F., Mercedes Lucas, M., Delvallé, D., Planchot, V., Jiménez, S., Pérez, R., Ball, S., D’Hulst, C., and Mérida, A. (2007). The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J. 49: 492-504.
55. Santelia, D., Kötting, O., Seung, D., Schubert, M., Thalmann, M., Bischof, S., Meekins, D.A., Lutz, A., Patron, N., Gentry, M.S., Allain, F.H.T., and Zeeman, S.C. (2011). The phosphoglucan phosphatase Like Sex Four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell 23: 4096-4111.
56. Scialdone, A., Mugford, S.T., Feike, D., Skeffington, A., Borrill, P., Graf, A., Smith, A.M., and Howard, M. (2013). Arabidopsis plants perform arithmetic division to prevent starvation at night. eLife 2: e00669.
57. Seung, D., Soyk, S., Coiro, M., Maier, B.A., Eicke, S., and Zeeman, S.C. (2015). PROTEIN TARGETING TO STARCH is required for localising GRANULE-BOUND STARCH SYNTHASE to starch granules and for normal amylose synthesis in Arabidopsis. PLoS Biol. 13: e1002080.
58. Skeffington, A.W., Graf, A., Duxbury, Z., Gruissem, W., and Smith, A.M. (2014). Gucan, water dikinase exterts little control over starch degradation in Arabidopsis leaves at night. Plant Physiol. 165: 866-879.
59. Smith, A.M. (2012). Starch in the Arabidopsis plant. Starke 64: 421-434.
60. Stein, L.D., Mungall, C., Shu, S., Caudy, M., Mangone, M., Day, A., Nickerson, E., Stajich, J.E., Harris, T.W., Arva, A., and Lewis, S. (2002). The generic genome browser: a building block for a model organism system database. Genome Res. 12: 1599-1610.
61. Streb, S., Delatte, T., Umhang, M., Eicke, S., Schorderet, M., Reinhardt, D., and Zeeman, S.C. (2008). Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell 20: 3448-3466.
62. Sulpice, R., Flis, A., Ivakov, A.A., Apelt, F., Krohn, N., Encke, B., Abel, C., Feil, R., Lunn, J.E., and Stitt, M. (2014). Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol. Plant 7: 137-155.
63. Szydlowski, N., et al. (2009). Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21: 2443-2457.
64. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
65. Tanimoto, M., Tremblay, R., and Colasanti, J. (2008). Altered gravitropic response, amyloplast sedimentation and circumnutation in the Arabidopsis shoot gravitropism 5 mutant are associated with reduced starch levels. Plant Mol. Biol. 67: 57-69.
66. Truernit, E., Bauby, H., Dubreucq, B., Grandjean, O., Runions, J., Barthélémy, J., and Palauqui, J.C. (2008). High-resolution wholemount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell 20: 1494-1503.
67. Usadel, B., Bläsing, O.E., Gibon, Y., Retzlaff, K., Höhne, M., Günther, M., and Stitt, M. (2008). Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol. 146: 1834-1861.
68. Waigh, T.A., Perry, P., Donald, A.M., Gidley, M.J., and Riekel, C. (1998). Chiral side-chain liquid-crystalline polymeric properties of starch. Macromolecules 31: 7980-7984.
69. Waigh, T.A., Kato, K.L., Donald, A.N., Gidley, M.J., Clarke, C.J., and Reikel, C. (2000). Side-chain liquid-crystalline model for starch. Starke 52: 450-460.
70. Weise, S.E., Weber, A.P., and Sharkey, T.D. (2004). Maltose is the major form of carbon exported from the chloroplast at night. Planta 218: 474-482.
71. Weise, S.E., and Kiss, J.Z. (1999). Gravitropism of inflorescence stems in starch-deficient mutants of Arabidopsis. Int. J. Plant Sci. 160: 521-527.
72. Yu, T.S., Lue, W.L., Wang, S.M., and Chen, J. (2000). Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol. 123: 319-326.
73. Yu, T.S., et al. (2001). The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13: 1907-1918.
74. Yu, T.S., et al. (2005). α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J. Biol. Chem. 280: 9773-9779.
75. Zeeman, S.C., Tiessen, A., Pilling, E., Kato, K.L., Donald, A.M., and Smith, A.M. (2002). Starch synthesis in Arabidopsis. Granule synthesis, composition, and structure. Plant Physiol. 129: 516-529.
76. Zeeman, S.C., Umemoto, T., Lue, W.L., Au-Yeung, P., Martin, C., Smith, A.M., and Chen, J. (1998). A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10: 1699-1712.
77. Zhang, X., Henriques, R., Lin, S.S., Niu, Q.W., and Chua, N.H. (2006). Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1: 641-646.