Transcript and metabolite signature of maize source leaves suggests a link between transitory starch to sucrose balance and the autonomous floral transition

Journal of Experimental Botany

Volumn 63, Issue 14, 2012, Pages 5079-5092

  Coneva, Viktoriya ^a   Guevara, David ^a   Rothstein, Steven J ^a   Colasanti, Joseph ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Autonomous floral transition; indeterminate1; maize; source leaf; teosinte; transcript and metabolite

Indexed keywords

CARBON; FLORIGEN; ID1 PROTEIN, PLANT; STARCH; SUCROSE; TRANSCRIPTION FACTOR; TRANSCRIPTOME; VEGETABLE PROTEIN;

ARTICLE; CITRIC ACID CYCLE; CYTOLOGY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; MASS FRAGMENTOGRAPHY; METABOLISM; PHOTOPERIODICITY; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY;

CARBON; CITRIC ACID CYCLE; FLORIGEN; FLOWERS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MICROSCOPY, ELECTRON, TRANSMISSION; PHOTOPERIOD; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STARCH; SUCROSE; TRANSCRIPTION FACTORS; TRANSCRIPTOME; ZEA MAYS;

ZEA MAYS;

EID: 84865773628     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ers158     Document Type: Article

References (75)

1. Ainsworth EA, Bush DR. 2011. Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiology 155, 64-69.
2. Amasino R. 2010. Seasonal and developmental timing of flowering. The Plant Journal 61, 1001-1013.
3. Aoki N, Hirose T, Takahashi S, Ono K, Ishimaru K, Ohsugi R. 1999. Molecular cloning and expression analysis of a gene for a sucrose transporter maize (Zea mays L.). Plant and Cell Physiology 40, 1072-1078.
4. Arnon DI. 1949. Copper enzymes in isolated chloroplasts-polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1-15.
5. Barker L, Kühn C, Weise A, Schulz A, Gebhardt C, Hirner B, Hellmann H, Schulze W, Ward JM, Frommer WB. 2000. SUT2, a putative sucrose sensor in sieve elements. The Plant Cell 12, 1153-1164.
6. Bodson M, Outlaw WH Jr. 1985. Elevation in the sucrose content of the shoot apical meristem of Sinapis alba at floral evocation. Plant Physiology 79, 420-424.
7. Botha CEJ, Cross RHM, van Bel AJE, Peter CI. 2000. Phloem loading in the sucrose-export-defective (SXD-1) mutant maize is limited by callose deposition at plasmodesmata in bundle sheath-vascular parenchyma interface. Protoplasma 214, 65-72.
8. Bradford M. 1976. A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye-binding. Analytical Biochemistry 72, 248-254.
9. Braun DM, Slewinski TL. 2009. Genetic control of carbon partitioning in grasses: roles of sucrose transporters and Tie-dyed loci in phloem loading. Plant Physiology 149, 71-81.
10. Buckler ES, Holland JB, Bradbury PJ, et al. 2009. The genetic architecture of maize flowering time. Science 325, 714-718.
11. Burkle L, Hibberd JM, Quick WP, Kühn C, Hirner B, Frommer WB. 1998. The H+-sucrose cotransporter NtSUT1 is essential for sugar export from tobacco leaves. Plant Physiology 118, 59-68.
12. Chardon F, Virlon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Charcosset A. 2004. Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta-analysis and synteny conservation with the rice genome. Genetics 168, 2169-2185.
13. Chen HJ, Wang SJ. 2008. Molecular regulation of sink-source transition in rice leaf sheaths during the heading period. Acta Physiologiae Plantarum 30, 639-649.
14. Chincinska IA, Liesche J, Kruegel U, Michalska J, Geigenberger P, Grimm B, Kühn C. 2008. Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiology 146, 515-528.
15. Chiou TJ, Bush DR. 1998. Sucrose is a signal molecule in assimilate partitioning. Proceedings of the National Academy of Sciences, USA 95, 4784-4788.
16. Colasanti J, Muszynski MG. 2008. The maize floral transition. In: Hake SC, Bennetzen JL, eds. Handbook of maize: its biology, Vol. 1. Berlin: Springer Science, 41-55.
17. Colasanti J, Tremblay R, Wong AYM, Coneva V, Kozaki A, Mable BK. 2006. The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants. BMC Genomics 7, 1-15.
18. Colasanti J, Yuan Z, Sundaresan V. 1998. The indeterminate gene encodes a zinc finger protein and regulates a leaf-generated signal required for the transition to flowering in maize. Cell 93, 593-603.
19. Coneva V, Zhu T, Colasanti J. 2007. Expression differences between normal and indeterminate1 maize suggest downstream targets of ID1, a floral transition regulator in maize. Journal of Experimental Botany 58, 3679-3693.
20. Corbesier L, Lejeune P, 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.
21. Corbesier L, Vincent C, Jang SH, et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033.
22. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. 2010. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Research 38, W64-W70.
23. Eimert K, Wang SM, Lue WL, Chen JC. 1995. Monogenic recessive mutations causing both late floral initiation and excess starch accumulation in Arabidopsis. The Plant Cell 7, 1703-1712.
24. El-Lithy ME, Reymond M, Stich B, Koornneef M, Vreugdenhil D. 2010. Relation among plant growth, carbohydrates and flowering time in the Arabidopsis Landsberg erecta×Kondara recombinant inbred line population. Plant, Cell and Environment 33, 1369-1382.
25. Emerson RA. 1924. Control of flowering in teosinte. Journal of Heredity 15, 41-48.
26. Feurtado JA, Huang DQ, Wicki-Stordeur L, Hemstock LE, Potentier MS, Tsang EWT, Cutler AJ. 2011. The Arabidopsis C2H2 zinc finger INDETERMINATE DOMAIN1/ENHYDROUS promotes the transition to germination by regulating light and hormonal signaling during seed maturation. The Plant Cell 23, 1772-1794.
27. Gibon Y, Pyl ET, Sulpice R, Lunn JE, Hohne M, Gunther M, 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 and Environment 32, 859-874.
28. Irish E, Jegla D. 1997. Regulation of extent of vegetative development of the maize shoot meristem. The Plant Journal 11, 63-71.
29. Irish EE, Nelson TM. 1991. Identification of multiple stages in the conversion of maize meristems from vegetative to floral development. Development 112, 891-898.
30. Jaeger KE, Graf A, Wigge PA. 2006. The control of flowering in time and space. Journal of Experimental Botany 57, 3415-3418.
31. Kikuchi R, Kawahigashi H, Ando T, Tonooka T, Handa H. 2009. Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering. Plant Physiology 149, 1341-1353.
32. Kopka J, Schauer N, Krueger S, et al. 2005. GMD@CSB.DB: the Golm Metabolome Database. Bioinformatics 21, 1635-1638.
33. Kozaki A, Hake S, Colasanti J. 2004. The maize ID1 flowering time regulator is a zinc finger protein with novel DNA binding properties. Nucleic Acids Research 32, 1710-1720.
34. Kühn C, Frommer W. 1995. A novel zinc finger protein encoded by a couch potatohomologue from Solanum tuberosumenables a sucrose transport-deficient yeast strain to grow on sucrose. Molecular and General Genetics 247, 759-763.
35. Lazakis CM, Coneva V, Colasanti J. 2011. ZCN8 encodes a potential orthologue of Arabidopsis FT florigen that integrates both endogenous and photoperiod flowering signals in maize. Journal of Experimental Botany 62, 4833-4842.
36. Leggewie G, Kolbe A, Lemoine R, et al. 2003. Overexpression of the sucrose transporter SoSUT1 in potato results in alterations in leaf carbon partitioning and in tuber metabolism but has little impact on tuber morphology. Planta 217, 158-167.
37. Lejeune P, Bernier G, Requier MC, Kinet JM. 1993. Sucrose increases during floral induction in the phloem sap collected at the apical part of the shoot of the long-day plant Sinapis-alba L. Planta 190, 71-74.
38. Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y. 2006. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proceedings of the National Academy of Sciences, USA 103, 6398-6403.
39. Lin MK, Belanger H, Lee YJ, et al. 2007. FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. The Plant Cell 19, 1488-1506.
40. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T) (-Delta Delta C) method. Methods 25, 402-408.
41. Ma Y, Slewinski TL, Baker RF, Braun DM. 2009. Tie-dyed1 encodes a novel, phloem-expressed transmembrane protein that functions in carbohydrate partitioning. Plant Physiology 149, 181-194.
42. Matsubara K, Yamanouchi U, Wang ZX, Minobe Y, Izawa T, Yano M. 2008. Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiology 148, 1425-1435.
43. Meng X, Muszynski MG, Danilevskaya ON. 2011. The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. The Plant Cell 23, 942-960.
44. Meyer RC, Steinfath M, Lisec J, et al. 2007. The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104, 4759-4764.
45. Morita MT, Sakaguchi K, Kiyose SI, Taira K, Kato T, Nakamura M, Tasaka M. 2006. A C2H2-type zinc finger protein, SGR5, is involved in early events of gravitropism in Arabidopsis inflorescence stems. The Plant Journal 47, 619-628.
46. Muszynski MG, Dam T, Li B, Shirbroun DM, Hou ZL, Bruggemann E, Archibald R, Ananiev EV, Danilevskaya ON. 2006. Delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiology 142, 1523-1536.
47. Nuin P, Weretilnyk, EA, Summers, PS, Guevara, DR, Golding, GB. 2004. GASP: GC/MS Analysis Software Package.
48. Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K. 2001. Effects of sugar on vegetative development and floral transition in arabidopsis. Plant Physiology 127, 252-261.
49. Park SJ, Kim SL, Lee S, et al. 2008. Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. The Plant Journal 56, 1018-1029.
50. Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJL, Nilsson O. 2010. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330, 1397-1400.
51. Radchuk R, Radchuk V, Weschke W, Borisjuk L, Weber H. 2006. Repressing the expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiology 140, 263-278.
52. Radchuk R, Emery RJN, Weier D, Vigeolas H, Geigenberger P, Lunn JE, Feil R, Weschke W, Weber H. 2010. Sucrose non-fermenting kinase 1 (SnRK1) coordinates metabolic and hormonal signals during pea cotyledon growth and differentiation. The Plant Journal 61, 324-338.
53. Raines CA, Paul MJ. 2006. Products of leaf primary carbon metabolism modulate the developmental programme determining plant morphology. Journal of Experimental Botany 57, 1857-1862.
54. Rideout JW, Raper CDJ, Miner GS. 1992. Changes in ratio of soluble sugars and free amino nitrogen in the apical meristem during floral transition in tobacco. International Journal of Plant Sciences 153, 78-88.
55. Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L. 2000. Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. The Plant Journal 23, 131-142.
56. Russin WA, Evert RF, Vanderveer PJ, Sharkey TJ, Briggs SP. 1996. Modification of a specific class of plasmodesmata and loss of sucrose export ability in the sucrose export defective1 maize mutant. The Plant Cell 8, 645-658.
57. Sachs RM, Hackett WP. 1983. Source-sink relationships and flowering. In: Meudt WJ, ed. Strategies of plant reproduciton. Totowa, NJ: Allenheld-Osmun, 263-272.
58. Salvi S, Sponza G, Morgante M, et al. 2007. Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proceedings of the National Academy of Sciences, USA 104, 11376-11381.
59. Seo PJ, Kim MJ, Ryu J-Y, Jeong E-Y, Park C-M. 2011a. Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism. Nature Communications 2, 303.
60. Seo PJ, Ryu J, Kang SK, Park CM. 2011b. Modulation of sugar metabolism by an INDETERMINATE DOMAIN transcription factor contributes to photoperiodic flowering in Arabidopsis. The Plant Journal 65, 418-429.
61. Sharkey TD, Laporte M, Lu Y, Weise S, Weber APM. 2004. Engineering plants for elevated CO2: a relationship between starch degradation and sugar sensing. Plant Biology 6, 280-288.
62. Sheehan MJ, Kennedy LM, Costich DE, Brutnell TP. 2007. Subfunctionalization of PhyB1 and PhyB2 in the control of seedling and mature plant traits in maize. The Plant Journal 49, 338-353.
63. Slewinski TL, Braun DM. 2010. Current perspectives on the regulation of whole-plant carbohydrate partitioning. Plant Science 178, 341-349.
64. Slewinski TL, Meeley R, Braun DM. 2009. Sucrose transporter1 functions in phloem loading in maize leaves. Journal of Experimental Botany 60, 881-892.
65. Tamaki S, Matsuo S, Wong HL, Yokoi S, Shimamoto K. 2007. Hd3a protein is a mobile flowering signal in rice. Science 316, 1033-1036.
66. Tanimoto M, Tremblay R, Colasanti J. 2008. Altered gravitropic response, amyloplast sedimentation and circumnutation in the Arabidopsis shoot gravitropism 5 mutant are associated with reduced starch levels. Plant Molecular Biology 67, 57-69.
67. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914-939.
68. Tsuji H, Taoka K, Shimamoto K. 2011. Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Current Opinion in Plant Biology 14, 45-52.
69. Vaughn MW, Harrington GN, Bush DR. 2002. Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proceedings of the National Academy of Sciences, USA 99, 10876-10880.
70. Weise SE, van Wijk KJ, Sharkey TD. 2011. The role of transitory starch in C(3), CAM, and C(4) metabolism and opportunities for engineering leaf starch accumulation. Journal of Experimental Botany 62, 3109-3118.
71. Weise SE, Weber APM, Sharkey TD. 2004. Maltose is the major form of carbon exported from the chloroplast at night. Planta 218, 474-482.
72. Wilson IW, Kennedy GC, Peacock JW, Dennis ES. 2005. Microarray analysis reveals vegetative molecular phenotypes of arabidopsis flowering-time mutants. Plant and Cell Physiology 46, 1190-1201.
73. Wong AYM, Colasanti J. 2007. Maize floral regulator protein INDETERMINATE1 is localized to developing leaves and is not altered by light or the sink/source transition. Journal of Experimental Botany 58, 403-414.
74. Wong CE, Singh MB, Bhalla PL. 2009. Molecular processes underlying the floral transition in the soybean shoot apical meristem. The Plant Journal 57, 832-845.
75. Wu CY, You CJ, Li CS, Long T, Chen GX, Byrne ME, Zhang QF. 2008. RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proceedings of the National Academy of Sciences, USA 105, 12915-12920.