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Carbohydrate regulation of leaf development: Prolongation of leaf senescence in Rubisco antisense mutants of tobacco

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Abstract

Previous investigations have shown that increased source strength as a result of elevated CO2 can alter the timing of the phases of change that occur in photosynthetic rates during dicot leaf ontogeny [Miller et al. (1997) Plant Physiol 115: 1195–1200]. To evaluate the converse situation of decreased source strength, we examined leaf development in rbcS antisense mutants of tobacco. These mutants have depressed Rubisco levels and decreased rates of carbohydrate production. We found that antisense leaves are longer-lived than wild type leaves and that this appeared to be due to a prolongation of the senescence phase of development, as monitored by photosynthetic rates, chlorophyll content, and the abundance and activity of Rubisco. Declines in these parameters during leaf ontogeny in both the wild type and mutant plants were generally accompanied by coordinate reductions in the levels of rbcS mRNA and rbcL mRNA, as well as by reductions in chloroplast rRNA, chloroplast DNA and total protein. We suggest that the prolongation of senescence in the antisense leaves is due to an impact of source strength on leaf developmental programming that occurs, at least in part, at the level of transcript abundance of nuclear and chloroplast genes for chloroplast rRNAs and proteins. We hypothesize that plants are capable of sensing a range of source strength conditions to initiate and modulate leaf developmental programming.

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References

  • Arnon DI (1949) Copper enzymes in chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24: 1–15

    Google Scholar 

  • Besford RT, Ludwig LJ and Withers AC (1990) The Greenhouse effect: acclimation of tomato plants growing in high CO2, photosynthesis and ribulose-1, 5-bisphosphate carboxylase protein. J Exp Bot 41: 925–931

    Google Scholar 

  • Bleecker AB and Patterson SE (1997) Last exit: Senescence, abscission, and meristem arrest in Arabidopsis. Plant Cell 9: 1169–1179

    Article  PubMed  Google Scholar 

  • Brutnell TP and Langdale JA (1998) Signals in leaf development. In: Advances in Botanical Research, Vol 28, pp 161–195. Academic Press Publishers, San Diego, California

    Google Scholar 

  • Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 307: 181–199

    Google Scholar 

  • Criqui MC, Durr A, Parmentier J, Marbach J, Fleck J and Jamet E (1992) How are photosynthetic genes repressed in freshlyisolated mesophyll protoplasts of Nicotiana sylvestris? Plant Physiol Biochem 30: 597–601

    Google Scholar 

  • Dai N, Schaffer A, Petreikov M, Shahak Y, Giller Y, Ratner K, Levine A and Granot D (1999) Overexpression of Arabidopsis hexokinase in tomato plants inhibits growth, reduces photosynthesis, and induces rapid senescence. Plant Cell 11: 1253–1266

    Article  PubMed  Google Scholar 

  • Dickinson CD, Altabella T and Chrispeels MJ (1991) Slow-growth phenotype of transgenic tomato expressing apoplastic invertase. Plant Physiol 95: 420–425

    Google Scholar 

  • Gan S and Amasino RM (1997) Making sense of senescence: molecular genetic regulation and manipulation of leaf senescence. Plant Physiol 113: 313–319

    PubMed  Google Scholar 

  • Gepstein S (1988) Photosynthesis. In: Noodén LD and Leopold AC (eds) Senescence and Aging in Plants, pp 85–109. Academic Press Publishers, San Diego, California

    Google Scholar 

  • Goldschmidt EE and Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol 99: 1443–1448

    Google Scholar 

  • Hensel LL, Grbic V, Baumgarten DA and Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. Plant Cell 5: 553–564

    Article  PubMed  Google Scholar 

  • Jang J-C and Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6: 1665–1679

    Article  PubMed  Google Scholar 

  • Jang J-C, León P, Zhou L and Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9: 5–19

    Article  PubMed  Google Scholar 

  • Jiang C-Z and Rodermel SR (1995) Regulation of photosynthesis during leaf development in rbcS antisense DNA mutants of tobacco. Plant Physiol 107: 215–224

    PubMed  Google Scholar 

  • Jiang C-Z, Rodermel SR and Shibles RM (1993) Photosynthesis, Rubisco activity and amount, and their regulation by transcription in senescing soybean leaves. Plant Physiol 101: 105–112

    PubMed  Google Scholar 

  • Jones PG, Lloyd JC and Raines CA (1996) Glucose feeding of intact wheat plants represses the expression of a number of Calvin cycle genes. Plant Cell Environ 19: 231–236

    Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509–540

    Article  PubMed  Google Scholar 

  • Krapp A and Stitt M (1994) Influence of high-carbohydrate content on the activity of plastidic and cytosolic isoenzyme pairs in photosynthetic tissues. Plant Cell Environ 17: 861–866

    Google Scholar 

  • Krapp A, Hofmann B, Schafer C and Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: A mechanism for the 'sink regulation' of photosynthesis? Plant J 3: 817–828

    Article  Google Scholar 

  • Krapp A, Quick WP and Stitt M (1991) Ribulose-1,5-bisphosphate carboxylase-oxygenase, other photosynthetic enzymes and chlorophyll decrease when glucose is supplied to mature spinach leaves via transpiration stream. Planta 186: 58–69

    Article  Google Scholar 

  • Lohman KN, Gan S, Manorama CJ and Amasino RM (1994) Molecular analysis of natural leaf senescence in Arabidopsis thaliana. Physiol Plant 92: 322–328

    Article  Google Scholar 

  • Matile P (1992) Chloroplast senescence. In: Baker NR and H Thomas H (eds) Crop photosynthesis: Spatial and Temporal Determinants, pp 413–441. Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • Miller A, Tsai C-H, Hemphill D, Endres M, Rodermel S and Spalding M (1997) Elevated CO2 effects during leaf ontogeny: A new perspective on acclimation. Plant Physiol 115: 1195–1200

    PubMed  Google Scholar 

  • Nie G, Hendrix DL, Webber AN, Kimball BA and Long SP (1995) Increased accumulation of carbohydrates and decreased photosynthetic gene transcript levels in wheat grown at an elevated CO2 concentration in the field. Plant Physiol 108: 975–983

    PubMed  Google Scholar 

  • Noodén LD, Hillsberg JW and Schneider MJ (1996) Induction of leaf senescence in Arabidopsis thaliana by long days through a light-dosage effect. Physiologia Plantarum 96: 491–495

    Article  Google Scholar 

  • Pearson Mand Brooks GL (1995) The influence of elevated CO2 on growth and age-related changes in leaf gas exchange. J Exp Bot 46: 1651–1659

    Google Scholar 

  • Quick WP, Schurr U, Scheibe R, Schulze E-D, Rodermel SR, Bogorad L and Stitt M (1991a) Decreased ribulose-1, 5-8 bisphospate carboxylase-oxygenase in transgenic tobacco transformed with 'antisense' rbcS. I. Impact on photosynthesis in ambient growth conditions. Planta 183: 542–554

    Article  Google Scholar 

  • Quick WP, Schurr U, Fichtner K, Schulze E-D, Rodermel SR, Bogorad L and Stitt M(1991b). The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS. Plant Journal 1: 51–58

    Article  Google Scholar 

  • Rodermel S (1999) Subunit control of Rubisco biosynthesis – a relic of an endosymbiotic past? Photosyn Res 59: 105–123

    Article  Google Scholar 

  • Rodermel SR, Abbott MS and Bogorad L (1988) Nuclear-organelle interactions: Nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55: 673–681

    Article  PubMed  Google Scholar 

  • Rodermel S, Haley J, Jiang C-Z, Tsai C-H and Bogorad L (1996) A mechanism for intergenomic integration: Abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large subunit mRNA. Proc Natl Acad Sci USA 93: 3881–3885

    Article  PubMed  Google Scholar 

  • Sheen J (1989) Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038

    Article  Google Scholar 

  • Sheen J (1994) Feedback control of gene expression. Photosynth Res 39: 427–438

    Article  Google Scholar 

  • Sims DA, Seemann JR and Luo Y (1998) Elevated CO2 concentration has independent effects on expansion rates and thickness of soybean leaves across light and nitrogen gradients. J Exp Bot 49: 583–591

    Article  Google Scholar 

  • Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14: 741–762

    Google Scholar 

  • Stitt M and Sonnewald U (1995) Regulation of metabolism in transgenic plants. Annu Rev Plant Physiol Plant Mol Biol 46: 341–368

    Article  Google Scholar 

  • Taylor G, Ranasinghe S, Bosac C, Gardner SDL and Ferris R (1994) Elevated CO2 and plant growth: Cellular mechanisms and responses of whole plants. J Exp Bot 45: 1761–1774

    Google Scholar 

  • Tsai C-H, Miller A, Spalding M and Rodermel S (1997) Source strength regulates an early phase transition of tobacco shoot morphogenesis. Plant Physiol 115: 907–914

    PubMed  Google Scholar 

  • Van Lijsebettens M and Clarke J (1998) Leaf development in Arabidopsis. Plant Physiol Biochem 36: 47–60

    Article  Google Scholar 

  • Van Oosten J-J and Besford RT (1995) Some relationships between the gas exchange, biochemistry and molecular biology of photosynthesis during leaf development of tomato plants after transfer to different carbon dioxide concentrations. Plant Cell Environ 18: 1253–1266

    Google Scholar 

  • Van Oosten J-J and Besford RT (1996) Acclimation of photosynthesis to elevated CO2 through feedback regulation of gene expression: Climate of opinion. Photosyn Res 48: 353–365

    Article  Google Scholar 

  • von Schaewen A, Stitt M, Schmidt R, Sonnewald U and Willmitzer L (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J 9: 3033–3044

    PubMed  Google Scholar 

  • Veierskov B (1987) Irradiance-dependent senescence of isolated leaves. Physiol Planta 71: 316–320

    Google Scholar 

  • Wingler A, von Schaewen A, Leegood RC, Lea PJ and Quick WP (1998) Regulation of leaf senescence by cytokinin, sugars, and light. Plant Physiol 116: 329–335

    Article  Google Scholar 

  • Zhou L, Jang J-C, Jones TL and Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci 95: 10294–10299

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Botany, IA State University, Ames, IA, 50011, USA

    Adam Miller, Carl Schlagnhaufer, Martin Spalding & Steven Rodermel

  2. Interdepartmental Plant Physiology Major, Iowa State University, Ames, IA, 50011, USA

    Adam Miller, Martin Spalding & Steven Rodermel

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  1. Adam Miller
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  2. Carl Schlagnhaufer
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  3. Martin Spalding
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  4. Steven Rodermel
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Miller, A., Schlagnhaufer, C., Spalding, M. et al. Carbohydrate regulation of leaf development: Prolongation of leaf senescence in Rubisco antisense mutants of tobacco. Photosynthesis Research 63, 1–8 (2000). https://doi.org/10.1023/A:1006367719639

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