Photosynthetica, 2007 (vol. 45), issue 3

Photosynthetica 2007, 45(3):400-408 | DOI: 10.1007/s11099-007-0068-3

Early seedling growth and morphogenesis in the xantha1 mutant of sunflower with alteration of chloroplast biogenesis

M. Fambrini1, G. Cionini2, N. Rascio3, F. Dalla Vecchia3, C. Pugliesi1,*
1 Dipartimento di Biologia delle Piante Agrarie-Sezione di Genetica, Università di Pisa, Pisa, Italy
2 Istituto di Biologia e Biotecnologia Agraria, CNR-Area della Ricerca di Pisa, Pisa, Italy
3 Dipartimento di Biologia, Università di Padova, Padova, Italy

In the xantha1 (xan1) mutant of sunflower (Helianthus annuus L.), the effects on organ anatomy and seedling growth did correlate to the alteration of chloroplast biogenesis. The xan1 seedlings grown under 165 µmol(photon) m-2 s-1 revealed a severely altered chloroplast ultrastructure in cotyledons and leaves. Cross-sections or clarified tissues of the xan1 cotyledons did not show evident alterations with respect to normal cotyledons suggesting that the impairment of chloroplast biogenesis has negligible consequences on embryonic leaves. By contrast, the analysis of xan1 leaves showed that the defects in chloroplast biogenesis were correlated to a drastic reduction of organ size and to a clear enhancement of the trichome growth. The differentiation of palisade and spongy parenchyma in cotyledons and leaves of the xan1 mutant was normal but both organs displayed a drastic reduction in the plastid number with respect to wild type. In addition, xan1 hypocotyls showed a reduced development of the main vascular bundles in comparison with normal seedlings and an undersized central cylinder of the primary root. The exogenous supply of sucrose was not sufficient to revert in vitro the deficit of xan1 growth and the constraints in morphogenetic processes.

Keywords: chloroplast ultrastructure; Helianthus annuus; in vitro culture; pigment-deficient mutant; trichome development

Received: October 19, 2006; Accepted: February 2, 2007; Published: September 1, 2007Show citation

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Fambrini, M., Cionini, G., Rascio, N., Vecchia, F., & Pugliesi, C. (2007). Early seedling growth and morphogenesis in the xantha1 mutant of sunflower with alteration of chloroplast biogenesis. Photosynthetica, 45(3), 400-408. doi: 10.1007/s11099-007-0068-3.
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    References

    1. Ahlert, D., Ruf, S., Bock, R.: Plastid protein synthesis is required for plant development in tobacco.-Proc. nat. Acad. Sci. USA 100: 15730-15735, 2003. Go to original source...
    2. Aluru, M.R., Bae, B., Wu, D., Rodermel, S.R.: The Arabidopsis immutans mutation affects plastid differentiation and the morphogenesis of white and green sectors in variegated plants.-Plant Physiol. 127: 67-77, 2001. Go to original source...
    3. Aluru, M.R., Yu, F., Fu, A., Rodermel, S.: Arabidopsis variegation mutants: new insights into chloroplast biogenesis.-J. exp. Bot. 57: 1871-1881, 2006.
    4. Asano, T., Yoshioka, Y., Machida, Y.: A defect in atToc159 of Arabidopsis thaliana causes severe defects in leaf development.-Genes genet. Syst. 79: 207-212, 2004. Go to original source...
    5. Barrero, J.M., Piqueras, P., González-Guzmán, M., Serrano, R., Rodriguez, P.L., Ponce, M.R., Micol, J.L.: A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development.-J. exp. Bot. 56: 2071-2083, 2005. Go to original source...
    6. Bellaoui, M., Gruissem, W.: Altered expression of the Arabidopsis ortholog of DCL affects normal plant development.-Planta 219: 819-826, 2004. Go to original source...
    7. Bellaoui, M., Keddie, J.S., Gruissem, W.: DCL is a plant-specific protein required for plastid ribosomal RNA processing and embryo development.-Plant mol. Biol. 53: 531-543, 2003. Go to original source...
    8. Bisanz, C., Begot, L., Carol, P., Bligny, M., Pesey, H., Gallois, J.L., Lerbs-Mache, S., Mache, R.: The Arabidopsis nuclear DAL gene encodes a chloroplast protein which is required for the maturation of plastid ribosomal RNAs and is essential for chloroplast differentiation.-Plant mol. Biol. 51: 651-663, 2003. Go to original source...
    9. Bonnema, A.B., Castillo, C., Reiter, N., Cunningham, M., Dams, H.P., O'Connell, M.: Molecular and ultrastructural analysis of a nonchromosomal variegated mutant. Tomato mitochondrial mutants that cause abnormal leaf development.-Plant Physiol. 109: 385-392, 1995. Go to original source...
    10. Chatterjee, M., Sparvoli, S., Edmunds, C., Garosi, P., Findlay, K., Martin, C.: DAG, a gene required for chloroplast differentiation and palisade development in Antirrhinum majus.-EMBO J. 15: 4194-4207, 1996. Go to original source...
    11. Cookson, P.J., Kiano, J.W., Shipton, C.A., Fraser, P.D., Romer, S., Schuch, W., Bramley, P.M., Pyke, K.A.: Increases in cell elongation, plastid compartment size and phytoene synthase activity underline the phenotype of the high pigment-1 mutant of tomato.-Planta 217: 896-903, 2003. Go to original source...
    12. Dewitte, W., Murray, J.A.: The plant cell cycle.-Annu. Rev. Plant Physiol. Plant mol. Biol. 54: 235-264, 2003. Go to original source...
    13. Fambrini, M., Bonsignori, E., Rapparini, F., Cionini, G., Michelotti, V., Bertini, D., Baraldi, R., Pugliesi, C.: stem fasciated, a recessive mutation in sunflower (Helianthus annuus), alters plant morphology and auxin level.-Ann. Bot. 98: 715-730, 2006. Go to original source...
    14. Fambrini, M., Castagna, A., Dalla Vecchia, F., Degl'Innocenti, E., Ranieri, A., Vernieri, P., Pardossi, A., Guidi, L., Rascio, N., Pugliesi, C.: Characterization of a pigment-deficient mutant of sunflower (Helianthus annuus L.) with abnormal chloroplast biogenesis, reduced PS II activity and low endogenous level of abscisic acid.-Plant Sci. 167: 79-89, 2004. Go to original source...
    15. González-Bayón, R., Kinsman, E.A., Quesada, V., Vera, A., Robles, P., Ponce, M.R., Pyke, K.A., Micol, J.L.: Mutations in the RETICULATA gene dramatically alter internal architecture but have little effect on overall organ shape in Arabidopsis leaves.-J. exp. Bot. 57: 3019-3031, 2006. Go to original source...
    16. Gray, J.C., Sullivan, J.A., Wang, J.H., Jerome, C.A., MacLean, D.: Coordination of plastid and nuclear gene expression.-Phil. Trans. roy. Soc. London B 358: 135-145, 2002.
    17. Guidi, L., Degl'Innocenti, E., Fambrini, M., Pugliesi, C., Soldatini, G.F.: Gas exchange analysis and chlorophyll a fluorescence in cotyledons of the xan1 sunflower mutant with defects in light energy utilization.-Environ. exp. Bot. 56: 182-189, 2006. Go to original source...
    18. Henriques, R., Jásik, J., Klein, M., Martinoia, E., Feller, U., Schell, J., Pais, M.S., Koncz, C.: Knock-out of Arabidopsis metal transporter gene IRT1 results in iron deficiency accompanied by cell differentiation defects.-Plant mol. Biol. 50: 587-597, 2002. Go to original source...
    19. Holding, D.R., Springer, P.S., Coomber, S.A.: The chloroplast and leaf development mutant, pale cress, exhibits light-conditional severity and symptoms characteristics of its ABA deficiency.-Ann. Bot. 86: 953-962, 2000. Go to original source...
    20. Hricová, A., Quesada, V., Micol, J.L.: The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis.-Plant Physiol. 141: 942-956, 2006.
    21. Johnson, H.B.: Plant pubescence: an ecological perspective.-Bot. Rev. 41: 233-258, 1975. Go to original source...
    22. Keddie, J.S., Carroll, B., Jones, J.D., Gruissem, W.: The DCL gene of tomato is required for chloroplast development and palisade cell morphogenesis in leaves.-EMBO J. 15: 4208-4217, 1996. Go to original source...
    23. Kuroda, H., Maliga, P.: The plastid clpP1 protease gene is essential for plant development.-Nature 425: 86-89, 2003. Go to original source...
    24. Kutschera, U.: Role of cotyledons in the maintenance of hypocotyl growth in Helianthus annuus L.-J. Plant Physiol. 140: 319-323, 1992. Go to original source...
    25. Labate, M.T.V., Ko, K., Ko, Z.W., Costa Pinto, L.S.R., Real, M.J.U.D., Romano, M.R., Barja, P.R., Granell, A., Friso, G., Wijk, K.J., Brugnoli, E., Labate, C.A.: Constitutive expression of pea Lhcb1-2 in tobacco affects plant development, morphology and photosynthetic capacity.-Plant mol. Biol. 55: 701-714, 2004. Go to original source...
    26. Lenzi, A., Fambrini, M., Barotti, S., Pugliesi, C., Vernieri, P.: Seed germination and seedling growth in a wilty mutant of sunflower (Helianthus annuus L.): Effect of abscisic acid and osmotic potential.-Environ. exp. Bot. 35: 427-434, 1995. Go to original source...
    27. Malamy, J.E.: Intrinsic and environmental response pathways that regulate root system architecture.-Plant Cell Environ. 28: 67-77, 2005. Go to original source...
    28. Mandel, M.A., Feldmann, K.A., Herrera-Estrella, L., Rocha-Sosa, M., Leon, P.: CLA1, a novel gene required for chloroplast development, is highly conserved in evolution.-Plant J. 9: 649-658, 1996. Go to original source...
    29. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures.-Physiol. Plant. 15: 473-497, 1962. Go to original source...
    30. Mustárdy, L., Garab, G.: Granum revisited. A three-dimensional model-where things fall into place.-Trends Plant Sci. 8: 117-122, 2003. Go to original source...
    31. Naested, H., Holm, A., Jenkins, T., Nielsen, H.B., Harris, C.A., Beale, M.H., Andersen, M., Mant, A., Scheller, H., Camara, B., Mattsson, O., Mundy, J.: Arabidopsis VARIEGATED 3 encodes a chloroplast-targeted, zinc-finger protein required for chloroplast and palisade cell development.-J. Cell Sci. 117: 4807-4818, 2004. Go to original source...
    32. Neuhaus, H.E., Emes, M.J.: Nonphotosynthetic metabolism in plastids.-Annu. Rev. Plant Physiol. Plant mol. Biol. 51: 111-140, 2000. Go to original source...
    33. Ramesar-Fortner, N.S., Aiken, S.G., Dengler, N.G.: Phenotypic plasticity in leaves of four species of arctic Festuca (Poaceae).-Can. J. Bot. 73: 1810-1823, 1995.
    34. Rodermel, S.: Pathways of plastid-to-nucleus signaling.-Trends Plant Sci. 6: 471-478, 2001. Go to original source...
    35. Ruzin, S.E.: Microtechnique notes and problem solving.-In: Plant Microtechnique and Microscopy. Pp. 137-144. Oxford University Press, New York-Oxford 1999.
    36. Sakamoto, W.: Leaf-variegated mutations and their responsible genes in Arabidopsis thaliana.-Genes genet. Syst. 78: 1-9, 2003. Go to original source...
    37. Simidjiev, I., Barzda, V., Mustárdy, L., Garab, G.: Role of thylakoid lipids in the structural flexibility of lamellar aggregates of the isolated light-harvesting chlorophyll a/b complex of photosystem II.-Biochemistry 37: 4169-4173, 1998. Go to original source...
    38. Somerville, C.R.: Analysis of photosynthesis with mutants of higher plants and algae.-Annu. Rev. Plant Physiol. 37: 467-507, 1986. Go to original source...
    39. Streatfield, S.J., Weber, A., Kinsman, E.A., Häusler, R.E., Li, J., Post-Beittenmiller, D., Kaiser, W.M., Pyke, K.A., Flügge, U.-I., Chory, J.: The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade development, and plastid-dependent nuclear gene expression.-Plant Cell 11: 1609-1621, 1999. Go to original source...
    40. Susek, R.E., Ausubel, F.M., Chory, J.: Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development.-Cell 74: 787-799, 1993.
    41. Swingle, C.F.: Regeneration and vegetative propagation.-Bot. Rev. 6: 301-355, 1940. Go to original source...
    42. Vasil, V., Hildebrandt, A.C.: Growth and tissue formation from single, isolated tobacco cells in microculture.-Science 147: 1454-1455, 1965. Go to original source...
    43. Wang, Y., Duby, G., Purnelle, B., Boutry, M.: Tobacco VDL gene encodes a plastid DEAD box RNA helicase and is involved in chloroplast differentiation and plant morphogenesis.-Plant Cell 12: 2129-2142, 2000. Go to original source...
    44. Wycliffe, P., Sitbon, F., Wernersson, J., Ezcurra, I., Ellerström, M., Rask, L.: Continuous expression in tobacco leaves of a Brassica napus PEND homologue blocks differentiation of plastids and development of palisade cells.-Plant J. 44: 1-15, 2005. Go to original source...
    45. Yano, S., Terashima, I.: Developmental process of sun and shade leaves in Chenopodium album L.-Plant Cell Environ. 27: 781-793, 2004. Go to original source...

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