Xylem development and cell wall changes of soybean seedlings grown in space.

BACKGROUND AND AIMS Plants growing in altered gravity conditions encounter changes in vascular development and cell wall deposition. The aim of this study was to investigate xylem anatomy and arrangement of cellulose microfibrils in vessel walls of different organs of soybean seedlings grown in Space. METHODS Seeds germinated and seedlings grew for 5 d in Space during the Foton-M2 mission. The environmental conditions, other than gravity, of the ground control repeated those experienced in orbit. The seedlings developed in space were compared with those of the control test on the basis of numerous anatomical and ultrastructural parameters such as number of veins, size and shape of vessel lumens, thickness of cell walls and deposition of cellulose microfibrils. KEY RESULTS Observations made with light, fluorescence and transmission electron microscopy, together with the quantification of the structural features through digital image analysis, showed that the alterations due to microgravity do not occur at the same level in the various organs of soybean seedlings. The modifications induced by microgravity or by the indirect effect of space-flight conditions, became conspicuous only in developing vessels at the ultrastructural level. The results suggested that the orientation of microfibrils and their assembly in developing vessels are perturbed by microgravity at the beginning of wall deposition, while they are still able to orient and arrange in thicker and ordered structures at later stages of secondary wall deposition. CONCLUSIONS The process of proper cell-wall building, although not prevented, is perturbed in Space at the early stage of development. This would explain the almost unaltered anatomy of mature structures, accompanied by a slower growth observed in seedlings grown in Space than on Earth.

[1]  T. W. Halstead,et al.  Plants in space. , 1987, Annual review of plant physiology.

[2]  H G Levine,et al.  Cell-wall architecture and lignin composition of wheat developed in a microgravity environment. , 2001, Phytochemistry.

[3]  R. Yamamoto,et al.  Changes in the rheological properties of the cell wall of plant seedlings under simulated microgravity conditions. , 1994, Biorheology.

[4]  EFFECT OF SIMULATED MICROGRAVITY ON SEEDLING DEVELOPMENT AND VASCULAR DIFFERENTIATION OF SOY , 2006 .

[5]  K. Ruel,et al.  Study of Lignification by Noninvasive Techniques in Growing Maize Internodes (An Investigation by Fourier Transform Infrared Cross-Polarization-Magic Angle Spinning 13C-Nuclear Magnetic Resonance Spectroscopy and Immunocytochemical Transmission Electron Microscopy) , 1997, Plant physiology.

[6]  J. Verbelen,et al.  Cellulose orientation determines mechanical anisotropy in onion epidermis cell walls. , 2006, Journal of experimental botany.

[7]  J. Thiery Mise en evidence des polysaccharides sur coupes fines en microscopie electronique , 1967 .

[8]  D J Cosgrove,et al.  Plant Cell Growth Responds to External Forces and the Response Requires Intact Microtubules , 1996, Plant physiology.

[9]  Gérald Perbal,et al.  Elongation and mitotic activity of cortical cells in lentil roots grown in microgravity , 1989 .

[10]  T. Giddings Microtubule-mediated control of microfibril deposition : a re-examination of the hypothesis , 1991 .

[11]  Maureen C. McCann,et al.  Direct visualization of cross-links in the primary plant cell wall , 1990 .

[12]  J. Joseleau,et al.  New immunogold probes for studying the distribution of the different lignin types during plant cell wall biogenesis , 1994 .

[13]  K. Eriksson,et al.  Micromorphological and Ultrastructural Aspects of Spruce Wood Degradation by Wild-Type Sporotrichum pulverulentum and its Cellulase-less Mutant Cel 44 , 1981 .

[14]  Tobias I. Baskin,et al.  On the alignment of cellulose microfibrils by cortical microtubules: A review and a model , 2005, Protoplasma.

[15]  V. Marinozzi Cytochimie ultrastructurale du nuclole RNA et protines intranuclolaires , 1964 .

[16]  D. Fisher,et al.  Extending the Microtubule/Microfibril paradigm. Cellulose synthesis is required for normal cortical microtubule alignment in elongating cells , 1998, Plant physiology.

[17]  V. Lozovaya,et al.  The effect of exposure to microgravity on the development and structural organisation of plant protoplasts flown on Biokosmos 9. , 1992, Physiologia plantarum.

[18]  R. Moore How effectively does a clinostat mimic the ultrastructural effects of microgravity on plant cells? , 1990, Annals of botany.

[19]  T. Wakasugi,et al.  Hypergravity stimulus enhances primary xylem development and decreases mechanical properties of secondary cell walls in inflorescence stems of Arabidopsis thaliana. , 2006, Annals of botany.

[20]  G. Aronne,et al.  The effect of uni-axial clinostat rotation on germination and root anatomy of Phaseolus vulgaris L. , 2003 .

[21]  J. Cowles,et al.  Growth and lignification in seedlings exposed to eight days of microgravity. , 1984, Annals of botany.

[22]  T. P. O’brien,et al.  PLANT MICROTECHNIQUE: SOME PRINCIPLES AND NEW METHODS , 1968 .

[23]  C. Haigler,et al.  Dispersed lignin in tracheary elements treated with cellulose synthesis inhibitors provides evidence that molecules of the secondary cell wall mediate wall patterning , 1992 .

[24]  A. Kylin,et al.  The effect of 8 days of microgravity on regeneration of intact plants from protoplasts , 1994 .

[25]  V. Micco Effect of Simulated Microgravity on Seedling Development and Vascular Differentiation of Soy , 2003 .

[26]  G. Aronne,et al.  Biometric anatomy of seedlings developed onboard of Foton-M2 in an automatic system supporting growth , 2006 .

[27]  E. Nedukha Possible mechanisms of plant cell wall changes at microgravity. , 1996, Advances in space research : the official journal of the Committee on Space Research.

[28]  T Hoson,et al.  Plant responses to simulated microgravity. , 1994, Advances in space biology and medicine.

[29]  C. Haigler,et al.  Roles of microtubules and cellulose microfibril assembly in the localization of secondary-cell-wall deposition in developing tracheary elements , 2004, Protoplasma.

[30]  Y. Barrière,et al.  Down-regulation of the AtCCR1 gene in Arabidopsis thaliana: effects on phenotype, lignins and cell wall degradability , 2003, Planta.

[31]  L. Schreiber,et al.  Effects of hypergravity conditions on elongation growth and lignin formation in the inflorescence stem of Arabidopsis thaliana , 2006, Journal of Plant Research.

[32]  Katherine Esau Anatomy of Seed Plants , 1960 .

[33]  T. Hoson,et al.  Growth and cell wall changes in rice roots during spaceflight , 2003, Plant and Soil.

[34]  T. Hoson,et al.  Stimulation of elongation growth and xyloglucan breakdown in Arabidopsis hypocotyls under microgravity conditions in space , 2002, Planta.

[35]  K. Nishitani,et al.  Effects of hypergravity on growth and cell wall properties of cress hypocotyls. , 1996, Journal of experimental botany.

[36]  D. Goring,et al.  ultrastructural arrangement of the wood cell wall , 1975 .

[37]  R. Brown,et al.  Gravity effects on cellulose assembly. , 1992, American journal of botany.

[38]  P. Harris,et al.  Atomic force microscopy of microfibrils in primary cell walls , 2003, Planta.

[39]  V. Lozovaya,et al.  The effect of microgravity on the development of plant protoplasts flown on Biokosmos 9. , 1992, Advances in space research : the official journal of the Committee on Space Research.

[40]  M. Yamada,et al.  Effects of hypergravity on the elongation growth in radish and cucumber hypocotyls , 1995, Journal of Plant Research.

[41]  T. Hoson Apoplast as the site of response to environmental signals , 1998, Journal of Plant Research.

[42]  Yukiko Nakamura,et al.  Stimulation of elongation growth and cell wall loosening in rice coleoptiles under microgravity conditions in space. , 2002, Plant & cell physiology.

[43]  T. Hoson,et al.  Hypergravity induces reorientation of cortical microtubules and modifies growth anisotropy in azuki bean epicotyls , 2006, Planta.

[44]  K. Ruel,et al.  Lamellation in the S2 layer of softwood tracheids as demonstrated by scanning transmission electron microscopy , 1978, Wood Science and Technology.

[45]  T. Iversen,et al.  Simulated weightlessness and hyper-g results in opposite effects on the regeneration of the cortical microtubule array in protoplasts from Brassica napus hypocotyls. , 1999, Physiologia plantarum.

[46]  A. P. Singh,et al.  Bridge-Like Structures Between Cellulose Microfibrils in Radiata Pine (Pinus radiata D. Don) Kraft Pulp and Holocellulose , 1998 .

[47]  L. Sieburth,et al.  Auxin is required for leaf vein pattern in Arabidopsis. , 1999, Plant physiology.