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Tytuł pozycji:

Light signals counteract alterations caused by simulated microgravity in proliferating plant cells.

Tytuł:
Light signals counteract alterations caused by simulated microgravity in proliferating plant cells.
Autorzy:
Manzano A; Centro de Investigaciones Biológicas Margarita Salas - CSIC, Ramiro de Maeztu 9, Madrid, 28040, Spain.
Pereda-Loth V; GSBMS/AMIS, Université Paul Sabatier Toulouse III, Toulouse, France.
de Bures A; CNRS, Laboratoire Génome et Développement des Plantes (LGDP), UMR 5096, Perpignan, 66860, France.; Université de Perpignan Via Domitia, LGDP, UMR 5096, Perpignan, 66860, France.
Sáez-Vásquez J; CNRS, Laboratoire Génome et Développement des Plantes (LGDP), UMR 5096, Perpignan, 66860, France.; Université de Perpignan Via Domitia, LGDP, UMR 5096, Perpignan, 66860, France.
Herranz R; Centro de Investigaciones Biológicas Margarita Salas - CSIC, Ramiro de Maeztu 9, Madrid, 28040, Spain.
Medina FJ; Centro de Investigaciones Biológicas Margarita Salas - CSIC, Ramiro de Maeztu 9, Madrid, 28040, Spain.
Źródło:
American journal of botany [Am J Bot] 2021 Sep; Vol. 108 (9), pp. 1775-1792. Date of Electronic Publication: 2021 Sep 15.
Typ publikacji:
Journal Article; Research Support, Non-U.S. Gov't
Język:
English
Imprint Name(s):
Publication: <2018-> : [Philadelphia, PA] : Wiley
Original Publication: Baltimore Md : Botanical Society Of America
MeSH Terms:
Arabidopsis*/genetics
Space Flight*
Weightlessness*
Meristem ; Plant Cells ; Plant Roots ; Seedlings
References:
Baserga, R. 2007. Is cell size important? Cell Cycle 6: 814-816.
Beemster, G. T. S., and T. I. Baskin. 1998. Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiology 116: 1515-1526.
Bernstein, K. A., F. Bleichert, J. M. Bean, F. R. Cross, and S. J. Baserga. 2007. Ribosome biogenesis is sensed at the start cell cycle checkpoint. Molecular Biology of the Cell 18: 953-964.
Blilou, I., J. Xu, M. Wildwater, V. Willemsen, I. A. Paponov, J. Friml, R. Heidstra, et al. 2005. The PIN efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433: 39-44.
Borst, A. G., and J. J. W. A. van Loon. 2009. Technology and developments for the Random Positioning Machine, RPM. Microgravity Science and Technology 21: 287-292. http://doi.org/10.1007/s12217-008-9043-2.
Boucheron-Dubuisson, E., A. I. Manzano, I. Le Disquet, I. Matía, J. Sáez-Vasquez, J. J. W. A. van Loon, R. Herranz, et al. 2016. Functional alterations of root meristematic cells of Arabidopsis thaliana induced by a simulated microgravity environment. Journal of Plant Physiology 207: 30-41.
Brunoud, G., D. M. Wells, M. Oliva, A. Larrieu, V. Mirabet, A. H. Burrow, T. Beeckman, et al. 2012. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482: 103-106.
Caldana, C., Y. Li, A. Leisse, Y. Zhang, L. Bartholomaeus, A. R. Fernie, L. Willmitzer, and P. Giavalisco. 2013. Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant Journal 73: 897-909.
Califar, B., N. J. Sng, A. Zupanska, A.-L. Paul, and R. J. Ferl. 2020. Root skewing-associated genes impact the spaceflight response of Arabidopsis thaliana. Frontiers in Plant Science 11: 239.
Christie, J. M., and A. S. Murphy. 2013. Shoot phototropism in higher plants: new light through old concepts. American Journal of Botany 100: 35-46.
Colon-Carmona, A., R. You, T. Haimovitch-Gal, and P. Doerner. 1999. Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant Journal 20: 503-508. http://doi.org/10.1046/j.1365-313x.1999.00620.x.
Comella, P., F. Pontvianne, S. Lahmy, F. Vignols, N. Barbezier, A. DeBures, E. Jobet, et al. 2008. Characterization of a ribonuclease III-like protein required for cleavage of the pre-rRNA in the 3'ETS in Arabidopsis. Nucleic Acids Research 36: 1163-1175.
De Micco, V., S. De Pascale, R. Paradiso, and G. Aronne. 2014. Microgravity effects on different stages of higher plant life cycle and completion of the seed-to-seed cycle. Plant Biology 16: 31-38.
Driss-Ecole, D., V. Legué, E. Carnero-Diaz, and G. Perbal. 2008. Gravisensitivity and automorphogenesis of lentil seedling roots grown on board the International Space Station. Physiologia Plantarum 134: 191-201.
Durut, N., M. Abou-Ellail, P. Comella, E. Jobet, A. de Bures & J. Sáez-Vásquez. 2019. NUCLEOLIN: similar and antagonistic roles in Arabidopsis thaliana. In 26th European Low Gravity Research Association Biennial Symposium and General Assembly, Book of abstracts, 150, Granada, Spain. Website: https://www.elgra.org/wp-content/uploads/2020/06/ELGRA2019-Book-of-abstracts.pdf.
Durut, N., M. Abou-Ellail, F. Pontvianne, S. Das, H. Kojima, S. Ukai, A. de Bures, et al. 2014. A duplicated NUCLEOLIN gene with antagonistic activity is required for chromatin organization of silent 45S rDNA in Arabidopsis. Plant Cell 26: 1330-1344.
Durut, N., and J. Sáez-Vásquez. 2015. Nucleolin: dual roles in rDNA chromatin transcription. Gene 556: 7-12.
Ferl, R. J., and A.-L. Paul. 2016. The effect of spaceflight on the gravity-sensing auxin gradient of roots: GFP reporter gene microscopy on orbit. npj Microgravity 2: 15023.
Ferreira, P., A. S. Hemerly, J. De Almeida Engler, C. Bergounioux, S. Burssens, M. Van Montagu, G. Engler, and D. Inzé. 1994. Three discrete classes of Arabidopsis cyclins are expressed during different intervals of the cell cycle. Proceedings of the National Academy of Sciences, USA 91: 11313-11317.
Herranz, R., R. Anken, J. Boonstra, M. Braun, P. C. M. Christianen, M. de Geest, J. Hauslage, et al. 2013. Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology 13: 1-17.
Hoson, T., K. Soga, K. Wakabayashi, S. Kamisaka, and E. Tanimoto. 2003. Growth and cell wall changes in rice roots during spaceflight. Plant and Soil 255: 19-26.
Janda, T., É. Hideg, and R. Vanková. 2020. The role of light in abiotic stress acclimation. Frontiers in Plant Science 11: 184.
Kamal, K. Y., R. Herranz, J. J. W. A. van Loon, and F. J. Medina. 2018. Simulated microgravity, Mars gravity, and 2g hypergravity affect cell cycle regulation, ribosome biogenesis, and epigenetics in Arabidopsis cell cultures. Scientific Reports 8: 6424.
Kruse, C. P. S., A. D. Meyers, P. Basu, S. Hutchinson, D. R. Luesse, and S. E. Wyatt. 2020. Spaceflight induces novel regulatory responses in Arabidopsis seedling as revealed by combined proteomic and transcriptomic analyses. BMC Plant Biology 20: 237.
Link, B. M., J. S. Busse, and B. Stankovic. 2014. Seed-to-seed-to-seed growth and development of Arabidopsis in microgravity. Astrobiology 14: 866-875.
Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25: 402-408.
López-Juez, E., E. Dillon, Z. Magyar, S. Khan, S. Hazeldine, S. M. de Jager, J. A. H. Murray, et al. 2008. Distinct light-initiated gene expression and cell cycle programs in the shoot apex and cotyledons of Arabidopsis. Plant Cell 20: 947-968.
Manzano A. I., R. Herranz, A. Manzano, and J. J. W. A. van Loon. 2016. Early effects of altered gravity environments on plant cell growth and cell proliferation: characterization of morphofunctional nucleolar types in an Arabidopsis cell culture system. Frontiers in Astronomy and Space Sciences 3. http://doi.org/10.3389/fspas.2016.00002.
Manzano, A. I., O. Larkin, C. Dijkstra, P. Anthony, M. Davey, L. Eaves, R. Hill, et al. 2013. Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings. BMC Plant Biology 13: 124.
Manzano, A. I., I. Matía, F. González-Camacho, E. Carnero-Diaz, J. J. W. A. van Loon, C. Dijkstra, O. Larkin, P. Anthony, M. R. Davey, R. Marco, and F. J. Medina. 2009. Germination of Arabidopsis seed in space and in simulated microgravity: alterations in root cell growth and proliferation. Microgravity Science and Technology 21: 293-297.
Manzano, A., A. Villacampa, J. Sáez-Vásquez, J. Z. Kiss, F. J. Medina, and R. Herranz. 2020. The importance of Earth reference controls in spaceflight -omics research: characterization of nucleolin mutants from the seedling growth experiments. iScience 23: 101686.
Manzano, A., V. Pereda-Loth, A. de Bures, J. Sáez-Vásquez, R. Herranz, and F. J. Medina. 2021. Data from: Light signals counteract alterations caused by simulated microgravity in proliferating plant cells. Dryad Digital Repository. https://doi.org/10.5061/dryad.63xsj3v2.
Massa, G. D., G. Newsham, M. E. Hummerick, J. L. Caro, G. W. Stutte, R. C. Morrow, and R. M. Wheeler. 2013. Preliminary species and media selection for the Veggie space hardware. Gravitational and Space Research 1: 95-106.
Matía, I., F. González-Camacho, R. Herranz, J. Z. Kiss, G. Gasset, J. J. W. A. van Loon, R. Marco, and F. J. Medina. 2010. Plant cell proliferation and growth are altered by microgravity conditions in spaceflight. Journal of Plant Physiology 167: 184-193.
Matía, I., J. W. A. van Loon, E. Carnero-Diaz, R. Marco, and F. J. Medina. 2009. Seed germination and seedling growth under simulated microgravity causes alterations in plant cell proliferation and ribosome biogenesis. Microgravity Science and Technology 21: 169-174.
Medina, F. J., A. Cerdido, and G. De Cárcer. 2000. The functional organization of the nucleolus in proliferating plant cells. European Journal of Histochemistry 44: 117-131.
Medina, F. J., F. González-Camacho, A. I. Manzano, A. Manrique, and R. Herranz. 2010. Nucleolin, a major conserved multifunctional nucleolar phosphoprotein of proliferating cells. Journal of Applied Biomedicine 8: 141-150.
Millar, K. D., C. M. Johnson, R. E. Edelmann, and J. Z. Kiss. 2011. An endogenous growth pattern of roots is revealed in seedlings grown in microgravity. Astrobiology 11: 787-797.
Mizukami, Y. 2001. A matter of size: developmental control of organ size in plants. Current Opinion in Plant Biology 4: 533-539.
Mohammed, B., S. F. Bilooei, R. Dóczi, E. Grove, S. Railo, K. Palme, F. A. Ditengou, et al. 2018. Converging light, energy and hormonal signaling control meristem activity, leaf initiation, and growth. Plant Physiology 176: 1365-1381.
Molas, M. L., and J. Z. Kiss. 2009. Phototropism and gravitropism in plants. Advances in Botanical Research 49: 1-34.
Mongelard, F., and P. Bouvet. 2007. Nucleolin: a multiFACeTed protein. Trends in Cell Biology 17: 80-86.
Musielak, T. J., L. Schenkel, M. Kolb, A. Henschen, and M. Bayer. 2015. A simple and versatile cell wall staining protocol to study plant reproduction. Plant Reproduction 28: 161-169.
Nakashima, J., F. Liao, J. A. Sparks, Y. Tang, and E. B. Blancaflor. 2014. The actin cytoskeleton is a suppressor of the endogenous skewing behaviour of Arabidopsis primary roots in microgravity. Plant Biology 16: 142-150.
Ottenschlager, I., P. Wolff, C. Wolverton, R. P. Bhalerao, G. Sandberg, H. Ishikawa, M. Evans, and K. Palme. 2003. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proceedings of the National Academy of Sciences, USA 100: 2987-2991.
Paul, A.-L., C. Amalfitano, and R. Ferl. 2012. Plant growth strategies are remodeled by spaceflight. BMC Plant Biology 12: 232.
Paul, A.-L., N. J. Sng, A. K. Zupanska, A. Krishnamurthy, E. R. Schultz, and R. J. Ferl. 2017. Genetic dissection of the Arabidopsis spaceflight transcriptome: Are some responses dispensable for the physiological adaptation of plants to spaceflight? PLoS One 12: e0180186.
Perrot-Rechenmann, C. 2010. Cellular responses to auxin: division versus expansion. Cold Spring Harbor Perspectives in Biology 2: a001446.
Pontvianne, F., M. Abou-Ellail, J. Douet, P. Comella, I. Matia, C. Chandrasekhara, A. DeBures, et al. 2010. Nucleolin is required for DNA methylation state and the expression of rRNA gene variants in Arabidopsis thaliana. PLoS Genetics 6: e1001225.
Pontvianne, F., I. Matía, J. Douet, S. Tourmente, F. J. Medina, M. Echeverría, and J. Sáez-Vasquez. 2007. Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Molecular Biology of the Cell 18: 369-379.
Pound, M. P., A. P. French, D. M. Wells, M. J. Bennett, and T. P. Pridmore. 2012. CellSeT: novel software to extract and analyze structured networks of plant cells from confocal images. Plant Cell 24: 1353-1361.
Roy, R., and D. C. Bassham. 2014. Root growth movements: waving and skewing. Plant Science 221-222: 42-47.
Sablowski, R., and M. Carnier Dornelas. 2014. Interplay between cell growth and cell cycle in plants. Journal of Experimental Botany 65: 2703-2714.
Sáez-Vásquez, J., D. Caparros-Ruiz, F. Barneche, and M. Echeverría. 2004. A plant snoRNP complex containing snoRNAs, fibrillarin, and nucleolin-like proteins is competent for both rRNA gene binding and pre-rRNA processing in vitro. Molecular and Cellular Biology 24: 7284-7297.
Sáez-Vásquez, J., and F. J. Medina. 2008. The plant nucleolus. In J. C. Kader and M. Delseny [eds.], Advances in botanical research Vol. 47, 1-46. Elsevier, San Diego, CA, USA.
Scheres, B., P. Benfey, and L. Dolan. 2002. Root development. The Arabidopsis book 1: e0101. http://doi.org/10.1199/tab.0101.
Schultz, E. R., A.-L. Paul, and R. J. Ferl. 2016. Root growth patterns and morphometric change based on the growth media. Microgravity Science and Technology 28: 621-631.
Silva-Navas, J., M. A. Moreno-Risueño, C. Manzano, B. Téllez-Robledo, S. Navarro-Neila, V. Carrasco, S. Pollmann, et al. 2016. Flavonols mediate root phototropism and growth through regulation of proliferation-to-differentiation transition. Plant Cell 28: 1372-1387.
Swarup, R., J. Friml, A. Marchant, K. Ljung, G. Sandberg, K. Palme, and M. Bennett. 2001. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes & Development 15: 2648-2653.
Ueda, J., K. Miyamoto, E. Uheda, M. Oka, S. Yano, A. Higashibata, and N. Ishioka. 2014. Close relationships between polar auxin transport and graviresponse in plants. Plant Biology 16: 43-49.
Valbuena, M. A., A. Manzano, J. P. Vandenbrink, V. Pereda-Loth, E. Carnero-Diaz, R. E. Edelmann, J. Z. Kiss, et al. 2018. The combined effects of real or simulated microgravity and red-light photoactivation on plant root meristematic cells. Planta 248: 691-704.
Vandenbrink, J. P., J. Z. Kiss, R. Herranz, and F. J. Medina. 2014. Light and gravity signals synergize in modulating plant development. Frontiers in Plant Science 5: 563.
Weis, B. L., J. Kovacevic, S. Missbach, and E. Schleiff. 2015. Plant-specific features of ribosome biogenesis. Trends in Plant Science 20: 729-740.
Xiong, Y., M. McCormack, L. Li, Q. Hall, C. Xiang, and J. Sheen. 2013. Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496: 181-186.
Yang, P., Q. Wen, R. Yu, X. Han, X. W. Deng, and H. Chen. 2020. Light modulates the gravitropic responses through organ-specific PIFs and HY5 regulation of LAZY4 expression in Arabidopsis. Proceedings of the National Academy of Sciences, USA 117: 18840-18848.
Yang, X., B. Wang, B. Farris, G. Clark, and S. J. Roux. 2015. Modulation of root skewing in Arabidopsis by apyrases and extracellular ATP. Plant and Cell Physiology 56: 2197-2206.
Contributed Indexing:
Keywords: abiotic stress; auxin transport; cell cycle; graviresponse; nucleolin; ribosome biogenesis; root meristem; space plant biology
Entry Date(s):
Date Created: 20210915 Date Completed: 20211018 Latest Revision: 20211018
Update Code:
20240105
DOI:
10.1002/ajb2.1728
PMID:
34524692
Czasopismo naukowe
Premise: Light and gravity are fundamental cues for plant development. Our understanding of the effects of light stimuli on plants in space, without gravity, is key to providing conditions for plants to acclimate to the environment. Here we tested the hypothesis that the alterations caused by the absence of gravity in root meristematic cells can be counteracted by light.
Methods: Seedlings of wild-type Arabidopsis thaliana and two mutants of the essential nucleolar protein nucleolin (nuc1, nuc2) were grown in simulated microgravity, either under a white light photoperiod or under continuous darkness. Key variables of cell proliferation (cell cycle regulation), cell growth (ribosome biogenesis), and auxin transport were measured in the root meristem using in situ cellular markers and transcriptomic methods and compared with those of a 1 g control.
Results: The incorporation of a photoperiod regime was sufficient to attenuate or suppress the effects caused by gravitational stress at the cellular level in the root meristem. In all cases, values for variables recorded from samples receiving light stimuli in simulated microgravity were closer to values from the controls than values from samples grown in darkness. Differential sensitivities were obtained for the two nucleolin mutants.
Conclusions: Light signals may totally or partially replace gravity signals, significantly improving plant growth and development in microgravity. Despite that, molecular alterations are still compatible with the expected acclimation mechanisms, which need to be better understood. The differential sensitivity of nuc1 and nuc2 mutants to gravitational stress points to new strategies to produce more resilient plants to travel with humans in new extraterrestrial endeavors.
(© 2021 The Authors. American Journal of Botany published by Wiley Periodicals LLC on behalf of Botanical Society of America.)

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