Abstract
Any space exploration initiative, such as the human presence in the Moon and Mars, must incorporate plants for life support. To enable space plant culture we need to understand how plants respond to extraterrestrial conditions, adapt to them, and compensate their deleterious effects at multiple levels. Gravity is a major difference between the terrestrial and the extraterrestrial environment. Gravitropism is the process of establishing a growth direction for plant organs according to the gravity vector. Gravity signals are sensed at specialized tissues by the motion of amyloplasts called statoliths and transduced to produce a cellular polarization capable of influencing the transport of auxin. Gravity alterations eventually result in changes in the lateral balance of auxin in the root, producing deviations of the growth direction. Under microgravity, auxin changes affect the root meristem causing increased cell proliferation and decreased cell growth. The nucleolus, the nuclear site of production of ribosomes, is a marker of this unbalance, which could alter plant development. At the molecular level, microgravity induces a reprogramming of gene expression that mostly affects plant defense systems against abiotic stresses, indicating that these categories of genes are involved in the adaptation to extraterrestrial habitats. Nevertheless, no specific genes for plant response to gravitational stress have been identified. Despite this stress, plants survive, develo** until the adult stage and reproducing under microgravity conditions. A major research challenge is to identify environmental factors, such as light, which could interact, modulate, or balance the impact of gravity, contributing to the tolerance and survival of plants under spaceflight conditions. Understanding the crosstalk between light and gravity sensing will contribute to the success of the next generation agriculture in human settlements outside the Earth.
Communicated by Maria-Carmen Risueño
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Afshinnekoo E, Scott RT, MacKay MJ, Pariset E, Cekanaviciute E, Barker R, Gilroy S, Hassane D, Smith SM, Zwart SR, Nelman-Gonzalez M, Crucian BE, Ponomarev SA, Orlov OI, Shiba D, Muratani M, Yamamoto M, Richards SE, Vaishampayan PA, Meydan C, Foox J, Myrrhe J, Istasse E, Singh N, Venkateswaran K, Keune JA, Ray HE, Basner M, Miller J, Vitaterna MH, Taylor DM, Wallace D, Rubins K, Bailey SM, Grabham P, Costes SV, Mason CE, Beheshti A (2020) Fundamental biological features of spaceflight: advancing the field to enable deep-space exploration. Cell 183(5):1162–1184. https://doi.org/10.1016/j.cell.2020.10.050
Baldwin KL, Strohm AK, Masson PH (2013) Gravity sensing and signal transduction in vascular plant primary roots. Am J Bot 100(1):126–142. https://doi.org/10.3732/ajb.1200318
Barjaktarovic Z, Schutz W, Madlung J, Fladerer C, Nordheim A, Hampp R (2009) Changes in the effective gravitational field strength affect the state of phosphorylation of stress-related proteins in callus cultures of Arabidopsis thaliana. J Exp Bot 60:779–789. https://doi.org/10.1093/jxb/ern324
Barker R, Lombardino J, Rasmussen K, Gilroy S (2020) Test of Arabidopsis space transcriptome: a discovery environment to explore multiple plant biology spaceflight experiments. Front Plant Sci 11(147). https://doi.org/10.3389/fpls.2020.00147
Baserga R (2007) Is cell size important? Cell Cycle 6(7):814–816. https://doi.org/10.4161/cc.6.7.4049
Bennett MJ, Marchant A, Green HG, May ST, Ward SP, Millner PA, Walker AR, Schulz B, Feldmann KA (1996) Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273(5277):948–950. https://doi.org/10.1126/science.273.5277.948
Bernstein KA, Baserga SJ (2004) The small subunit processome is required for cell cycle progression at G1. Mol Biol Cell 15(11):5038–5046. https://doi.org/10.1091/mbc.E04-06-0515
Bernstein KA, Bleichert F, Bean JM, Cross FR, Baserga SJ (2007) Ribosome biogenesis is sensed at the start cell cycle checkpoint. Mol Biol Cell 18(3):953–964. https://doi.org/10.1091/mbc.E06-06-0512
Bérut A, Chauvet H, Legué V, Moulia B, Pouliquen O, Forterre Y (2018) Gravisensors in plant cells behave like an active granular liquid. Proc Natl Acad Sci U S A 115(20):5123–5128. https://doi.org/10.1073/pnas.1801895115
Blancaflor EB (2013) Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am J Bot 100(1):143–152. https://doi.org/10.3732/ajb.1200283
Boucheron-Dubuisson E, Manzano AI, Le Disquet I, Matía I, Sáez-Vasquez J, van Loon JJWA, Herranz R, Carnero-Diaz E, Medina FJ (2016) Functional alterations of root meristematic cells of Arabidopsis thaliana induced by a simulated microgravity environment. J Plant Physiol 207:30–41. https://doi.org/10.1016/j.jplph.2016.09.011
Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI (2010) The nucleolus under stress. Mol Cell 40(2):216–227. https://doi.org/10.1016/j.molcel.2010.09.024
Briggs WR (2014) Phototropism: some history, some puzzles, and a look ahead. Plant Physiol 164(1):13–23. https://doi.org/10.1104/pp.113.230573
Brinckmann E (2005) ESA hardware for plant research on the international space station. Adv Space Res 36(7):1162–1166. https://doi.org/10.1016/j.asr.2005.02.019
Califar B, Sng NJ, Zupanska A, Paul A-L, Ferl RJ (2020) Root skewing-associated genes impact the spaceflight response of Arabidopsis thaliana. Front Plant Sci 11(239). https://doi.org/10.3389/fpls.2020.00239
Choi W-G, Barker RJ, Kim S-H, Swanson SJ, Gilroy S (2019) Variation in the transcriptome of different ecotypes of Arabidopsis thaliana reveals signatures of oxidative stress in plant responses to spaceflight. Am J Bot 106(1):123–136. https://doi.org/10.1002/ajb2.1223
Correll MJ, Pyle TP, Millar KDL, Sun Y, Yao J, Edelmann RE, Kiss JZ (2013) Transcriptome analyses of Arabidopsis thaliana seedlings grown in space: implications for gravity-responsive genes. Planta:1–15. https://doi.org/10.1007/s00425-013-1909-x
Darbelley N, Driss-École D, Perbal G (1986) Différentiation et proliferation dans des racines de maïs cultivé en microgravité (Biocosmos 1985). Adv Space Res 6(12):157–160. https://doi.org/10.1016/0273-1177(86)90080-3
Doerner P (2008) Transcriptional control of the plant cell cycle. In: Verma D, Hong Z (eds) Cell division control in plants, Plant cell monographs, vol 9. Springer, Berlin, pp 13–32. https://doi.org/10.1007/7089_2007_120
Driss-École D, Schoevaert D, Noin M, Perbal G (1994) Densitometric analysis of nuclear DNA content in lentil roots grown in space. Biol Cell 81(1):59–64. https://doi.org/10.1016/0248-4900(94)90055-8
Driss-École D, Jeune B, Prouteau M, Julianus P, Perbal G (2000) Lentil root statoliths reach a stable state in microgravity. Planta 211:396–405. https://doi.org/10.1007/s004250000298
Driss-Ecole D, Legué V, Carnero-Diaz E, Perbal G (2008) Gravisensitivity and automorphogenesis of lentil seedling roots grown on board the international space station. Physiol Plantarum 134(1):191–201. https://doi.org/10.1111/j.1399-3054.2008.01121.x
Durut N, Sáez-Vásquez J (2015) Nucleolin: dual roles in rDNA chromatin transcription. Gene 556(1):7–12. https://doi.org/10.1016/j.gene.2014.09.023
Durut N, Abou-Ellail M, Pontvianne F, Das S, Kojima H, Ukai S, de Bures A, Comella P, Nidelet S, Rialle S, Merret R, Echeverria M, Bouvet P, Nakamura K, Sáez-Vásquez J (2014) A duplicated NUCLEOLIN gene with antagonistic activity is required for chromatin organization of silent 45S rDNA in Arabidopsis. Plant Cell 26(3):1330–1344. https://doi.org/10.1105/tpc.114.123893
Durut N, Abou-Ellail M, Comella P, Jobet E, de Bures A, Sáez-Vásquez J (2019) NUCLEOLIN: similar and antagonistic roles in arabidopsis thaliana. In: 26th European low gravity research association biennial symposium and general assembly. https://www.elgra.org/wp-content/uploads/2020/06/ELGRA2019-Book-of-abstracts.pdf. p 150, Granada (Spain)
Fengler S, Spirer I, Neef M, Ecke M, Nieselt K, Hampp R (2015) A whole-genome microarray study of Arabidopsis thaliana semisolid callus cultures exposed to microgravity and nonmicrogravity related spaceflight conditions for 5 days on board of Shenzhou 8. Biomed Res Int. 547495, 15 p. https://doi.org/10.1155/2015/547495
Ferl RJ, Paul A-L (2016) The effect of spaceflight on the gravity-sensing auxin gradient of roots: GFP reporter gene microscopy on orbit. NPJ Microgravity 2:15023. https://doi.org/10.1038/npjmgrav.2015.23
Ferl RJ, Koh J, Denison F, Paul A-L (2015) Spaceflight induces specific alterations in the proteomes of Arabidopsis. Astrobiology 15(1):32–56. https://doi.org/10.1089/ast.2014.1210
Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002) Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415(6873):806–809. https://doi.org/10.1038/415806a
Furutani M, Hirano Y, Nishimura T, Nakamura M, Taniguchi M, Suzuki K, Oshida R, Kondo C, Sun S, Kato K, Fukao Y, Hakoshima T, Morita MT (2020) Polar recruitment of RLD by LAZY1-like protein during gravity signaling in root branch angle control. Nat Commun 11(1):76. https://doi.org/10.1038/s41467-019-13729-7
Gadalla DS, Braun M, Böhmer M (2018) Gravitropism in higher plants: cellular aspects. In: Ruyters G, Braun M (eds) Gravitational biology I: gravity sensing and graviorientation in microorganisms and plants. Springer, Cham, pp 75–92. https://doi.org/10.1007/978-3-319-93894-3_6
Ginisty H, Sicard H, Roger B, Bouvet P (1999) Structure and functions of nucleolin. J Cell Sci 112:761–772
González-Camacho F, Medina FJ (2006) The nucleolar structure and the activity of NopA100, a nucleolin-like protein, during the cell cycle in proliferating plant cells. Histochem Cell Biol 125(1–2):139–153. https://doi.org/10.1007/s00418-005-0081-1
Guo M, Liu J-H, Ma X, Luo D-X, Gong Z-H, Lu M-H (2016) The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 7(114). https://doi.org/10.3389/fpls.2016.00114
Herranz R, Medina FJ (2014) Cell proliferation and plant development under novel altered gravity environments. Plant Biol 16:23–30. https://doi.org/10.1111/plb.12103
Herranz R, Valbuena MA, Youssef K, Medina FJ (2014) Mechanisms of disruption of meristematic competence by microgravity in Arabidopsis seedlings. Plant Signal Behav 9(2):e28289. https://doi.org/10.4161/psb.28289
Herranz R, Vandenbrink JP, Villacampa A, Manzano A, Poehlman WL, Feltus FA, Kiss JZ, Medina FJ (2019) RNAseq analysis of the response of Arabidopsis thaliana to fractional gravity under blue-light stimulation during spaceflight. Front Plant Sci 10(1529). https://doi.org/10.3389/fpls.2019.01529
Hoson T, Soga K (2003) New aspects of gravity responses in plant cells. In: International review of cytology, vol 229. Academic, pp 209–244. https://doi.org/10.1016/S0074-7696(03)29005-7
Hoson T, Soga K, Wakabayashi K, Kamisaka S, Tanimoto E (2003) Growth and cell wall changes in rice roots during spaceflight. Plant Soil 255(1):19–26. https://doi.org/10.1023/A:1026105431505
Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40(1):77–105. https://doi.org/10.1146/annurev.genet.40.110405.090431
Johnson CM, Subramanian A, Pattathil S, Correll MJ, Kiss JZ (2017) Comparative transcriptomics indicate changes in cell wall organization and stress response in seedlings during spaceflight. Am J Bot 104(8):1219–1231. https://doi.org/10.3732/ajb.1700079
Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakano A, Wada M (2009) Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci U S A 106(31):13106–13111. https://doi.org/10.1073/pnas.0906250106
Kalinina NO, Makarova S, Makhotenko A, Love AJ, Taliansky M (2018) The multiple functions of the nucleolus in plant development, disease and stress responses. Front Plant Sci 9(132). https://doi.org/10.3389/fpls.2018.00132
Kamal KY, Herranz R, van Loon JJWA, Medina FJ (2018) Simulated microgravity, Mars gravity, and 2g hypergravity affect cell cycle regulation, ribosome biogenesis, and epigenetics in Arabidopsis cell cultures. Sci Rep 8(1):6424. https://doi.org/10.1038/s41598-018-24942-7
Kamal KY, Herranz R, van Loon JJWA, Medina FJ (2019a) Cell cycle acceleration and changes in essential nuclear functions induced by simulated microgravity in a synchronized Arabidopsis cell culture. Plant Cell Environ 42(2):480–494. https://doi.org/10.1111/pce.13422
Kamal KY, van Loon JJWA, Medina FJ, Herranz R (2019b) Differential transcriptional profile through cell cycle progression in Arabidopsis cultures under simulated microgravity. Genomics 111(6):1956–1965. https://doi.org/10.1016/j.ygeno.2019.01.007
Kiss JZ, Kumar P, Millar KDL, Edelmann RE, Correll MJ (2009) Operations of a spaceflight experiment to investigate plant tropisms. Adv Space Res 44(8):879–886. https://doi.org/10.1016/j.asr.2009.06.007
Korver RA, Koevoets IT, Testerink C (2018) Out of shape during stress: a key role for auxin. Trends Plant Sci 23(9):783–793. https://doi.org/10.1016/j.tplants.2018.05.011
Kraft TFB, van Loon JJWA, Kiss JZ (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-position machine. Planta 211:415–422. https://doi.org/10.1007/s004250000302
Kruse CPS, Meyers AD, Basu P, Hutchinson S, Luesse DR, Wyatt SE (2020) Spaceflight induces novel regulatory responses in Arabidopsis seedling as revealed by combined proteomic and transcriptomic analyses. BMC Plant Biol 20(1):237. https://doi.org/10.1186/s12870-020-02392-6
Kwon T, Sparks JA, Nakashima J, Allen SN, Tang Y, Blancaflor EB (2015) Transcriptional response of Arabidopsis seedlings during spaceflight reveals peroxidase and cell wall remodeling genes associated with root hair development. Am J Bot 102(1):21–35. https://doi.org/10.3732/ajb.1400458
Legué V, Yu F, Driss-École D, Perbal G (1996) Effects of gravitropic stress on the development of the primary root of lentil seedlings grown in space. J Biotechnol 47(2–3):129–135. https://doi.org/10.1016/0168-1656(96)01356-9
Leitz G, Kang B-H, Schoenwaelder MEA, Staehelin LA (2009) Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing arabidopsis columella cells. Plant Cell 21(3):843–860. https://doi.org/10.1105/tpc.108.065052
Link BM, Busse JS, Stankovic B (2014) Seed-to-seed-to-seed growth and development of arabidopsis in microgravity. Astrobiology 14(10):866–875. https://doi.org/10.1089/ast.2014.1184
Madrigal P, Gabel A, Villacampa A, Manzano A, Deane CS, Bezdan D, Carnero-Diaz E, Medina FJ, Hardiman G, Grosse I, Szewczyk N, Weging S, Giacomello S, Harridge SDR, Morris-Paterson T, Cahill T, da Silveira WA, Herranz R (2020) Revam** space-omics in Europe. Cell Syst. https://doi.org/10.1016/j.cels.2020.10.006
Manzano AI, van Loon JJWA, Christianen PCM, Gonzalez-Rubio JM, Medina FJ, Herranz R (2012) Gravitational and magnetic field variations synergize to cause subtle variations in the global transcriptional state of Arabidopsis in vitro callus cultures. BMC Genomics 13(1):105. https://doi.org/10.1186/1471-2164-13-105
Manzano AI, Larkin O, Dijkstra C, Anthony P, Davey M, Eaves L, Hill R, Herranz R, Medina FJ (2013) Meristematic cell proliferation and ribosome biogenesis are decoupled in diamagnetically levitated Arabidopsis seedlings. BMC Plant Biol 13(1):124. https://doi.org/10.1186/1471-2229-13-124
Manzano AI, Herranz R, Manzano A, Van Loon JJWA, Medina FJ (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. Front Astron Space Sci 3. https://doi.org/10.3389/fspas.2016.00002
Manzano A, Creus E, Tomás A, Valbuena MA, Villacampa A, Ciska M, Edelmann RE, Kiss JZ, Medina FJ, Herranz R (2020a) The FixBox: hardware to provide on-orbit fixation capabilities to the EMCS on the ISS. Microgravity Sci Technol 32(6):1105–1120. https://doi.org/10.1007/s12217-020-09837-5
Manzano A, Pereda-Loth V, de Bures A, Sáez-Vásquez J, Herranz R, Medina FJ (2020b) Interaction of light and gravity signals as a mechanism of counteracting alterations caused by simulated microgravity in proliferating plant cells. Am J Bot. https://doi.org/10.21203/rs.3.rs-29236/v1
Manzano A, Villacampa A, Sáez-Vásquez J, Kiss JZ, Medina FJ, Herranz R (2020c) The importance of earth reference controls in spaceflight -omics research: characterization of nucleolin mutants from the seedling growth experiments. iScience 23(11):101686. https://doi.org/10.1016/j.isci.2020.101686
Massa GD, Newsham G, Hummerick ME, Caro JL, Stutte GW, Morrow RC, Wheeler RM (2013) Preliminary species and media selection for the veggie space hardware. Gravitational Space Res 1(1):95–106. http://gravitationalandspaceresearch.org/index.php/journal/article/view/616/636
Matía I, González-Camacho F, Herranz R, Kiss JZ, Gasset G, van Loon JJWA, Marco R, Medina FJ (2010) Plant cell proliferation and growth are altered by microgravity conditions in spaceflight. J Plant Physiol 167(3):184–193. https://doi.org/10.1016/j.jplph.2009.08.012
Mayer C, Grummt I (2005) Cellular stress and nucleolar function. Cell Cycle 4(8):1036–1038. https://doi.org/10.4161/cc.4.8.1925
Mazars C, Brière C, Grat S, Pichereaux C, Rossignol M, Pereda-Loth V, Eche B, Boucheron-Dubuisson E, Le Disquet I, Medina FJ, Graziana A, Carnero-Diaz E (2014) Microgravity induces changes in microsome-associated proteins of arabidopsis seedlings grown on board the international space station. PLoS One 9(3):e91814. https://doi.org/10.1371/journal.pone.0091814
Medina FJ, González-Camacho F (2003) Nucleolar proteins and cell proliferation in plant cells. In: Pandalai S (ed) Recent research developments in plant biology, vol 3. Research signpost, pp 55–68
Medina FJ, Cerdido A, De Cárcer G (2000) The functional organization of the nucleolus in proliferating plant cells. Eur J Histochem 44(2):117–131. https://digital.csic.es/bitstream/10261/211236/1/Medina_2000_EurJHistochem_review.pdf
Medina FJ, Gonzalez-Camacho F, Manzano AI, Manrique A, Herranz R (2010) Nucleolin, a major conserved multifunctional nucleolar phosphoprotein of proliferating cells. J Appl Biomed 8(3):141–150. https://doi.org/10.2478/v10136-009-0017-5
Menges M, Murray JAH (2006) Synchronization, transformation, and cryopreservation of suspension-cultured cells. In: Salinas J, Sánchez-Serrano JJ (eds) Arabidopsis protocols, Methods in molecular biology, 2nd edn. Humana Press, Totowa, pp 45–61. https://doi.org/10.1385/1-59745-003-0:45
Menges M, de Jager SM, Gruissem W, Murray JAH (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41(4):546–566. https://doi.org/10.1111/j.1365-313X.2004.02319.x
Millar KD, Johnson CM, Edelmann RE, Kiss JZ (2011) An endogenous growth pattern of roots is revealed in seedlings grown in microgravity. Astrobiology 11:787–797. https://doi.org/10.1089/ast.2011.0699
Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opinion Plant Biol 4(6):533–539. https://doi.org/10.1016/S1369-5266(00)00212-0
Moreno Díaz de la Espina S, Medina FJ, Risueño MC (1980) Correlation of nucleolar activity and nucleolar vacuolation in plant cells. Eur J Cell Biol 22(2):724–729
Moulia B, Bastien R, Chauvet-Thiry H, Leblanc-Fournier N (2019) Posture control in land plants: growth, position sensing, proprioception, balance, and elasticity. J Exp Bot 70(14):3467–3494. https://doi.org/10.1093/jxb/erz278
Muday GK, Haworth P (1994) Tomato root growth, gravitropism, and lateral development – correlation with auxin transport. Plant Physiol Biochem 32(2):193–203
Musgrave ME, Kuang A, **ao Y, Stout SC, Bingham GE, Briarty LG, Levinskikh MA, Sychev VN, Podolski IG (2000) Gravity independence of seed-to-seed cycling in Brassica rapa. Planta 210(3):400–406. https://doi.org/10.1007/PL00008148
Nakamura M, Nishimura T, Morita MT (2019) Bridging the gap between amyloplasts and directional auxin transport in plant gravitropism. Curr Opinion Plant Biol 52:54–60. https://doi.org/10.1016/j.pbi.2019.07.005
Nakashima J, Liao F, Sparks JA, Tang Y, Blancaflor EB (2014) The actin cytoskeleton is a suppressor of the endogenous skewing behaviour of Arabidopsis primary roots in microgravity. Plant Biol 16(s1):142–150. https://doi.org/10.1111/plb.12062
Overbey EG, Saravia-Butler AM, Zhang Z, Rathi KS, Fogle H, da Silveira WA, Barker RJ, Reinsch S, Davin LB, Gilroy S, Herranz R, Kruse CPS, Lewis NG, Villacampa A, Wyatt SE, Costes SV, Galazka JM (2020) NASA GeneLab RNA-seq consensus pipeline: standardized processing of short-read RNA-seq data. Cell Rep. https://doi.org/10.1101/2020.11.06.371724v1
Paul A-L, Amalfitano C, Ferl R (2012a) Plant growth strategies are remodeled by spaceflight. BMC Plant Biol 12(1):232. https://doi.org/10.1186/1471-2229-12-232
Paul A-L, Zupanska AK, Ostrow DT, Zhang Y, Sun Y, Li J-L, Shanker S, Farmerie WG, Amalfitano CE, Ferl RJ (2012b) Spaceflight transcriptomes: unique responses to a novel environment. Astrobiology 12(1):40–56. https://doi.org/10.1089/ast.2011.0696
Paul A-L, Sng NJ, Zupanska AK, Krishnamurthy A, Schultz ER, Ferl RJ (2017) Genetic dissection of the Arabidopsis spaceflight transcriptome: are some responses dispensable for the physiological adaptation of plants to spaceflight? PLoS One 12(6):e0180186. https://doi.org/10.1371/journal.pone.0180186
Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2(5):a001446. https://doi.org/10.1101/cshperspect.a001446
Plackett ARG, Coates JC (2016) Life's a beach – the colonization of the terrestrial environment. New Phytol 212(4):831–835. https://doi.org/10.1111/nph.14295
Pontvianne F, Matia I, Douet J, Tourmente S, Medina FJ, Echeverria M, Saez-Vasquez J (2007) Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Mol Biol Cell 18(2):369–379. https://doi.org/10.1091/mbc.E06-08-0751
Porterfield DM (2002) The biophysical limitations in physiological transport and exchange in plants grown in microgravity. J Plant Growth Regul 21(2):177–190. https://doi.org/10.1007/s003440010054
Rai A, Robinson JA, Tate-Brown J, Buckley N, Zell M, Tasaki K, Karabadzhak G, Sorokin IV, Pignataro S (2016) Expanded benefits for humanity from the international Space Station. Acta Astronaut 126:463–474. https://doi.org/10.1016/j.actaastro.2016.06.030
Rashotte AM, DeLong A, Muday GK (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 13(7):1683–1697. https://doi.org/10.1105/tpc.010158
Raska I, Shaw PJ, Cmarko D (2006) Structure and function of the nucleolus in the spotlight. Curr Opinion Cell Biol 18:325–334. https://doi.org/10.1016/j.ceb.2006.04.008
Ray S, Gebre S, Fogle H, Berrios DC, Tran PB, Galazka JM, Costes SV (2018) GeneLab: omics database for spaceflight experiments. Bioinformatics 35(10):1753–1759. https://doi.org/10.1093/bioinformatics/bty884
Reichler SA, Balk J, Brown ME, Woodruff K, Clark GB, Roux SJ (2001) Light differentially regulates cell division and the mRNA abundance of pea nucleolin during de-etiolation. Plant Physiol 125(1):339–350. https://doi.org/10.1104/pp.125.1.339
Rinaldi A (2016) Research in space: in search of meaning. EMBO Rep 17(8):1098–1102. https://doi.org/10.15252/embr.201642858
Roy R, Bassham DC (2014) Root growth movements: waving and skewing. Plant Sci 221-222:42–47. https://doi.org/10.1016/j.plantsci.2014.01.007
Rutter L, Barker R, Bezdan D, Cope H, Costes SV, Degoricija L, Fisch KM, Gabitto MI, Gebre S, Giacomello S, Gilroy S, Green SJ, Mason CE, Reinsch SS, Szewczyk NJ, Taylor DM, Galazka JM, Herranz R, Muratani M (2020) A new era for space life science: international standards for space omics processing (ISSOP). Patterns. https://doi.org/10.1016/j.patter.2020.100148
Sáez-Vásquez J, Delseny M (2019) Ribosome biogenesis in plants: from functional 45S ribosomal DNA organization to ribosome assembly factors. Plant Cell 31(9):1945–1967. https://doi.org/10.1105/tpc.18.00874
Sáez-Vásquez J, Medina FJ (2008) The plant nucleolus. In: Kader JC, Delseny M (eds) Advances in botanical research, vol 47. Elsevier, San Diego, pp 1–46. https://doi.org/10.1016/S0065-2296(08)00001-3
Sáez-Vásquez J, Caparros-Ruiz D, Barneche F, Echeverría M (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. Mol Cell Biol 24(16):7284–7297. https://doi.org/10.1128/MCB.24.16.7284-7297.2004
Srivastava M, Pollard HB (1999) Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J 13(14):1911–1922. https://doi.org/10.1096/fasebj.13.14.1911
Swarup R, Bennett MJ (2018) Root gravitropism. Ann Plant Rev:157–174. https://doi.org/10.1002/9781119312994.apr0401
Tajrishi MM, Tuteja R, Tuteja N (2011) Nucleolin: the most abundant multifunctional phosphoprotein of nucleolus. Commun Integr Biol 4(3):267–275. https://doi.org/10.4161/cib.4.3.14884
Taniguchi M, Furutani M, Nishimura T, Nakamura M, Fushita T, Iijima K, Baba K, Tanaka H, Toyota M, Tasaka M, Morita MT (2017) The arabidopsis LAZY1 family plays a key role in gravity signaling within statocytes and in branch angle control of roots and shoots. Plant Cell 29(8):1984–1999. https://doi.org/10.1105/tpc.16.00575
Toyota M, Gilroy S (2013) Gravitropism and mechanical signaling in plants. Am J Bot 100(1):111–125. https://doi.org/10.3732/ajb.1200408
Ueda J, Miyamoto K, Yuda T, Hoshino T, Fujii S, Mukai C, Kamigaichi S, Aizawa S, Yoshizaki I, Shimazu T, Fukui K (1999) Growth and development, and auxin polar transport in higher plants under microgravity conditions in space: BRIC-AUX on STS-95 space experiment. J Plant Res 112(4):487–492. https://doi.org/10.1007/PL00013904
Valbuena MA, Manzano A, Vandenbrink JP, Pereda-Loth V, Carnero-Diaz E, Edelmann RE, Kiss JZ, Herranz R, Medina FJ (2018) The combined effects of real or simulated microgravity and red-light photoactivation on plant root meristematic cells. Planta 248(3):691–704. https://doi.org/10.1007/s00425-018-2930-x
van Loon JJWA, Cras P, Bouwens WHACM, Roozendaal W, Vernikos J (2020) Gravity deprivation: is it ethical for optimal physiology? Front Physiol 11(470). https://doi.org/10.3389/fphys.2020.00470
Vandenbrink JP, Kiss JZ, Herranz R, Medina FJ (2014) Light and gravity signals synergize in modulating plant development. Front Plant Sci 5:563. https://doi.org/10.3389/fpls.2014.00563
Vandenbrink JP, Herranz R, Medina FJ, Edelmann RE, Kiss JZ (2016) A novel blue-light phototropic response is revealed in roots of Arabidopsis thaliana in microgravity. Planta 244(6):1201–1215. https://doi.org/10.1007/s00425-016-2581-8
Vandenbrink JP, Herranz R, Poehlman WL, Alex Feltus F, Villacampa A, Ciska M, Medina FJ, Kiss JZ (2019) RNA-seq analyses of Arabidopsis thaliana seedlings after exposure to blue-light phototropic stimuli in microgravity. Am J Bot 106(11):1466–1476. https://doi.org/10.1002/ajb2.1384
Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136(6):1005–1016. https://doi.org/10.1016/j.cell.2009.03.001
Volkmann D, Baluška F (2006) Gravity: one of the driving forces for evolution. Protoplasma 229(2):143–148. https://doi.org/10.1007/s00709-006-0200-4
Yamamoto K, Kiss JZ (2002) Disruption of the actin cytoskeleton results in the promotion of gravitropism in inflorescence stems and hypocotyls of Arabidopsis. Plant Physiol 128(2):669–681. https://doi.org/10.1104/pp.010804
Yoder TL, H-q Z, Todd P, Staehelin LA (2001) Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity-sensing apparatus of roots. Plant Physiol 125(2):1045–1060. https://doi.org/10.1104/pp.125.2.1045
Yoshihara T, Spalding EP (2017) LAZY genes mediate the effects of gravity on auxin gradients and plant architecture. Plant Physiol 175(2):959–969. https://doi.org/10.1104/pp.17.00942
Yu F, Driss-École D, Rembur J, Legué V, Perbal G (1999) Effect of microgravity on the cell cycle in the lentil root. Physiol Plant 105:171–178. https://doi.org/10.1034/j.1399-3054.1999.105125.x
Zupanska AK, Denison FC, Ferl RJ, Paul A-L (2013) Spaceflight engages heat shock protein and other molecular chaperone genes in tissue culture cells of Arabidopsis thaliana. Am J Bot 100(1):235–248. https://doi.org/10.3732/ajb.1200343
Zupanska AK, Schultz ER, Yao J, Sng NJ, Zhou M, Callaham JB, Ferl RJ, Paul A-L (2017) ARG1 functions in the physiological adaptation of undifferentiated plant cells to spaceflight. Astrobiology 17(11):1077–1111. https://doi.org/10.1089/ast.2016.1538
Zupanska AK, LeFrois C, Ferl RJ, Paul A-L (2019) HSFA2 functions in the physiological adaptation of undifferentiated plant cells to spaceflight. Int J Mol Sci 20(2):390. https://doi.org/10.3390/ijms20020390
Acknowledgements
We wish to thank all those colleagues in many laboratories all over the world, especially in Europe and the USA, with whom we have interacted, collaborated in shared experiments and exchanged data, results, and ideas. Among all of them, we would like to mention Prof. John Z. Kiss (University of North Carolina at Greensboro, USA) and Dr. Ing. Jack van Loon (ESA-ESTEC and Free University of Amsterdam, The Netherlands). We would also like to express our gratitude to technicians, engineers, and management personnel who has decisively contributed to the success of our spaceflight and ground-based experiments and to astronauts of the different ISS crews who took care of and effectively performed the spaceflight operations. Work performed in the authors’ laboratory was supported by different grants of the Spanish National Agency for Research of the Spanish Government, e.g. Grants #ESP2015-64323-R and #RTI2018-099309-B-I00 (co-funded by EU-ERDF). Access to ISS was made possible by ESA and NASA, and the use of ground-based facilities for microgravity simulation was supported by the ESA-CORA-GBF Program.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Medina, F.J., Manzano, A., Kamal, K.Y., Ciska, M., Herranz, R. (2021). Plants in Space: Novel Physiological Challenges and Adaptation Mechanisms. In: Lüttge, U., Cánovas, F.M., Risueño, MC., Leuschner, C., Pretzsch, H. (eds) Progress in Botany Vol. 83. Progress in Botany, vol 83. Springer, Cham. https://doi.org/10.1007/124_2021_53
Download citation
DOI: https://doi.org/10.1007/124_2021_53
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-12781-6
Online ISBN: 978-3-031-12782-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)