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Morphometric analyses of petioles of seedlings grown in a spaceflight experiment

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Abstract

Gravity is a constant unidirectional stimulus on Earth, and gravitropism in plants involves three phases: perception, transduction, and response. In shoots, perception takes place within the endodermis. To investigate the cellular machinery of perception in microgravity, we conducted a spaceflight study with Arabidopsis thaliana seedlings, which were grown in microgravity in darkness using the Biological Research in Canisters (BRIC) hardware during space shuttle mission STS-131. In the 14-day-old etiolated plants, we studied seedling development and the morphological parameters of the endodermal cells in the petiole. Seedlings from the spaceflight experiment (FL) were compared to a ground control (GC), which both were in the BRIC flight hardware. In addition, to assay any potential effects from growth in spaceflight hardware, we performed another control by growing seedlings in Petri dishes in standard laboratory conditions (termed the hardware control, HC). Seed germination was significantly lower in samples grown in flight hardware (FL, GC) compared to the HC. In terms of cellular parameters of endodermal cells, the greatest differences also were between seedlings grown in spaceflight hardware (FL, GC) compared to those grown outside of this hardware (HC). Specifically, the endodermal cells were significantly smaller in seedlings grown in the BRIC system compared to those in the HC. However, a change in the shape of the cell, suggesting alterations in the cell wall, was one parameter that appears to be a true microgravity effect. Taken together, our results suggest that caution must be taken when interpreting results from the increasingly utilized BRIC spaceflight hardware system and that it is important to perform additional ground controls to aid in the analysis of spaceflight experiments.

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References

  • Andres C, Agne B, Kessler F (2010) The TOC complex: preprotein gateway to the chloroplast. Biochim Biophys Acta 1803:715–723

    Article  CAS  PubMed  Google Scholar 

  • Bastien R, Douady S, Moulia B (2014) A unifying modeling of plant shoot gravitropism with an explicit account of the effects of growth. Front Plant Sci 5:136. doi:10.3389/fpls.2014.00136

    Article  PubMed Central  PubMed  Google Scholar 

  • Battista N, Meloni MA, Bari M, Mastrangelo N, Galleri G, Rapino C, Dainese E, Agro AF, Pippia P, Maccarrone M (2012) 5-lipoxygenase-dependent apoptosis of human lymphocytes in the International Space Station: data from the ROALD experiment. FASEB J 26:1791–1798

    Article  CAS  PubMed  Google Scholar 

  • Blancaflor EB (2013) Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am J Bot 100:143–152

    Article  CAS  PubMed  Google Scholar 

  • Correll MJ, Pyle TP, Millar KDL, Sun Y, Yao J, Edelmann RE, Kiss JZ (2013) Transcriptome analysis of Arabidopsis thaliana seedlings grown in space: implications for gravity responsive genes. Planta 238:519–533

    Article  CAS  PubMed  Google Scholar 

  • De Micco V, Aronne G, Joseleau J-P, Ruel K (2008) Xylem development and cell wall changes of soybean seedlings grown in space. Ann Bot 101:661–669

    Article  PubMed Central  PubMed  Google Scholar 

  • Driss-École D, Vassy J, Rembur J, Guivarc’h A, Prouteau M, Dewitte W, Perbal G (2000) Immunolocalization of actin in root statocytes of Lens culinaris L. J Exp Bot 51:521–528

    Article  PubMed  Google Scholar 

  • Evans ML, Moore R, Hasenstein KH (1986) How roots respond to gravity. Sci Am 255:112–119

    Article  CAS  PubMed  Google Scholar 

  • Fukaki H, Tasaka M (1999) Gravity perception and gravitropic response of inflorescence stems in Arabidopsis thaliana. Adv Space Res 24:763–770

    Article  CAS  PubMed  Google Scholar 

  • Guisinger MM, Kiss JZ (1999) The influence of microgravity and spaceflight on columella cell ultrastructure in starch-deficient mutants of Arabidopsis. Am J Bot 86:1357–1366

    Article  CAS  PubMed  Google Scholar 

  • Haberlandt G (1914) Physiological plant anatomy, 4th edn. Macmillan, London

    Google Scholar 

  • Halstead TW, Dutcher FR (1987) Plants in space. Ann Rev Plant Physiol 38:317–345

    Article  CAS  Google Scholar 

  • Hashiguchi Y, Tasaka M, Morita MT (2013) Mechanism of higher plant gravity sensing. Am J Bot 100:91–100

    Article  CAS  PubMed  Google Scholar 

  • Hertel R, De la Fuente RK, Leopold AC (1969) Geotropism and the lateral transport of auxin in the corn mutant amylomaize. Planta 88:204–214

    Article  CAS  PubMed  Google Scholar 

  • Hoson T, Soga K, Mori R, Saiki M, Nakamura Y, Wakabayashi K, Kamisaka S (2002) Stimulation of elongation growth and cell wall loosening in rice coleoptiles under microgravity conditions in space. Plant Cell Physiol 43:1067–1071

    Article  CAS  PubMed  Google Scholar 

  • Iversen T-H (1969) Elimination of gravitropic responsiveness in roots of cress (Lepidium sativum) by removal of statolith starch. Physiol Plant 22:1251–1262

    Article  CAS  PubMed  Google Scholar 

  • Josse E-M, Halliday KJ (2008) Skotomorphogenesis: the dark side of light signaling. Curr Bio 18:R1144–R1146

    Article  CAS  Google Scholar 

  • Kern VD, Sack FD, White NJ, Anderson K, Wells W, Martin CA (1999) Spaceflight hardware allowing unilateral irradiation and chemical fixation in Petri dishes. Adv Space Res 24:775–778

    Article  CAS  PubMed  Google Scholar 

  • Kiss JZ (2000) Mechanisms of the early phases of plant gravitropism. Crit Rev Plant Sci 19:551–573

    Article  CAS  PubMed  Google Scholar 

  • Kiss JZ, Sack FD (1990) Severely reduced gravitropism in dark-grown hypocotyls of a starch-deficient mutant of Nicotiana sylvestris. Plant Physiol 94:1867–1873

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kiss JZ, Hertel R, Sack FD (1989) Amyloplasts are necessary for full gravitropic sensitivity in roots of Arabidopsis thaliana. Planta 177:198–206

    Article  Google Scholar 

  • Kiss JZ, Wright JB, Caspar T (1996) Gravitropism in roots of intermediate-starch mutants of Arabidopsis. Physiol Plant 97:237–244

    Article  CAS  PubMed  Google Scholar 

  • Kiss JZ, Guisinger MM, Miller AJ, Stackhouse KS (1997) Reduced gravitropism in hypocotyls of starch-deficient mutants of Arabidopsis. Plant Cell Physiol 38:518–525

    Article  CAS  PubMed  Google Scholar 

  • Kiss JZ, Edelmann RE, Wood CP (1999) Gravitropism of hypocotyls of wild-type and starch-deficient Arabidopsis seedlings in spaceflight studies. Planta 209:96–103

    Article  CAS  PubMed  Google Scholar 

  • Kiss JZ, Kumar P, Bowman RN, Steele MK, Eodice MT, Correll MJ, Edelmann RE (2007) Biocompatibility studies in preparation for a spaceflight experiment on plant tropisms (TROPI). Adv Space Res 39:1154–1160

    Article  Google Scholar 

  • Kiss JZ, Millar KDL, Edelmann RE (2012) Phototropism of Arabidopsis thaliana in microgravity and fractional gravity on the International Space Station. Planta 236:635–645

    Article  CAS  PubMed  Google Scholar 

  • Kraft TFB, VanLoon JJWA, Kiss JZ (2000) Plastid position in Arabidopsis columella cells is similar in microgravity and on a random-positioning machine. Planta 211:415–422

    Article  CAS  PubMed  Google Scholar 

  • Kumar NS, Stevens MHH, Kiss JZ (2008) Plastid movement in statocytes of the ARG1 (altered response to gravity) mutant. Am J Bot 95:177–184

    Article  Google Scholar 

  • Leitz G, Kang B, Schoenwaelder MEA, Staehelin LA (2009) Statolith sedimentation kinetics and force transduction to the cortical endoplasmic reticulum in gravity-sensing Arabidopsis columella cells. Plant Cell 21:843–860

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Levine LH, Heyenga AG, Levine HG, Choi JW, Davin LB, Krikorian AD, Lewis NG (2001) Cell-wall architecture and lignin composition of wheat developed in a microgravity environment. Phytochemistry 57:835–846

    Article  CAS  PubMed  Google Scholar 

  • Lloyd SA, Ferguson VS, Simske SJ, Dunlap AW, Livingston EW, Bateman TA (2013) Housing in the animal enclosure module spaceflight hardware increases trabecular bone mass in ground-control mice. Gravit Space Res 1:2–19

    Google Scholar 

  • MacCleery SA, Kiss JZ (1999) Plastid sedimentation kinetics in roots of wild-type and starch-deficient mutants of Arabidopsis. Plant Physiol 120:183–192

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mano E, Horiguchi G, Tsukaya H (2006) Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh. Plant Cell Physiol 47:217–223

    Article  CAS  PubMed  Google Scholar 

  • Massa G, Newsham G, Hummerick ME, Caro JL, Stutte GW, Morrow RC, Wheeler RM (2013) Preliminary species and media selection for the veggie space hardware. Gravit Space Res 1:95–106

    Google Scholar 

  • Millar KDL, Johnson CM, Edelmann RE, Kiss JZ (2011) An endogenous growth pattern in roots is revealed in seedlings grown in microgravity. Astrobiology 11:787–797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Molas ML, Kiss JZ (2009) Phototropism and gravitropism in plants. Adv Bot Res 49:1–34

    Article  CAS  Google Scholar 

  • Moore R (1990) How effectively does a clinostat mimic the ultrastructural effects of microgravity on plant cells? Ann Bot 65:213–216

    CAS  PubMed  Google Scholar 

  • Moore R, Evans ML (1986) How roots perceive and respond to gravity. Am J Bot 73:574–587

    Article  CAS  PubMed  Google Scholar 

  • Morita MT, Kato T, Nagafusa K, Saito C, Ueda T, Nakano A, Tasaka M (2002) Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. Plant Cell 14:47–56

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Musgrave ME, Kuang A, Matthews SW (1997) Plant reproduction during spaceflight: importance of the gaseous environment. Planta 203:S177–S184

    Article  CAS  PubMed  Google Scholar 

  • Musgrave ME, Kuang A, Brown CS, Matthews SW (1998) Changes in Arabidopsis leaf ultrastructure, chlorophyll and carbohydrate content during spaceflight depend on ventilation. Ann Bot 81:503–512

    Article  CAS  PubMed  Google Scholar 

  • Nakashima J, Liao F, Sparks JA, Tang Y, Blancaflor EB (2014) The actin cytoskeleton is a suppressor of the endogenous skewing behavior of Arabidopsis primary roots in microgravity. Plant Biol 16:142–150

    Article  PubMed  Google Scholar 

  • Palmieri M, Kiss JZ (2006) The role of plastids in gravitropism. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 507–525

    Chapter  Google Scholar 

  • Parsons-Wingerter P, Vickerman MB, Paul A-L, Ferl RJ (2014) Mapping by VESGEN of leaf venation patterning in Arabidopsis thaliana with bioinformatic dimensions of gene expression. Gravit Space Res 2:68–81

    Google Scholar 

  • Paul A-L, Amalfitano CE, Ferl RJ (2012a) Plant growth strategies are remodeled by spaceflight. BMC Plant Biol 12:232

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 12:40–56

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Perbal G (2009) From ROOTS to GRAVI-1: twenty five years for understanding how plants sense gravity. Microgravity Sci Technol 21:3–10

    Article  Google Scholar 

  • Perbal G, Driss-École D (1989) Polarity of statocytes in lentil seedling roots grown in space (spacelab D1 mission). Physiol Plant 75:518–524

    Article  CAS  PubMed  Google Scholar 

  • Perbal G, Driss-École D (1994) Sensitivity of gravistimulus of lentil seedling roots grown in space during the IML 1 mission of spacelab. Phys Plant 90:313–318

    Article  CAS  Google Scholar 

  • Pickard BG, Thimann KV (1966) Geotropic response of wheat coleoptiles in absence of amyloplast starch. J Gen Physiol 49:1065–1086

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Roberts JA (1984) Tropic responses of hypocotyls from normal tomato plants and the gravitropic mutant Lazy-1. Plant Cell Environ 7:515–520

    Google Scholar 

  • Sack FD (1987) The structure of the stem endodermis in etiolated pea seedlings. Can J Bot 65:1514–1519

    Article  CAS  PubMed  Google Scholar 

  • Sack FD (1991) Plant gravity sensing. Int Rev Cytol 127:193–252

    Article  CAS  PubMed  Google Scholar 

  • Saito C, Morita MT, Kato T, Tasaka M (2005) Amyloplasts and vacuolar membrane dynamics in the living graviperceptive cell of the Arabidopsis inflorescence stem. Plant Cell 17:548–558

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salisbury FB (1993) Gravitropism: changing ideas. Hortic Rev 15:233–278

    Google Scholar 

  • Schultz ER, Zupanska AK, Manning-Roach S, Camacho J, Levine H, Paul A-L, Ferl RJ (2012) Testing the bio-compatibility of aluminum PDFU BRIC hardware. Gravit Space Res 26:48–63

    Google Scholar 

  • Scott AC, Allen NS (1999) Changes in cytosolic pH within Arabidopsis root columella cells play a key role in the early signaling pathway for root gravitropism. Plant Physiol 121:1291–1298

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sievers A, Kruse S, Kuo-Huang L-L, Wendt M (1989) Statoliths and microfilaments in plant cells. Planta 179:275–278

    Article  CAS  PubMed  Google Scholar 

  • Song LU, Brock TG, Kaufman PB (1988) Do starch statoliths act as the gravisensors in cereal grass pulvini? Plant Physiol 86:1155–1162

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stanga JP, Kanokporn B, Sedbrook JC, Otegui MS, Masson PH (2009) A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol 149:1896–1905

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Strohm AK, Barrett-Wilt GA, Masson PA (2014) A functional TOC complex contributes to gravity signal transduction in Arabidopsis. Front Plant Sci 5:148. doi:10.3389/fpls.2014.00148

    Article  PubMed Central  PubMed  Google Scholar 

  • Stutte GW, Roberts MS (2011) Effects of microgravity on the early events of biological nitrogen fixation in Medicago truncatula: initial results from the SyNRGE experiment. NASA Technical Report KSC-2011-249. http://ntrs.nasa.gov/search.jsp?R=20120010667 Accessed 5 May 2015

  • Tasaka M, Kato T, Fukaki H (1999) The endodermis and shoot gravitropism. Trends Plant Sci 4:103–107

    Article  CAS  PubMed  Google Scholar 

  • Vandenbrink JP, Kiss JZ, Herranz R, Medina FJ (2014) Light and gravity signals synergize in modulating plant development. Front Plant Sci 5:563. doi:10.3389/fpls.2014.00563

    Article  PubMed Central  PubMed  Google Scholar 

  • Vitha S, Yang M, Sack FD, Kiss JZ (2007) Gravitropism in the starch excess mutant of Arabidopsis thaliana. Am J Bot 94:590–598

    Article  PubMed  Google Scholar 

  • Volkmann D, Sievers A (1979) Graviperception in multicellular organs. In: Haupt W, Feinleib ME (eds) Encyclopedia of plant physiology. Springer, Berlin, pp 573–600

    Google Scholar 

  • Volkmann D, Behrens HM, Sievers A (1986) Development and gravity sensing of cress roots under microgravity. Naturwissenschaften 73:438–441

    Article  CAS  PubMed  Google Scholar 

  • Wells B, Best MD, McCray RH, Levine HG (2001) A flight-rated Petri dish apparatus providing two stage fluid injection for aseptic biological investigations in space. 31st international conference on environmental systems, SAE International 2001-01-2286

  • Wheeler RM, Peterson BV, Stutte GW (2004) Ethylene production throughout growth and development of plants. Hort Sci 39:1541–1545

    CAS  Google Scholar 

  • Yamamoto K, Kiss JZ (2002) Disruption of the actin cytoskeleton results in the promotion of gravitropism in infloresence stems and hypocotyls of Arabidopsis. Plant Physiol 128:669–681

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yoder T, Zheng H, Todd P, Staehelin L (2001) Amyloplast sedimentation dynamics in maize columella cells support a new model for the gravity sensing apparatus of roots. Plant Physiol 125:1045–1060

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This spaceflight experiment would not have been possible without the efforts of the staff at NASA’s Kennedy Space Center including Howard Levine, Christopher Comstock, David Cox, Kimberly Slater, Susan Manning-Roach, David Reed, and Stacy Engel. We also thank Astronaut Stephanie Wilson for her in-flight interactions with our hardware on STS-131. In addition, we are grateful to Jin Nakashima for his on-site photography of samples at KSC, Kathy Millar for her assistance with sample processing, and Matthew Duley for additional technical assistance. Financial support for this project was provided by NASA though grant NNX10AF44G.

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Authors and Affiliations

  1. Biology Department, Miami University, Oxford, OH, 45056, USA

    Christina M. Johnson, Aswati Subramanian & Richard E. Edelmann

  2. Biology Department and the Graduate School, University of Mississippi-Oxford, Oxford, MS, 38677, USA

    John Z. Kiss

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  1. Christina M. Johnson
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  2. Aswati Subramanian
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  3. Richard E. Edelmann
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  4. John Z. Kiss
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Correspondence to John Z. Kiss.

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Johnson, C.M., Subramanian, A., Edelmann, R.E. et al. Morphometric analyses of petioles of seedlings grown in a spaceflight experiment. J Plant Res 128, 1007–1016 (2015). https://doi.org/10.1007/s10265-015-0749-0

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