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Root Growth Patterns and Morphometric Change Based on the Growth Media

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Abstract

Arabidopsis thaliana roots skew with minimal waving in the microgravity environment of the International Space Station. Root skewing and root waving have been studied on the ground as well as in spaceflight, but often using different media types. In this study, Arabidopsis seedlings were grown on nutrient media plates that were comprised of various gelling agents with varied hardness in order to better assess these media for spaceflight research experiments. ImageJ was used to quantify the root morphology of 8-dayold seedlings, while R was used to perform statistical analyses. Root growth was drastically different between Difco agar, agarose, and Phytagel. Additionally, root waving masked skewing in certain media. Regression analysis revealed overall patterns when organized by hardness but also revealed that differences in media type had more of an impact on root growth than hardness itself. Different arrangements of media around the root tip revealed that roots grown on the media surface were longer and had fewer waves per millimeter than roots grown embedded in media. The implications for spaceflight research are discussed.

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References

  • Bisgrove, S.R., Lee, Y.R., Liu, B., Peters, N.T., Kropf, D.L.: The microtubule plus-end binding protein EB1 functions in root responses to touch and gravity signals in Arabidopsis. Plant. Cell. 20(2), 396–410 (2008). doi:10.1105/tpc.107.056846

    Article  Google Scholar 

  • Buer, C.S., Masle, J., Wasteneys, G.O.: Growth conditions modulate root-wave phenotypes in Arabidopsis. Plant. Cell. Physiol. 41(10), 1164–1170 (2000)

    Article  Google Scholar 

  • Buer, C.S., Wasteneys, G.O., Masle, J.: Ethylene modulates root-wave responses in Arabidopsis. Plant. Physiol. 132(2), 1085–1096 (2003). doi:10.1104/pp.102.019182

    Article  Google Scholar 

  • Canty, A., Ripley, B.: boot: Bootstrap R (S-Plus) Functions. In: R package version 1.3–15 (2015)

  • Darwin, C., Darwin, F.: The Power of Movement in Plants. John Murray, London (1880)

    Book  MATH  Google Scholar 

  • de Mendiburu, F.: agricolae: statistical procedures for agricultural research. In: http://CRAN.R-project.org/package=agricolae, R package version 1.2-1 (2014)

  • Evans, M.: Touch sensitivity in plants: be aware or beware. Trends. Plant. Sci. 8(7), 312–314 (2003). doi:10.1016/S1360-1385(03)00133-X

    Article  Google Scholar 

  • Fox, J., Weisberg, S.: An RCompanion to applied regression, second edition. In: Sage. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion, Thousand Oaks, CA (2011)

  • Grabov, A., Ashley, M.K., Rigas, S., Hatzopoulos, P., Dolan, L., Vicente-Agullo, F.: Morphometric analysis of root shape. New. Phytol. 165(2), 641–651 (2005). doi:10.1111/j.1469-8137.2004.01258.x

    Article  Google Scholar 

  • Hothorn, T., Bretz, F., Westfall, P.: Simultaneous inference in general parametric models. Biom. J 50 (3), 346–363 (2008). doi:10.1002/bimj.200810425

    Article  MathSciNet  MATH  Google Scholar 

  • Iida, H., Furuichi, T., Nakano, M., Toyota, M., Sokabe, M., Tatsumi, H.: New candidates for mechano-sensitive channels potentially involved in gravity sensing in Arabidopsis thaliana. Plant. Biol. (Stuttg). 16. Suppl. 1, 39–42 (2014). doi:10.1111/plb.12044

    Article  Google Scholar 

  • Kim, S.K., Chojnacka, K.: Marine algae extracts: processes, products, and applications, 2 Volume Set. vol. v. 1 Wiley (2015)

  • Kushwah, S., Jones, A.M., Laxmi, A.: Cytokinin interplay with ethylene, auxin, and glucose signaling controls Arabidopsis seedling root directional growth. Plant. Physiol. 156(4), 1851–1866 (2011). doi:10.1104/pp.111.175794

    Article  Google Scholar 

  • Lamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D.L., Garcia-Hernandez, M., Karthikeyan, A.S., Lee, C.H., Nelson, W.D., Ploetz, L., Singh, S., Wensel, A., Huala, E.: The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic. Acids. Res. 40(Database issue), D1202–1210 (2012). doi:10.1093/nar/gkr1090

    Article  Google Scholar 

  • Langsrud, O.: ANOVA For unbalanced data: use type II instead of type III sums of squares. Stat. Comput. 13(2), 163–167 (2003)

    Article  MathSciNet  Google Scholar 

  • Lemon, J.: Plotrix: a package in the red light district of R. R-News 6(4), 8–12 (2006)

    Google Scholar 

  • Li, H., Shen, T., Smith, M.B., Fujiwara, I., Vavylonis, D., Huang, X.: Automated actin filament segmentation, tracking and tip elongation measurements based on open active contour models. Proceedings/IEEE. Int. Symp. Biomed. Imaging. 2009, 1302–1305 (2009). doi:10.1109/ISBI.2009.5193303

    Google Scholar 

  • Manak, M.S., Paul, A. -L., Sehnke, P.C., Ferl, R.J.: Remote sensing of gene expression in Planta: transgenic plants as monitors of exogenous stress perception in extraterrestrial environments. Life. Support. Biosph. Sci. 8(2), 83–91 (2002)

    Google Scholar 

  • Massa, G.D., Gilroy, S.: Touch and gravitropic set-point angle interact to modulate gravitropic growth in roots. Adv. Space. Res. 31(10), 2195–2202 (2003a)

  • Massa, G.D., Gilroy, S.: Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana. Plant. J 33(3), 435–445 (2003b)

  • Millar, K.D., Johnson, C.M., Edelmann, R.E., Kiss, J.Z.: An endogenous growth pattern of roots is revealed in seedlings grown in microgravity. Astrobiology 11(8), 787–797 (2011). doi:10.1089/ast.2011.0699

    Article  Google Scholar 

  • Mochizuki, S., Harada, A., Inada, S., Sugimoto-Shirasu, K., Stacey, N., Wada, T., Ishiguro, S., Okada, K., Sakai, T.: The Arabidopsis WAVY GROWTH 2 protein modulates root bending in response to environmental stimuli. Plant. Cell. 17(2), 537–547 (2005). doi:10.1105/tpc.104.028530

    Article  Google Scholar 

  • Nakano, M., Samejima, R., Iida, H.: Mechanosensitive channel candidate MCA2 is involved in touch-induced root responses in Arabidopsis. Front. Plant. Sci. 5, 421 (2014). doi:10.3389/fpls.2014.00421

    Google Scholar 

  • Nakashima, J., Liao, F., Sparks, J.A., Tang, Y., Blancaflor, E.B.: The actin cytoskeleton is a suppressor of the endogenous skewing behaviour of Arabidopsis primary roots in microgravity. Plant. Biol. (Stuttg). 16. Suppl. 1, 142–150 (2014). doi:10.1111/plb.12062

    Article  Google Scholar 

  • Okada, K., Shimura, Y.: Reversible root tip rotation in Arabidopsis seedlings induced by obstacle-touching stimulus. Science 250(4978), 274–276 (1990). doi:10.1126/science.250.4978.274

    Article  Google Scholar 

  • Oliva, M., Dunand, C.: Waving and skewing: How gravity and the surface of growth media affect root development in Arabidopsis. New. Phytol. 176(1), 37–43 (2007). doi:10.1111/j.1469-8137.2007.02184.x

    Article  Google Scholar 

  • Pandey, S., Monshausen, G.B., Ding, L., Assmann, S.M.: Regulation of root-wave response by extra large and conventional G proteins in Arabidopsis thaliana. Plant. J. 55(2), 311–322 (2008). doi:10.1111/j.1365-313X.2008.03506.x

    Article  Google Scholar 

  • Paul, A. -L., Amalfitano, C.E., Ferl, R.J.: Plant growth strategies are remodeled by spaceflight. BMC Plant. Biol. 12, 232 (2012). doi:10.1186/1471-2229-12-232

    Article  Google Scholar 

  • R Core Team: R: a language and environment for statistical computing. In: http://www.R-project.org/, R Foundation for Statistical Computing, Vienna, Austria (2014)

  • Roux, S.J.: Root waving and skewing: unexpectedly in micro-g. BMC Plant. Biol. 12, 231 (2012). doi:10.1186/1471-2229-12-231

    Article  Google Scholar 

  • Roy, R., Bassham, D.C.: Root growth movements: waving and skewing. Plant. Sci. 221-222, 42–47 (2014). doi:10.1016/j.plantsci.2014.01.007

    Article  Google Scholar 

  • RStudio: RStudio: Integrated development environment for R (version 0.98.994). In: http://www.rstudio.org/, Boston, MA (2013)

  • Sakai, T., Mochizuki, S., Haga, K., Uehara, Y., Suzuki, A., Harada, A., Wada, T., Ishiguro, S., Okada, K.: The wavy growth 3 E3 ligase family controls the gravitropic response in Arabidopsis roots. Plant. J 70(2), 303–314 (2012). doi:10.1111/j.1365-313X.2011.04870.x

    Article  Google Scholar 

  • Scherer, G.F., Pietrzyk, P.: Gravity-dependent differentiation and root coils in Arabidopsis thaliana wild type and phospholipase-A-I knockdown mutant grown on the International Space Station. Plant. Biol. (Stuttg). 16. Suppl. 1, 97–106 (2014). doi:10.1111/plb.12123

    Article  Google Scholar 

  • Schneider, C.A., Rasband, W.S., Eliceiri, K.W.: NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 9(7), 671–675 (2012)

    Article  Google Scholar 

  • Sedbrook, J., Boonsirichai, K., Chen, R., Hilson, P., Pearlman, R., Rosen, E., Rutherford, R., Batiza, A., Carroll, K., Schulz, T., Masson, P.H.: Molecular genetics of root gravitropism and waving in Arabidopsis thaliana. Gravit. Space. Biol. Bull. 11(2), 71–78 (1998)

    Google Scholar 

  • Sedbrook, J.C., Carroll, K.L., Hung, K.F., Masson, P.H., Somerville, C.R.: The Arabidopsis SKU5 gene encodes an extracellular glycosyl phosphatidylinositol-anchored glycoprotein involved in directional root growth. Plant. Cell. 14(7), 1635–1648 (2002)

    Article  Google Scholar 

  • Shih, H.W., Miller, N.D., Dai, C., Spalding, E.P., Monshausen, G.B.: The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr. Biol. 24(16), 1887–1892 (2014). doi:10.1016/j.cub.2014.06.064

    Article  Google Scholar 

  • Smith, M.B., Li, H., Shen, T., Huang, X., Yusuf, E., Vavylonis, D.: Segmentation and tracking of cytoskeletal filaments using open active contours. Cytoskeleton. (Hoboken) 67(11), 693–705 (2010). doi:10.1002/cm.20481

    Article  Google Scholar 

  • Swanson, S.J., Barker, R., Ye, Y., Gilroy, S.: Evaluating mechano-transduction and touch responses in plant roots. Methods. Mol. Biol. 1309, 143–150 (2015). doi:10.1007/978-1-4939-2697-812

    Article  Google Scholar 

  • Takahashi, N., Goto, N., Okada, K., Takahashi, H.: Hydrotropism in abscisic acid, wavy, and gravitropic mutants of Arabidopsis thaliana. Planta 216(2), 203–211 (2002). doi:10.1007/s00425-002-0840-3

    Article  Google Scholar 

  • Thompson, M.V., Holbrook, N.M.: Root-gel interactions and the root waving behavior of Arabidopsis. Plant. Physiol. 135(3), 1822–1837 (2004). doi:10.1104/pp.104.040881

    Article  Google Scholar 

  • Trewavas, A., Knight, M.: Mechanical signalling, calcium and plant form. Plant. Mol. Biol. 26(5), 1329–1341 (1994)

    Article  Google Scholar 

  • Ulmasov, T., Murfett, J., Hagen, G., Guilfoyle, T.J.: Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant. Cell. 9(11), 1963–1971 (1997). doi:10.1105/tpc.9.11.1963

    Article  Google Scholar 

  • Vaughn, L.M., Masson, P.H.: A QTL study for regions contributing to Arabidopsis thaliana root skewing on tilted surfaces. G3. (Bethesda) 1(2), 105–115 (2011). doi:10.1534/g3.111.000331

    Article  Google Scholar 

  • Weerasinghe, R.R., Swanson, S.J., Okada, S.F., Garrett, M.B., Kim, S.Y., Stacey, G., Boucher, R.C., Gilroy, S., Jones, A.M.: Touch induces ATP release in Arabidopsis roots that is modulated by the heterotrimeric G-protein complex. FEBS Lett. 583(15), 2521–2526 (2009). doi:10.1016/j.febslet.2009.07.007

    Article  Google Scholar 

  • Wickham, H.: The split-apply-combine strategy for data analysis. J. Stat. Softw. 40(1), 1–29 (2011)

    Article  MathSciNet  Google Scholar 

  • Wickham, H., Francois, R.: dplyr: a grammar of data manipulation. In: http://CRAN.R-project.org/package=dplyr, R package version 0.4.1 (2015)

  • Yamamoto, C., Sakata, Y., Taji, T., Baba, T., Tanaka, S.: Unique ethylene-regulated touch responses of Arabidopsis thaliana roots to physical hardness. J. Plant. Res. 121(5), 509–519 (2008). doi:10.1007/s10265-008-0178-4

    Article  Google Scholar 

  • Yuen, C.Y., Pearlman, R.S., Silo-Suh, L., Hilson, P., Carroll, K.L., Masson, P.H.: WVD2 And WDL1 modulate helical organ growth and anisotropic cell expansion in Arabidopsis. Plant. Physiol. 131(2), 493–506 (2003). doi:10.1104/pp.015966

    Article  Google Scholar 

  • Yuen, C.Y., Sedbrook, J.C., Perrin, R.M., Carroll, K.L., Masson, P.H.: Loss-of-function mutations of ROOT HAIR DEFECTIVE3 suppress root waving, skewing, and epidermal cell file rotation in Arabidopsis. Plant. Physiol. 138(2), 701–714 (2005). doi:10.1104/pp.105.059774

    Article  Google Scholar 

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Acknowledgments

The authors thank Andrew Schuerger, James Colee, and Ryan Schultz for their ideas and discussions to help improve this manuscript. The experimental work presented here is supported by the National Aeronautics and Space Administration grants NNX12AN69G and NNX07AH27G to A-L Paul and R.J. Ferl and the National Aeronautics and Space Administration Training Grant NNX15AI10H to Florida Space Grant Consortium to E.R. Schultz.

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Correspondence to Robert J. Ferl.

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Schultz, E.R., Paul, AL. & Ferl, R.J. Root Growth Patterns and Morphometric Change Based on the Growth Media. Microgravity Sci. Technol. 28, 621–631 (2016). https://doi.org/10.1007/s12217-016-9514-9

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