Mechanical touch responses of Arabidopsis TCH1-3 mutant roots on inclined hard-agar surface

Open access

Abstract

The gravity-induced mechanical touch stimulus can affect plant root architecture. Mechanical touch responses of plant roots are an important aspect of plant root growth and development. Previous studies have reported that Arabidopsis TCH1-3 genes are involved in mechano-related events, how-ever, the physiological functions of TCH1-3 genes in Arabidopsis root mechanoresponses remain unclear. In the present study, we applied an inclined hard agar plate method to produce mechanical touch stimulus, and provided evidence that altered mechanical environment could influence root growth. Furthermore, tch1-3 Arabidopsis mutants were investigated on inclined agar surfaces to explore the functions of TCH1-3 genes on Arabidopsis root mechanoresponses. The results showed that two tch2 mutants, cml24-2 and cml24-4, exhibited significantly reduced root length, biased skewing, and decreased density of lateral root. In addition, primary root length and density of lateral root of tch3 (cml12-2) was significantly decreased on inclined agar surfaces. This study indicates that the tch2 and tch3 mutants are hypersensitive to mechanical touch stimulus, and TCH2 (CML24-2 and CML24-4) and TCH3 (CML12-2) genes may participate in the mechanical touch response of Arabidopsis roots.

Braam J., 1992. Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. Proc. National Academy of Sciences, 89(8), 3213-3216.

Braam J. and Davis R.W., 1990. Rain-induced, wind-induced, and touch-induced expression of calmodulin and calmodulin-related genes in arabidopsis. Cell, 60(3), 357-364.

Chehab E.W., Eich E., and Braam J., 2009. Thigmomorphogenesis: a complex plant response to mechano-stimulation. J. Experimental Botany, 60(1), 43-56.

Coutand C., 2010. Mechanosensing and thigmomorphogenesis, a physiological and biomechanical point of view. Plant Sci., 179(3), 168-182.

De Smet I., White P.J., Bengough A.G., Dupuy L., Parizot B., Casimiro I., Heidstra R., Laskowski M., Lepetit M., Hochholdinger F., Draye X., Zhang H., Broadley M.R., Peret B., Hammond J.P., Fukaki H., Mooney S., Lynch J.P., Nacry P., Schurr U., Laplaze L., Benfey P., Beeckman T., and Bennett M., 2012. Analyzing lateral root development: how to move forward. Plant Cell, 24(1), 15-20.

Delk N.A., Johnson K.A., Chowdhury N.I., and Braam J., 2005. CML24, regulated in expression by diverse stimuli, encodes a potential Ca2+ sensor that functions in responses to abscisic acid, daylength, and ion stress. Plant Physiology, 139(1), 240-253.

Ditengou F. A., Tealea W.D., Kochersperger P., Flittner K.A., Kneuper I., van der Graaff E., Nziengui H., Pinosa F., Li X., Nitschke R., Laux T., and Palme K., 2008. Mechanical induction of lateral root initiation in Arabidopsis thaliana. Proc. Nat. Acad. Sci. USA, 105(48), 18818-18823.

Dubrovsky J., Gambetta G., Hernandez-Barrera A., Shishkova S., and Gonzalez I., 2006. Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density and predictability. Annals Botany, 97(5), 903-915.

Gleeson L., Squires S., and Bisgrove S.R., 2012. The microtubule associated protein END BINDING 1 represses root responses to mechanical cues. Plant Sci., 187, 1-9.

Hamant O., Heisler M.G., Jonsson H., Krupinski P., Uyttewaal M., Bokov P., Corson F., Sahlin P., Boudaoud A., Meyerowitz E.M., Couder Y., and Traas J., 2008. Developmental patterning by mechanical signals in Arabidopsis. Science, 322(5908), 1650-1655.

Henry-Vian C., Vian A., Davies E., Ledoigt G., and Desbiez M.O., 1995. Wounding regulates polysomal incorporation of hsp70 and tch1 transcripts during signal storage and retrieval. Physiologia Plantarum, 95(3), 387-392.

Lee D., Polisensky D.H., and Braam J., 2005. Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. New Phytologist, 165(2), 429-444.

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

McCormack E. and Braam J., 2003. Calmodulins and related potential calcium sensors of Arabidopsis. New Phytologist, 159(3), 585-598.

McCormack E., Tsai Y.C., and Braam J., 2005. Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci., 10(8), 383-389.

Migliaccio F., Tassone P., and Fortunati A., 2013. Circumnutation as an autonomous root movement in plants. Am. J. Bot., 100(1), 4-13.

Monshausen G.B., Bibikova T.N., Weisenseel M.H., and Gilroy S., 2009. Ca2+ regulates reactive oxygen species production and ph during mechanosensing in Arabidopsis roots. Plant Cell, 21(8), 2341-2356.

Monshausen G.B. and Gilroy S., 2009a. The exploring root – root growth responses to local environmental conditions. Current Opinion Plant Biology, 12(6), 766-772.

Monshausen G.B. and Gilroy S., 2009b. Feeling green: mechanosensing in plants. Trends in Cell Biol., 19(5), 228-235.

Okada K. and Shimura Y., 1990. Reversible root-tip rotation in Arabidopsis seedlings induced by obstacle-touching stimulus. Science, 250(4978), 274-276.

Oliva M. and Dunand C., 2007. Waving and skewing: how gravity and the surface of growth media affect root development in Arabidopsis. New Phytologist, 176(1), 37-43.

Qi B. and Zheng H., 2013. Modulation of root-skewing responses by KNAT1 in Arabidopsis thaliana. The Plant J., 76(3), 380-392.

Richter G.L., Monshausen G.B., Krol A., and Gilroy S., 2009. Mechanical stimuli modulate lateral root organogenesis. Plant Physiology, 151(4), 1855-1866.

Rutherford R. and Masson P.H., 1996. Arabidopsis thaliana sku mutant seedlings show exaggerated surface-dependent alteration in root growth vector. Plant Physiology, 111(4), 987-998.

Silverberg J.L., Noar R.D., Packer M.S., Harrison M.J., Henley C.L., Cohen I., and Gerbode S.J., 2012. 3D imaging and mechanical modeling of helical buckling in Medicago truncatula plant roots. Proc. National Academy of Sciences, 109(42), 16794-16799.

Sistrunk M.L., Antosiewicz D.M., Purugganan M.M., and Braam J., 1994. Arabidopsis tch3 encodes a novel Ca2+ binding-protein and shows environmentally-induced and tissue-specific regulation. Plant Cell, 6(11), 1553-1565.

Tamura W., Hidaka Y., Tabuchi M., Kojima S., Hayakawa T., Sato T., Obara M., Kojima M., Sakakibara H., and Yamaya T., 2010. Reverse genetics approach to characterize a function of NADH-glutamate synthase1 in rice plants. Amino Acids, 39(4), 1003-1012.

Telewski F.W., 2006. A unified hypothesis of mechanoperception in plants. Am. J. Bot., 93(10), 1466-1476.

Thompson M.V. and Holbrook N.M., 2004. Root-gel interactions and the root waving behavior of Arabidopsis. Plant Physiology, 135(3), 1822-1837.

Tsai Y.-C., Delk N.A., Chowdhury N.I., and Braam J., 2007. Arabidopsis potential calcium sensors regulate nitric oxide levels and the transition to flowering. Plant Signaling Behavior, 2(6), 446-454.

Wang Y., Wang B., Gilroy S., Chehab E.W., and Braam J., 2011. CML24 is involved in root mechanoresponses and cortical microtubule orientation in Arabidopsis. J. Plant Growth Regulation, 30(4), 467-479.

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

International Agrophysics

The Journal of Institute of Agrophysics of Polish Academy of Sciences

Journal Information


IMPACT FACTOR 2017: 1.242
5-year IMPACT FACTOR: 1.267

CiteScore 2018: 1.44

SCImago Journal Rank (SJR) 2018: 0.399
Source Normalized Impact per Paper (SNIP) 2018: 0.891

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 203 154 16
PDF Downloads 88 80 7